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MOSBY ELSEVIER

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HAND FUNCTION IN THE CHILD: FOUNDATIONS FOR REMEDIATION Copyright © 2006,1995 by Mosby Inc.

ISBN-13: 978-0323-03186-8 ISBN-I0 : 0-323-03186-2

All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permissions may be sought directly from Elsevier's Health Sciences Rights Department in Philadelphia, PA, USA: phone: (+1) 215 239 3804, fax: (+1) 215 239 3805, e-mail: [email protected]. You may also complete your request on-line via the Elsevier homepage (http:/ /www.elsevier.com) . by selecting ' Customer Support' and then 'Obtaining Permissions'.

Notice Neither the Publisher nor the Editors assume any responsibility for any loss or injury and/or damage to persons or property arising out of or related to any use of the material contained in this book. It is the responsibility of the treating practitioner, relying on independent expertise and knowledge of the patient, to determine the best treatment and method of application for the patient. The Publ isher

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CONTRIBUTORS Dorit Haenosh Aaron, MA, OTR, CHT, FAOTA Coordinator Hand Therapy Fellowship Department of Occupational Therapy Texas Women’s University Houston, Texas Mary Benbow, MS, OTR Private Consultant and Lecturer La Jolla, California Jane Case-Smith, EdD, OTR/L, FAOTA Professor Division of Occupational Therapy The Ohio State University School of Allied Medical Professions Columbus, Ohio Sharon A. Cermak, EdD, OTR/L, FAOTA Professor of Occupational Therapy Department of Rehabilitation Sciences Boston University, Sargent College; Director of Occupational Therapy Training Leadership and Education in Neurodevelopment Disabilities Children’s Hospital and University of Massachusetts Medical Center Boston, Massachusetts Ann-Christin Eliasson, PhD, OT Associate Professor Neuropsychiatric Research Unit Institution of Woman and Child Health Karolinska Institute Stockholm, Sweden

Charlotte E. Exner, PhD, OTR/L, FAOTA Professor Department of Occupational Therapy and Occupational Science Dean College of Health Professions Towson University Towson, Maryland Kimberly Brace Granhaug, OTR, CHT Clinical Manager Sports Medicine and Rehabilitation Christus St. Catherine Katy, Texas Anne Henderson, PhD, OTR Professor Emeritus Department of Occupational Therapy Boston University/Sargent College of Allied Health Professions Boston, Massachusetts Elke H. Kraus, PhD, BSc.Occ.Ther., Dip.Ad.Ed Professor of Occupational Therapy Alice-Saloman University of Applied Sciences Berlin, Germany Carol Anne Myers, MS, OTR/L Occupational Therapist Early Childhood Education Program Newton Public Schools Newton, Massachusetts Charlane Pehoski, ScD, OTR/L, FAOTA Consultant Eunice Kennedy Shriver Center University of Massachusetts Medical School Waltham, Massachusetts

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Ashwini K. Rao, EdD, OTR Assistant Professor of Clinical Physical Therapy Program in Physical Therapy Department of Rehabilitation Medicine Columbia University New York, New York

Scott D. Tomchek, MS, OTR/L Chief of Occupational Therapy Child Evaluation Center University of Louisville School of Medicine Department of Pediatrics Louisville, Kentucky

Birgit Rösblad, PhD, PT Associate Professor Community Medicine and Rehabilitation, Physiotherapy University of Umeå Umeå, Sweden

Laura K. Vogtle, PhD, OTR/L, ATP Associate Professor Department of Occupational Therapy University of Alabama at Birmingham Birmingham, Alabama

Colleen M. Schneck, ScD, OTR/L, FAOTA Professor and Post Professional Program Graduate Coordinator Department of Occupational Therapy Eastern Kentucky University Richmond, Kentucky James W. Strickland, MD Clinical Professor Indiana University School of Medicine Indianapolis, Indiana

Margaret Wallen, MA, OT Senior Occupational Therapist – Research Department of Occupational Therapy The Children’s Hospital at Westmead Westmead, New South Wales, Australia Jenny Ziviani, BAppScOT, BA, MEd, PhD Associate Professor School of Health and Rehabilitation Science The University of Queensland Queensland, Australia

PREFACE TO THE SECOND EDITION The everyday occupations that most of us engage in involve extensive use of our hands. As we perform these occupations we give little thought to the enormous variety of actions our hands can do. A hand can be a platform, a vise, or a hook. It can push and poke, pull and twist, scratch or rub. It can hold a football, an apple, or a raisin. It is the enabler of multiple tool uses. A major task of childhood is the development of this wide variety of hand actions. When a child’s hands are not functioning well or if there is a delay in development, the occupations of childhood are affected, such as playing with objects, dressing, and using tools such as spoons, scissors, or pencils. Remediation of the hand is therefore a major focus of intervention. Hand Function in the Child originally grew out of the recognition that there was a significant gap in the professional literature addressing the problems of hand dysfunction in children, despite the importance of the hand to the child’s development. It has been 10 years since the first edition was published and it still remains the only complete text covering this topic. This second edition again reviews detailed information on the neurological, structural, and developmental foundations of hand function in children. We maintain the focus on the hand as a tool for action and an organ of accomplishment and highlight the complexity of skilled hand use and the long developmental period needed for its perfection. As many of the chapters review information from rapidly changing fields of study, an important purpose of the revised edition was to update these chapters. Another purpose was to add chapters in several areas of content that we felt to be important. The content is presented in three parts. The first part, “Foundation of Hand Skills,” provides information on the anatomical, neurological, physiological, and psychological aspects of hand function. This section begins with an updated chapter on control within the central nervous system that describes the mechanisms that allow skilled use of the hand as it relates to handobject interaction. This is followed by a chapter on the embryology, anatomy, kinesiology, and biomechanics

of the hand. The third chapter explores sensory control and the way in which the control of grasp and lifting of objects varies with differing sizes, shapes, and textures. The next chapter examines the development and evaluation of the ability of infants and children to recognize objects and object properties felt by the hand. The fifth chapter updates the research on the role of vision in the control of movements in the environment, and covers the development of visual control in childhood. The final chapter in Part I is new in this edition and highlights the cognitive processes required for the acquisition and performance of hand skills. Part II, Development of Hand Skills, explores the changes in hand skills that occur with age. The first chapter on the early development of grasp, release, and bimanual activities has been revised to present the content in the context of infant play from birth to 2 years. The second chapter examines object manipulation from birth throughout childhood. Chapter 9, on handedness and its development, is new and includes an extensive review of research on hand preference as well as on the evaluation of hand preference. Chapter 10, on the development of self-care activities in relation to the development of hand skills, contains additional information on current measures and on cultural influences. The final chapter in Part II has a new, extensive review of recent research on handwriting. Therapeutic intervention is presented in Part III. The chapters focus on the overall remediation of hand skills, on the remediation of special problems, and on specific areas of intervention. Chapters 12 and 15 have been updated and revised. The remaining six chapters in this section are new. Chapter 13 presents ideas on how the engage the preschool child in hand activity and to incorporate treatment activities into the classroom. The next chapter reviews problems related to handwriting difficulties and presents formal and informal assessments. Chapters 16, 17, and 18 focus on specific areas of dysfunction and intervention. We chose a review of research on the effectiveness of improving hand function for the final chapter.

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Our primary vision continues to be to present in a single text current information on the neurological foundations of hand skills, the development of hand skills, and intervention for children with problems related to hand skills. We hope that a comprehensive review of the hand will provide an important resource and clinical guide for students, practicing pediatric therapists, and others who work with children.

ACKNOWLEDGMENTS The editors wish first to acknowledge with gratitude the time and expertise donated by the contributors to this volume. These authors are highly regarded in their respective fields, and we thank them for their insights and the wealth of practical and theoretical understanding they bring through their chapters. We hope that the diversity of ideas presented here will enrich the reader’s understanding and appreciation of the immense complexity and the multiple dimensions of the human hand and particularly of its importance to daily living from birth through adolescence. This book is the culmination of the efforts of many people who contributed ideas over an extended period of time. The formal beginnings of the book occurred during a series of workshops for occupational and physical therapists funded by the Maternal and Child

Health Bureau, U.S. Department of Health and Human Services, Department of Public Health. The workshops were sponsored by the Occupational Therapy and Physical Therapy Departments at the University of Illinois at Chicago between 1988 and 1991. Several of the contributors to the first edition participated in yearly task groups on the hand of the child, motivated by the need to share information in a field where so little had previously been written. It was from these meetings that the idea of a comprehensive book on hand skills in children arose. The reception of the first edition by many professional colleagues and their comments helped shape this second edition. We would also like to acknowledge the help and assistance of Kathy Falk, our editor at Elsevier, whose support enhanced all the phases of the production of this book by answering our questions and providing a workable and timely schedule. Thanks also to Sarah Wunderly, our production manager, and other Elsevier staff for assisting in the final phase of our work. Finally we want to recognize the families and children we and our authors have known through our professional practice and research for they have contributed much to our current knowledge of hand function in the child. Anne Henderson Charlane Pehoski

PREFACE TO THE FIRST EDITION …[M]an though the use of his hands, as they are energized by mind and will, can influence the state of his own health. (Reilly, 1962, p.2)

The hand is our primary means of interaction with the physical environment, both though the dexterous grasp and manipulation of objects and as the enabler of multiple tool functions. The enormous variety of actions accomplished by our hands ranges from the practical to the creative. The hand is incredibly versatile. It can be a platform, a hook, or a vise. It can hold a football, a hammer, or a needle. It can explore objects, express emotion, or communicate language. The hand is the subject of this book, most specifically the hand as a tool for action, as an organ of accomplishment. The motor functions of the hand are some of the most complex and advanced of all human motor skills. Hand use is voluntary, under the control of the conscious mind, and is regulated by feedback from sensory organs. The complexity of skilled hand use is shown by the long developmental period needed for its perfection. The ability to manipulate objects with the efficiency and precision of an adult continues to improve throughout late childhood and early adolescence. The plan for this book grew out of the recognition that, although the treatment of hand dysfunction has been a critical area of occupational therapy practice since the beginning of the profession, for many years the professional literature in pediatrics placed a greater emphasis on the neurophysiology and development of gross motor abilities than on manipulative skills. A renewed attention to manipulative abilities, beginning about 15 years ago, was spearheaded by the writings of therapists such as Rhonda Erhart, Reggie Boehm, and Charlotte Exner, and professional literature on the developmental treatment of hand skills has since increased. During a similar period there has been increasing research attention in the fields of neurophysiology and psychology to the motor skills of the hand. Although there are many unresolved issues about hand devel-

opment and dysfunction in childhood, it seemed timely to review that which is currently known. This book is intended for the professional and student interested in the current research and treatment of problems in children’s hand skills. The text is organized around themes from neurobehavior and development, drawing together information that is pertinent to the understanding of dysfunction in the hand in children and as a guidance to intervention. Hand function is reviewed from the perspectives of neurophysiology, neuropsychology, cognitive psychology, developmental psychology, and therapeutic intervention. The text is organized into three sections, each of which presents several dimensions of hand function. Section I includes chapters on the biologic and psychologic foundations of hand function. The first chapter describes the cortical control of skilled hand use and identifies the properties of that control that are different from the control of gross motor skills. The second chapter presents the anatomic structure and function of the hand facilitating the varied functions. Two chapters on the sensory guidance of the hand function follow, one on touch and proprioception and the other on vision. The other two chapters in Section I review knowledge from several branches of psychology, including the perceptual functions of the hand and the role of cognition in hand activity. Section II focuses on development in both general and specific areas of hand skill. Two chapters in this section focus on the development of basic skills. The first reviews research on the development of grasp, release, and bimanual skills in infancy and the second the development of object manipulation. Other chapters cover specific and complex skill areas of graphic skill and self-care and the development of hand dominance.

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Section III provides knowledge from selected pediatric clinical practice areas. Two of the five chapters describe dysfunction and treatment of special populations with cerebral palsy and Down syndrome. Another chapter presents the principles and practice of the remediation of hand skill problems, while a fourth focuses on the specific area of teaching handwriting. The remaining chapter identifies the many toys that are the natural media for the treatment of hand dysfunction in children. Despite the acceleration of research in the last decade, the study of the development of hand use and the treatment of hand dysfunction in children is still in its infancy. It is our hope that assembling this

information on hand skills will stimulate interest in the development of research programs that will increase the body of knowledge about normal and deviant hand skill development and the efficacy of intervention. This text was written primarily for pediatric occupational therapists and could serve as a graduate level text or as a reference book in entry level education. However, we anticipate that it will be of value for anyone working with toddlers and children, including preschool and elementary teachers, special educators, early intervention providers, and other therapists. Anne Henderson Charlane Pehoski

Chapter

1

CORTICAL CONTROL OF HAND-OBJECT INTERACTION Charlane Pehoski

CHAPTER OUTLINE MOVING THE FINGERS INDEPENDENTLY: DIRECT CORTICOSPINAL CONNECTIONS TO ALPHA MOTOR NEURONS OF THE HAND AND PRIMARY MOTOR CORTEX Direct Corticospinal Connections to Alpha Motor Neurons of Hand Muscles Primary Motor Cortex Use-Dependent Organization of the Primary Motor Cortex SENSORY GUIDANCE OF HAND MOVEMENTS: PRIMARY SOMATOSENSORY CORTEX Cortical Organization of the Somatosensory System Use-Dependent Organization Within the Primary Somatosensory Cortex Role of Somatosensory Input in Grasp Role of Somatosensory Cortex in Motor Learning THE TRANSFORMATION OF VISUALLY OBSERVED CHARACTERISTICS ABOUT OBJECTS INTO APPROPRIATE HAND CONFIGURATIONS: POSTERIOR PARIETAL LOBE AND VENTRAL PREMOTOR CORTEX Role of the Inferior Parietal Lobe in Preshaping of the Hand Role of the Ventral Premotor Cortex in Preshaping of the Hand Use-Dependent Organization of the Inferior Parietal and Ventral Premotor Cortex The Inferior Parietal Cortex and Tool Use SUMMARY AND THERAPEUTIC IMPLICATIONS

When I first met Katie she was 6 years old and was having a great deal of difficulty managing the fine motor tasks typical of most kindergarten children. She was clumsy and had difficulty with such tasks as buttoning and using tools. Her score on the Peabody Developmental Fine Motor Scales was −2.33 standard deviations below the mean for her age and her age equivalent score was 3 years 6 months. This is not an unusual profile for children referred because of poor fine motor skills. What was unique about Katie was that the source of her difficulty was known. A benign tumor had been removed from her right posterior parietal lobe when she was 3 years old. Many of the difficulties she experienced in hand–object interaction could be attributed to the location of her lesion. For example, she was underresponsive to tactile input and often used excess force when holding objects. When asked to feel forms placed in her hand without looking, she just grasped them and did not explore them with her fingers. She had a great deal of difficulty in tasks that required “in-hand manipulation,” such as moving a small object from the palm of the hand to the fingers. Objects often were dropped. This chapter discusses the posterior parietal lobe and its importance for hand–object interaction. However, this is not the only important area; other cortical regions are also explored. The capacity to use the hand with skill in hand– object interactions represents an evolutionary ability characteristic of the behavior of higher primates. Three fundamental prerequisites are necessary for this function: (a) the capacity for independent control over the fingers, (b) a sophisticated somatosensory system to guide finger movements, and (c) the ability to transform sensory information concerning object properties into appropriate hand configurations (Binkofski et al., 1999). Each of these prerequisites is served by separate

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Part I • Foundation of Hand Skills

but interconnected areas of the cerebral cortex. This includes the primary motor cortex, primary somatosensory cortex, parietal cortex (particularly the area around the intraparietal sulcus), and premotor cortex (particularly the ventral portion). That is not to say that other motor structures, such as the supplementary motor areas, cingulated motor areas, cerebellum, and basal ganglion do not also serve important functions (e.g., Ehrsson, Kuhtz-Buschbeck, & Forssberg, 2002; Lemon, 1999; Schlaug, Knorr & Seitz, 1994), but rather that the cortical regions mentioned previously seem critically related to skilled action of the hand, particularly as it interacts with objects. This chapter reviews each of the mentioned prerequisite skills and the cortical areas important for their functions. The purpose of this chapter is to better understand the problems of children like Katie and provide evidence for the need to encourage skilled hand use in these children.

MOVING THE FINGERS INDEPENDENTLY: DIRECT CORTICOSPINAL CONNECTIONS TO ALPHA MOTOR NEURONS OF THE HAND AND PRIMARY MOTOR CORTEX DIRECT CORTICOSPINAL CONNECTIONS TO ALPHA MOTOR N EURONS OF HAND M USCLES As indicated, one prerequisite for skilled hand use is the control over individual finger movements. This is true even for a seemingly simple task such as picking up an object using a precision grip.1 Try picking up a small object between your index finger and thumb. Pick it up slowly enough so you can observe the action of the fingers. Note the isolation of movement between the index finger and thumb and the movement of the remaining fingers as they get out of the way of the action. If, during this task, your hand muscles had been attached to an electromyograph (EMG) you would have seen that the muscles necessary for this task showed marked variation with respect to the precise timing of their onset and time course of activity during the task, resulting in the specificity of finger move1 This chapter uses the term “precision grip” when referring to the act of picking up a small object between the index finger and thumb because this is the term used in the neurophysiologic research that is reviewed.

ments. This is in contrast to a power grip, in which all the muscles are coactivated (Bennett & Lemon, 1996; Muir, 1985). Even simple finger movements such as this require hand muscles to work in a specific temporal order and with varying amounts of force (DarianSmith, Burman, & Darian-Smith, 1999). This ability to “fractionate,” or move the fingers individually, is thought to result from the special contribution of direct corticospinal connections primarily from neurons in the motor cortex to the alpha motor neuron of hand muscles in the ventral horn in the spinal cord (see Lemon, 1993, for a review). The ventral horn of the spinal cord is divided into two main sections, an interneuron zone and the motor neuronal pool or “final common pathway” to the muscle. The motor neurons in the ventral horn are not randomly distributed but are clustered into cell columns, a medial cell column that contains the motor neurons for the trunk, shoulder girdle, and hips, and a lateral cell column that contains motor neurons for the distal extremities (Kuypers, 1981). Almost all descending motor fibers first terminate in the interneuronal zone, so that there is at least one interneuron between the descending motor fiber and motor neuron. An important exception is the direct corticospinal fibers to alpha motor neurons of the distal extremity (Figure 1-1). This direct path is fast and thought to be important in moving the hand with speed and skill. These special connections also are thought to be preferentially related to the intrinsic hand muscles (Maier et al., 2002). The intrinsic hand muscles provide the ability to handle small objects with precision (Long et al., 1970). Direct corticospinal fibers seem to be a feature unique to

Corticospinal tract Direct corticospinal input Indirect corticospinal input

Interneuron zone

Muscle of distal extremity

Figure 1-1 Termination of the corticospinal tract in the spinal cord. The diagram shows a single fiber that synapses in the interneuronal zone and then makes connections with a muscle through the interneuron. Also shown is a fiber within the corticospinal tract that makes a direct connection to a motor neuron of a distal limb muscle.

Cortical Control of Hand-Object Interaction • 5 primates and are particularly well developed in the most dexterous primate species (Nakajima et al., 2000). Lemon (1993) suggests that the direct corticospinal projections allow motor commands to bypass spinal mechanisms and break up synergies by direct access to the motoneurons and the final common pathway. This allows the flexibility of individual finger movements with wrist actions appropriate to a given task.

PRIMARY MOTOR CORTEX Although a large number of structures are involved in the neural control of the hand, the importance of the primary motor cortex for the execution of independent finger movements is well established (Ehrsson et al., 2002; Huntley & Jones, 1991) (Figure 1-2). Neurons that are the source of the direct corticospinal connections are more numerous in the hand area of the primary motor cortex than connections from other cortical areas, such as the supplementary motor cortex (Lemon et al., 2002; Maier et al., 2002). This area of cortex is particularly well represented in nonhuman primates by the ability to form a precision grip. Damage to the motor cortex results in deficits in fine manual coordination. Monkeys with lesions to this area lose the ability to produce a precision grip and small objects are picked up by the use of a more mass grasp in which all the fingers work together (Fogassi et al., 2001; Rouiller et al., 1998; Schieber & Poliakov, 1998). Difficulty with independent finger movements can also be seen in humans with lesions restricted to the primary motor cortex or the corticospinal tract. Lang and Schieber (2003) found that the fingers of the affected hand in patients with damage to these areas moved less independently than the fingers of the uninvolved extremity or normal controls. This was particularly true for abduction and adduction of the fin-

Primary motor cortex Central sulcus

Figure 1-2

Diagram of the primary motor cortex.

gers. When EMG recordings were made of hand muscles during abduction and adduction movements of the fingers, activation of the first dorsal interosseous of the normal hand was seen only when the person moved the index finger. That is, the muscle’s response was isolated and only related to the movement of this one finger. In the disabled hand, this muscle was active with thumb, index, and ring finger movements. The authors concluded that cerebral areas and descending pathways that are spared in humans may activate finger muscles, but cannot fully compensate for the highly selective control provided by the primary motor cortex. The primary motor cortex has a particular relationship to the hand. The cortical representation of muscles involving the fingers occupies a larger area than those concerned with shoulder movement (Paillard, 1993). Hand muscles may also be more dependent on cortical mechanisms. Turton and Lemon (1999) used transcranial magnetic stimulation (TMS) to look at the effects of stimulation of the primary motor cortex on EMG output of the deltoid, biceps, and first dorsal interosseous muscles when the participants contracted each muscle. (TMS is a noninvasive way to stimulate neurons in the motor cortex using a small coil placed over the appropriate area of the head.) They found that the EMG response to this additional facilitation was significantly greater in the hand muscles than the biceps, which was greater than in the deltoid. That is, the “extra” input provided by the TMS through the primary motor cortex was greatest in the hand muscles. They suggest that this reflects a major difference in the dependence on cortical mechanisms in hand muscles as opposed to more proximal muscles. Therefore the hand seems to have a privileged relationship with the primary motor cortex.

USE-DEPENDENT ORGANIZATION OF THE PRIMARY MOTOR CORTEX One of the significant research findings in the last few years is that the functional organization of the primary motor cortex is dynamic and changes as a result of use. “Use-dependent” changes have been seen in the motor cortex of a wide variety of animals (e.g., Kleim et al., 1996; Remple et al., 2001), including humans (e.g., Classen et al., 1998; Pascual-Leone, Grafman, & Hallett, 1994). What appears to happen is that the representation of the “used” muscles expands or the movements that are used together are represented together (Nudo et al., 1996). There is not one representation of the human hand in the motor cortex; rather, multiple overlapping representations are functionally connected through a horizontal network between motor neurons (Butefisch, 2004; Huntley & Jones, 1991; Sanes & Donoghue, 2000). Dynamically

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changing patterns can be achieved by changing the strength of these horizontal networks through use (Butefisch, 2004). This is a requirement for motor learning. The brain must have the ability to adapt to new and changing circumstances, including both the learning of new skills and recovery from injury (Jackson & Lemon, 2001). An example of a “use-dependent” change was demonstrated by Karni et al. (1998). In this study, typical adults practiced a finger sequence task daily for 5 weeks (opposing the fingers of the nondominant hand to the thumb in a specific order). The participants also were given a second finger sequence that was not practiced and served as a control for the study. Functional magnetic resonance imaging (fMRI) of the cerebral cortex was done at the start of the experiment and then weekly until the end of the experiment. The authors found that in the initial images done before the experiment began there were no differences between the cortical representation of the experimental and control sequences. At 3 weeks, when the experimental sequence had been well learned, the area of motor cortex representing the experimental sequence had become larger. Changes also have been seen using intracortical microstimulation in monkeys, in which the neuronal representative of movements in the distal forelimb area of the primary motor cortex can be specifically mapped. In one study the extent of the representation of the hand was mapped and then the monkeys were trained to pick up small food pellets from a food well (Nudo et al., 1996). After training, intracortical microstimulation of the primary motor cortex was done again and the researchers found that the representation of the movements used in the food retrieval task had expanded. They also looked at the representation of unpracticed wrist and forearm movements, and found that the representation of these movements had contracted. To demonstrate that these changes are reversible and that the primary motor cortex changes are based on use, the monkeys were then trained to perform supination and pronation movements in a key turning task. Intracortical microstimulation demonstrated an expansion of the forelimb area and contraction of the digital representational zones. They also found that movement combinations used in the acquisition of these skilled motor tasks had come to be represented in the same cortical territory. Consequently, use of a particular motor pattern causes structural reorganization in the primary motor cortex. Actions that are practiced come to represent a larger area of cortex and the muscle groups involved also come to be represented together in what appear to be functional groupings (Nudo et al., 1996); however, not all “use” or practice may be as effective in driving these changes. As discussed later, passive movements and

strength training appear to be less effective in driving reorganization of the primary motor cortex. Alternately, skill training or learning may be a particularly powerful force for reorganization. With respect to passive movements, Lotze et al. (2003) used fMRI to look at the effects of 30 minutes of passive versus active wrist movement in typical adults. They found that the accuracy of wrist movements improved more with active movements and that cortical reorganization as measured by fMRI also was greater with active compared with passive movement. In a clever experiment that looked at the effect of strength training, Remple et al. (2001) trained one group of rats to break increasingly larger bundles of pasta with their forelimb and a second group to break single strands of pasta. A control group that had no training in either task also was included in the study. After 30 days of training, the researchers found an increase in the proportion of motor cortex occupied by distal forelimb movements in both experimental groups but not the control group. They concluded that the development of skilled forelimb movements, but not increased forelimb strength, is associated with reorganization of forelimb areas in the primary motor cortex. The need for the animal to be engaged in a skilled task or actually learn a task for significant changes in the primary motor cortex to be observed also has been reported. In two complementary studies, Nudo et al. (1996) and, Plautz, Miliken, and Nudo (2000), the researchers trained monkeys to retrieve food pellets from food wells. In one group, the well was large and therefore the task was fairly easy, so no skill or learning was involved (Plautz et al., 2000) (Figure 1-3). Another group of monkeys was required to use much smaller food wells that required learning to retrieve the food pellet (Nudo et al., 1996). Both groups used the same fingers and were given the same number of pellets to retrieve but only in the group of monkeys in which the task required learning a new skill was there evidence of modification of cortical maps. The authors concluded that, “Repetitive motor activity alone does not produce functional reorganization of cortical maps. Instead we propose that motor skill acquisition or motor learning is a prerequisite factor in driving representational plasticity in the primary motor cortex” (Plautz et al., 2000; p. 27).

Even adult patients who had reached a plateau in their recovery after suffering a stroke showed an increase in function (Taub & Morris, 2001) and expansion of the cortical hand representation (Liepert et al., 2000) after constraint induced movement therapy (noninvolved extremity restrained to force use of the involved extremity).

Cortical Control of Hand-Object Interaction • 7

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Figure 1-3 Depiction of a squirrel monkey performing a large pellet retrieval task. Note the relative simplicity of the task because of the size of the well compared with the size of the animal’s hand. (Redrawn from Plautz E, Miliken G, Nudo R [2000]. Effects of repetitive motor training on movement representation in adult squirrel monkeys: Role of use versus learning, Neurobiology of Learning and Memory, 74:27–55.)

Use can change the organization of the primary motor cortex, but disuse also can have an effect on centers important to motor skills. Using kittens, Martin et al. (2004) demonstrated that restricting the use of one paw for the first 7 weeks after birth created permanent changes both in the skill of that paw and the morphology of the direct corticospinal connections in the spinal cord. In another example, a group of researchers followed adults who had undergone surgical treatment of the flexor tendons of the hand (deJong et al., 2003). For 6 weeks after surgery, the patients were required to wear a dynamic immobilization splint that allowed passive but not active finger flexion. After the splint was removed, the patients complained of a temporary clumsiness of the hand that could not be explained by stiffness of the fingers or adhesions. In one patient, EMG studies were done after splint removal and flexion of the fingers showed increased cocontraction of the extensor muscles and no full relaxation of this muscle was seen between sets of movement. In four patients, positron emission tomography (PET) was used to look at task-related increases in cerebral blood flow as they flexed their fingers. These scans were done immediately after the splint was removed and again 6 to 10 weeks after removal. They found that scans immediately after splint removal demonstrated activation in the posterior parietal lobe and cingulate sulcus. This was not seen in the nonsurgical hand. The authors suggested that the increase in parietal involvement (an area of tactile and visual convergence discussed later in this chapter) may

be related to an increased demand on body scheme representation that is needed for instructing the appropriate parts of the hand to move. The cingulate may represent the recruitment of secondary motor function for the execution of simple hand movements. After the splint had been removed for several weeks, a second scan showed movements related to the putamen, a subcortical structure. The authors indicated that the shift from cortical to subcortical involvement may indicate that movements have been relearned. In summary, hand skill is possible because of the ability to move the finger individually and with speed. This ability is provided by the primary motor cortex and direct corticospinal fibers to hand muscles. The integrity of this cortical motor system is being tested in part when a child is asked to tap his or her index finger and thumb together as rapidly as possible or quickly oppose the individual fingers to the thumb. The speed with which these movements can be performed increases with age (e.g., Denckla, 1974). Evans, Harrison, and Stephens (1990) suggest that there is a relationship between a child’s ability to perform rapid finger movements and maturation of a cutaneomuscular reflex dependent on the corticospinal tract, as well as the main sensory pathway. The results of maturation in this system are demonstrated when an infant of 9 to 10 months begins to use a precision grip to pick up small objects (Siddiqui, 1995). It is apparent that the hand needs to be used, particularly in skilled tasks. This need for use also is seen for other cerebral areas involved in control of the hand, particularly the primary somatosensory cortex, which is discussed next.

SENSORY GUIDANCE OF HAND MOVEMENTS: PRIMARY SOMATOSENSORY CORTEX The hand is both a motor and sensing organ and there is a tight interplay between these two functions. The delicate movements of the hand and fingers are needed to “gather” sensory information, and those delicate movements need sensory feedback to guide action, particularly actions with objects. When objects are handled they do not fall from the fingers, nor does one use excessive force when picking things up. The information needed for these activities is provided by sensory feedback. The importance of this sensory information is obvious when one removes a glove to gather change from a pocket or when performing any delicate activity with the hand. Figure 1-4 shows the attempts of a woman with complete loss of sensation in her right hand trying to crumple a piece of paper (Jeannerod,

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Part I • Foundation of Hand Skills RH

LH

Michel, & Prablanc, 1984). Note the difficulty she has in coordinating the fingers of her right hand. She was reported to be able to reach for objects, eat normally, and write (although with difficulty), all tasks she could control using vision. Activities outside visual control, such as combing hair or buttoning, were problematic, as were activities that require the fingers to work together as in the paper-crumbling task. No detectable motor deficit, such as the ability to perform rapid tapping of the index finger, was noted (i.e., motor functions were intact). A computed tomography (CT) scan found that this woman had a very large lesion involving the somatosensory cortex and superior parietal lobe (Jeannerod, Michel, & Prablanc, 1984). (Note that this woman’s lesion extended beyond the primary sensory cortex and probably contributed to the severity of her disability). Figure 1-5 shows similar disorganization of finger movements in a monkey with a lesion in area 2 of the somatosensory cortex (Hikosaka et al., 1985). Brochier, Boudreau, and Smith (1999) also found a loss of finger coordination and poor positioning of the fingers when grasping objects in monkeys with inactivation of the somatosensory cortex. This section discusses the important roles sensory information plays in skilled hand movements, including the role it plays in motor learning.

CORTICAL ORGANIZATION OF THE SOMATOSENSORY SYSTEM

Figure 1-4 Schematic of a woman with a lesion in the somatosensory cortex and superior parietal lobe attempting to crumble a sheet of paper with her left hand (LH) and involved right hand (RH). (Redrawn from Jeannerod M, Michel M, Prablanc C [1984]. The control of hand movements in a case of hemianaesthesia following a parietal lesion. Brain, 107:899–920.)

The primary receiving area for somatosensory information from the limbs is the area of cortex just behind the central gyrus. This area generally is called the primary somatosensory cortex (Figure 1-6). It is the major termination of the dorsal columns, which carries discrete somatosensory information from the periphery. This major tract has evolved in parallel with the corticospinal tract, and like this system it reaches it highest level of development in humans (Paillard, 1993). Information carried in the dorsal columns can register even small movements of joints and provide knowledge of the exact location of stimulus on the skin. It was designed to provide specific information about what is happening in the periphery. In both monkeys (Sakata & Iwamura, 1978) and humans (Moore et al., 2000) the primary somatosensory cortex is composed of four areas, generally called Brodmann’s areas 3a, 3b, 1, and 2 (see Figure 1-6). An understanding of the function of the primary somatosensory area is helpful to appreciate the complexity of information processing within this area, particularly for the hand. Afferent fibers from the dorsal columns project mainly to area 3b for cutaneous input and area 3a for

Cortical Control of Hand-Object Interaction • 9

IPSI

CONTRA

Figure 1-5 Disruption of finger coordination after inactivation of area 2 in a monkey. The sequence of movements (left to right) shows the animal’s attempts at picking up a piece of apple from a funnel. IPSI indicates the “normal” hand ipsilateral to the inactivated region. CONTRA indicates the disorganized movements of the affected hand contralateral to the inactivated region. (Redrawn from Hikosaka O, Tanaka M, Sakamoto M, Iwamura Y [1985]. Deficits in manipulative behaviors induced by local injection of muscimol in the first somatosensory cortex of the conscious monkey. Brain Research, 325:375–380.)

deep, proprioceptive information (information arising from an activity such as active flexion and extension of the fingers) (Iwamura, 1998; Moore et al., 2000). Area 3b sends information to area 1 and area 1 sends information to area 2. Both areas then send information to the parietal lobe (Inoue et al., 2004). Therefore there is a serial or hierarchical processing of information across this area (Ageranioti-Belanger & Chapman, 1992; Inoue et al., 2004; Iwamura, 1998; Iwamura et al., 1985). One of the transformations in sensory information that is seen as information is processed in more posterior cortical regions is the response of a single neuron to stimulation over wider areas of skin. For example, there is an increase in the number of multidigit receptive fields (the area from which stimulation causes a single cortical neuron to fire) when progressing from area 3b, where 46% of neurons respond to multiple sites; to area 1, where the percentage is 63%; to area 2, where 85% of neurons respond to stimulation from multiple sites (Ageranioti-Belanger & Chapman, 1992). That is, the discrete information that first arises from the periphery appears to be combined into progressively more functionally relevant networks. In a study of neurons in area 2 of monkeys, Iwamura et al. (1985) suggested that this convergence represents skin surfaces that come in contact as the result of com-

mon behaviors of the animal. Like the primary motor cortex, which tends to cluster muscles that have repeatedly worked together in interconnected networks, the same appears to be true of sensory information processed in the primary somatosensory cortex. Also like the motor cortex, the organization of the sensory cortex is dependent on use. Therefore these two areas allow for a great deal of flexibility in how information is organized to best serve a variety of functional activities.

USE-DEPENDENT ORGANIZATION WITHIN THE PRIMARY SOMATOSENSORY CORTEX The primary sensory cortex is dynamic and changing. This has led one researcher to suggest that at any given time the details of the somatosensory cortex organization reflect the behavioral experience of the animal (Recanzone et al., 1992). That is, the sensory representation of the extremities contracts or expands depending on the use or lack of use of a body part. In an interesting study, Scheibel et al. (1990) did a postmortem examination of the dendritic complexity in several areas of the cerebral cortex in 10 individuals. The authors found a great deal of variability in the hand area of the somatosensory cortex of these individuals

10

Part I • Foundation of Hand Skills Central Sulcus

3a

3b 1 2 Primary somatosensory cortex

A

Central sulcus 2 1

B

3b

3a

Figure 1-6 A. Somatosensory cortex. B. Cross section of somatosensory cortex showing Brodmann’s areas 3a, 3b, 1, and 2.

and felt that at least in some (e.g., former typist, appliance repairman) these differences might be related to the individual’s premorbid occupation. In a more recent study, Hashimoto et al. (2004) used noninvasive techniques to study the somatosensory cortex in string players. They found an enlarged cortical representation of the hand area in these individuals compared with controls who did not play a string instrument. Like the motor cortex, research seems to indicate that skilled learning or attention to a task may be particularly effective in mediating these cortical changes. Using a behavioral task similar to the one used for studying the changes in the motor cortex of monkeys, animals were trained to pick up food pellets placed in wells of varying diameters (Xerri et al., 1999). This included large-diameter wells in which the pellets were easy to retrieve, and smaller-diameter wells in which retrieval was more difficult. The researchers found that sensory neurons responsive to the specific finger surfaces that had been engaged in the small retrieval task showed major representative changes within area 3b of the somatosensory cortex that were not seen with other finger surfaces. That is, changes reflected digital surfaces that were necessary for object retrieval under

difficult task conditions or in which the animal had to learn a skilled task. In another study, Recanzone et al. (1992) trained two groups of monkeys to place their hands on a mold of the hand. The purpose of the mold was to keep the hand in the same position so a vibratory stimulus could be given to a small site on one of the fingers. One group of animals was trained to lift the hand when they perceived changes in the vibratory input. In other words, these monkeys were to attend to and then make an adaptive response to this tactile stimulus. Another group of monkeys also received the vibratory stimulus but were trained to lift the hand to changes in an auditory stimulus. These animals therefore received the vibratory stimulus in a passive manner and were not required to act on the input. When the area in the primary sensory cortex of these animals that represents the stimulated portion of skin was mapped, both experimental animals showed an increase in the representation of this skin area. However, the increase in the animal who had been the passive recipient of the vibratory stimulus was modest. The authors suggest that attention influences cortical reorganization and that stimulation alone is far less effective in driving cortical reorganization than an active response to the stimulus. In other words, being engaged in the activity and making an adaptive response based on sensory input were the most efficient means of driving the cortical changes seen in this study. It also should be mentioned that in humans, Godde, Ehrhardt, and Braun (2003) showed a 20% decrease in two-point thresholds on the tip of the index finger and a change in the cortical map of this finger after 3 hours of intermittent, purely passive tactile stimulation to the fingertip. Apparently passive input also can promote organizational changes in the primary somatosensory cortex along with some modest improvement in tactile discrimination.

ROLE OF SOMATOSENSORY I NPUT IN G RASP Tactile information from the fingers is necessary to adjust the grip to the weight and friction of an object. This is particularly true when picking up a small object in the fingertips. Sensitive tactile receptors in the fingertips are able to sense the “slip” of an object even before this slip comes to conscious attention. Appropriate adjustments in the grip then can be automatically made (Johansson & Westling 1984, 1987; Westling & Johansson, 1984). If the friction between the finger and objects is different for different fingers, these differences are monitored separately (Edin, Wrestling, & Johansson, 1992). That is, if one side of an object is covered with silk and contacted by the index finger and

Cortical Control of Hand-Object Interaction • 11 the other side of the object is covered with sandpaper and contacted by the thumb, each finger adjusts to the frictional conditions on its grip surface. Anesthesia of the fingers results in an increase in the dropping of objects (particularly small and slippery objects) and the application of significantly greater grip forces (Augurelle et al., 2003; Monzee, Lamarre & Smith, 2003; Westling & Johansson, 1984). The “just right grip,” which includes just enough margin of safety so the object will not be dropped, is lost. Anesthesia of the fingers also appears to prevent the exact alignment of the fingers on the object surface. Monzee, Lamarre, and Smith (2003) found that although these misalignments were too small to be visually apparent, they still caused enough of a tangential force so that the measured grip forces were close to the slip point. Therefore sensation from the fingers not only allows the application of appropriate grip forces and adjustments to small slips, this information also appears to help placement of the fingers to the most appropriate position for a secure grip. Because accurate sensory information is necessary for calibrating the “just right” grip force, children with reduced sensation in the hand, such as Katie, might have difficulty modulating grip and therefore manipulating small objects. This reduction in sensation has been found in children with cerebral palsy (see Eliasson, this volume), as well as children with developmental coordination disorders and attention deficit disorder (Pereira et al., 2001). Differences in establishing the “just right” grip also might be suspected in children with Down syndrome who have been shown to have impaired peripheral somatosensory function in the upper extremity (Brandt, 1996; Brandt & Rosen, 1995). Even in young children, the ability to adjust the grip force to the “just right” level is problematic. Young children, particularly those 4 years or younger, tend to use significantly larger grip forces when compared with adults (Forssberg et al., 1991). This may be one reason why an in-hand manipulation task such as moving a small peg from the palm to the fingers or turning a peg over in the fingers is difficult for children 4 years of age and younger (Pehoski, Henderson, & Tickel-Degnen, 1997a,b). This was a difficult task for Katie; she often dropped the manipulated object.

ROLE OF SOMATOSENSORY CORTEX IN MOTOR LEARNING Area 2 in the primary sensory cortex is connected to the primary motor cortex through corticocortical connections (Asanuma & Pavlides, 1997). Sensory information from the hand may be important to learn a new motor skill but not to retain a skill already learned. For

example, Pavlides, Miyashita, and Asanuma (1993) had monkeys learn a new motor task, but with each of the two hands subject to different conditions. In the first condition, the somatosensory cortex to one hand was lesioned. When the monkey had recovered from surgery, both hands were trained to retrieve food pellets falling at various velocities from a dispenser. The authors found that the hand contralateral to the lesion had difficulty learning the task and even when learned, never achieved the skill of the “normal” hand. In the second condition or experiment, the primary sensory cortex to the “normal” hand was lesioned. Despite this damage, the ability to perform the task with this hand remained. The authors concluded, “The corticocortical projections from the somatosensory to the motor cortex play an important role in learning new motor skills, but not in the execution of existing motor skills” (Pavlides, Miyashita, & Asanuma, 1993, p. 733). Practicing a task produces a vigorous circulation of impulses among the peripheral sensory inputs, somatosensory cortex, and primary motor cortex (Asanuma & Pavlides, 1997; Nadler, Harrison, & Stephens, 2000; Stefan et al., 2000). This specific input from the primary somatosensory cortex to the motor cortex is said to serve as a “teacher” (Asanuma & Pavlides, 1997). The “teacher” informs the motor cortex of the results of a movement so that eventually the exact combination and sequence of muscles needed for the task can be selected. Everyone has experienced clumsiness when learning a new skill. The movements are not smooth and unnecessary movements (and therefore muscles) are used when performing the task. As the task is practiced, these unnecessary movements are eliminated and an efficient, reproducible series of actions is seen. Try this activity. Pick up a pencil with your preferred hand with the fingers close to the eraser end rather than the writing end. Now move your fingers up the pencil shaft until they are in the proper position for writing. Try the same activity with your nonpreferred hand. Did you note a marked difference in the skill of this task on the two sides? Was the nonpreferred side awkward and clumsy? A possible interpretation of the study by Asanuma and Pavlides (1997) is that practice is one of the differences between the two hands in this task. The nonpreferred hand has not had an opportunity for sensory feedback to “teach” the motor cortex how to do the task most efficiently. It is not hard for people to understand how important sensory feedback is to hand function. Everyone has experienced the frustration of picking up a small object from the table with a Band-Aid covering the distal pad of one finger. Just think of how clumsy skilled motor acts of the hand would be if this reduction in sensation

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Part I • Foundation of Hand Skills

were experienced throughout the entire hand. One would have difficulty moving the fingers with skill and adjusting the hand to the “just right” grip so objects are not dropped.2 There might even be some difficulty learning a new motor task with the hands. Nonetheless actual engagement with objects is more complicated than just picking them up so they do not drop or manipulating them within the hand. This is particularly true for tool use. Preparation for grasp occurs even before the object is touched and is based on the observed characteristics of the object and the use that will be made of the object. Consideration of the posterior parietal lobe and connection with the premotor cortex is covered next.

THE TRANSFORMATION OF VISUALLY OBSERVED CHARACTERISTICS ABOUT OBJECTS INTO APPROPRIATE HAND CONFIGURATIONS: POSTERIOR PARIETAL LOBE AND VENTRAL PREMOTOR CORTEX Think for a moment what it would be like if one had an excellent mechanism for the control of finger movements and somatosensory feedback to guide the movements but did not have a mechanism for selecting the grasp appropriate for a particular object. There would be a lot of trial and error. Movements would be slow. A glass would be approached in the same way as a fork. The hand would land on an object and then “feel” for the appropriate grasp. One function that would help would be vision. Up until now vision has not been considered. The primary motor cortex has limited access to direct visual information (Jeannerod et al., 1995). Vision allows for the preparation of grasp before contact; therefore the hand could be preshaped to match objects of different shapes, sizes, and orientation. Any final adjustments could be made by somatosensory feedback on contact. This preshaping of the hand is one of the functions provided by a posterior parietal cortex–prefrontal lobe cortex circuit.

2

It should be noted that besides the neural mechanisms responsible for the “just right” grip, there are other ways to increase the friction at the finger–object interface, the oils or moisture of the fingers themselves. Washing and drying the hands (Johansson & Westling, 1984) or the introduction of chemicals that reduce sweating of the hands (Smith, Codoret, & St-Amour, 1997) cause an increase in the grip force.

ROLE OF I NFERIOR PARIETAL LOBE IN PRESHAPING OF THE HAND Almost all interactions with objects start with a reach. Reach is composed of two main parts, the transport of the hand and the preparation of the hand for grasp (see Rosblad, this volume). Each of these requires different visual information about the object. Reach requires the analysis of distance and direction. Preparation of the hand for grasp requires the analysis of the object’s shape, size, and orientation (Jeannerod et al., 1995). Try this: Place two objects of different sizes on the table, such as a paper clip and the box the paper clip comes in, then reach for each one. Note the difference in the hand opening for the larger as opposed to the smaller object. As the hand is brought toward the object, the fingers open to ready the hand for grasp, and this opening is calibrated to the size of the object to be grasped, although it is always a bit larger than the object itself (Jeannerod, 1981). Here is another activity. With one hand, hold a pencil out in front of you and reach for it with the other hand while the pencil is held in a vertical position and then with the pencil in a horizontal position. Did you rotate your forearm during the reach to accommodate the difference in orientation of the pencil (e.g., “thumb up” for the vertical position and “thumb down” for the horizontal position)? Not only is the hand opening “programmed” as a part of the reach, but forearm rotation and wrist position also are part of the pattern of the reach. All of this preparation ensures that a secure grasp is achieved once contact with the object is made (Jeannerod et al., 1995). The ability to scale the hand opening and orient the hand appropriately to an object is not seen in young infants. Changes to the orientation of the wrist or forearm to an object is seen at about 7 to 9 months of age (Lockman, Ashmead, & Bushnell, 1984; Morrongiello & Rocca, 1989; von Hofsten & FazelZandy, 1984; McCarthy et al., 2001) and adjusting the opening of the hand to changes in an object’s size at about 9 months of age (von Hofsten, 1979, 1991; von Hofsten & Ronnquist, 1988). The transformation of the visual image of an object into an appropriate hand opening and orientation is processed in the posterior parietal lobe. In a study of reach and grasp in monkeys, the timing of the firing of neurons in the posterior parietal lobe was compared with those of the primary somatosensory cortex (Debowy et al., 2001). The researchers found that the neurons in the posterior parietal lobe were more active during the approach stage as the hand was preshaped and before the hand touched the object. Most of the somatosensory neurons fired on contact with the

Cortical Control of Hand-Object Interaction • 13 object. Contact appeared to be the transition point from visually guided behavior to tactile guidance of the action. The posterior parietal lobe is composed of two parts, the superior and inferior parietal lobes (Figure 1-7). It is an important center for the integration of sensory information, particularly somatosensory and visual information. With respect to somatosensory input, this area completes the hierarchical processing of this information that started in the primary somatosensory cortex. The superior parietal lobe receives information from area 1 and more strongly from area 2 in the primary somatosensory cortex (Hyvarinen, 1982). The inferior parietal lobe’s sensory representation is more complex than the superior parietal lobe because it not only receives information from areas 1 and 2 and the superior parietal lobe, it also receives a great deal of information from the visual cortex; therefore this is an area where visual and somatosensory information converge (Hyvarinen, 1982; Mountcastle et al., 1975). Within the inferior parietal lobe is an area that has recently attracted much attention, the anterior intraparietal sulcus (see Figure 1-7). In this area are neurons related to grasping that fire preferentially to the shape, size, and orientation of objects (Sakata et al., 1995, 1999; Taira et al., 1990). Patients with lesions in this area have no difficulty in reaching but hand shaping is significantly disturbed and often there is no preshaping of the hand at all (Binkofski et al., 1998). Monkeys with reversible inactivation of this area also have difficulty grasping. Grasping in these animals often is achieved only after several corrections that rely on tactile feedback (Gallese et al., 1994). Binkofski et al. (1999) found neurons in the intraparietal sulcus active (along

Central sulcus

Primary somatosensory cortex Superior parietal lobe

with the ventral premotor area, superior parietal lobe, and secondary sensory cortex) when imaging studies were done of typical adults manipulating complex objects in their hands.

ROLE OF THE VENTRAL PREMOTOR CORTEX IN PRESHAPING OF THE HAND Registering information about an object’s size, shape, and orientation is important, but the parietal lobe is primarily a sensory area and this information must be transferred from sensory to motor areas for use in actual movement execution. The anterior interparietal sulcus has corticocortical connections with the ventral premotor area (Luppino et al., 1999) (Figure 1-8). The “description” of the object is used here to select the most appropriate grip. Neurons in the ventral premotor cortex area of monkeys, such as those in the anterior parietal sulcus, are selective in the type of objects that cause them to fire (Rizzolatti et al., 1988). In monkeys, many neurons in this area can be classified by their action (e.g., grasping, holding, tearing, or manipulating); grasping neurons are most represented. Many also are selective to the type of prehension used, such as a precision grip, finger prehension, or whole hand prehension. (These grips are the three most common grips seen in monkeys [Fadiga & Craighero, 2003].) Some neurons in this area are specific for different finger configurations within a grip type. They are also selective to what part of the grip movement they fire. Some discharge during the whole action with the object, others during finger closure, and others after contact with the object; therefore these neurons form a “vocabulary”

Primary motor cortex Ventral premotor cortex

Central sulcus

Intraparietal sulcus

Inferior parietal lobe

Figure 1-7 Diagram of the intraparietal sulcus dividing the superior parietal lobe and inferior parietal lobe.

Figure 1-8 Diagram of ventral premotor area and relationship to primary motor cortex.

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Part I • Foundation of Hand Skills

of possible actions the hand can take on an object (see Rizzolatti & Fadiga, 1998, for a review). This vocabulary is related more to the goal of an action than to individual movements (e.g., a specific neuron might fire to “grasping” with the mouth and also with either hand) (Rizzolatti et al., 1988; Rizzolatti & Fadiga, 1998). The ventral premotor cortex is connected to the primary motor cortex and from there to the direct corticospinal fibers to hand muscles (Luppino et al., 1999). What differentiates the primary motor cortex from the ventral premotor cortex is that the latter stores motor schemata that are goal directed, whereas the primary motor area stores movements regardless of the action or context in which they are used (Rizzolatti & Fadiga, 1998). That is, the visual information processed in the anterior intraparietal sulcus about the three-dimensional characteristics of an object is sent to the ventral premotor cortex for the selection of grip and then to the motor cortex for sequencing of the actual muscles to be used. Neurons in the inferior premotor area are known to facilitate neural action in the primary motor cortex. Stimulation of a neuron in the hand area of the primary motor cortex of monkeys causes changes in the EMG reading from hand muscles, but stimulation of an inferior premotor neuron or inferior parietal neuron alone does not. If stimulation is first given to the premotor cortex and then to the primary motor cortex, the EMG hand muscle response is greater than when the motor cortex is stimulated alone. The authors indicate that this input might be part of the wider control system that helps shape the pattern of activity of different hand muscles for grasp of specific objects (Shimazu et al., 2004). If a small injection of an agent that temporarily inactivates neurons is placed in the ventral premotor cortex of monkeys, the results are similar to those seen with inactivation of the anterior interparietal sulcus. That is, the animal is able to use tactile feedback to succeed in an appropriate grasp when preshaping of the hand is absent, but only after contact with the object, This is particularly true for small objects (Fogassi et al., 2001). It is interesting that large lesions at this site also produced problems with hand shaping of the ipsilateral hand. Further, when monkeys with large lesions were presented with raisins placed in a board with two rows of six horizontally placed holes, the monkeys tended to pick up the raisins in the right holes with the right hand and those on the left with the left hand. They also tended to remove the raisin first from the holes ipsilateral to the injection site. When food was presented bilaterally, they always preferred the ipsilateral presentation.

USE-DEPENDENT ORGANIZATION OF THE I NFERIOR PARIETAL AND VENTRAL PREMOTOR CORTEX Although use-dependent changes have not been directly studied in either the anterior intraparietal sulcus or the ventral premotor area, it seems apparent that these areas are influenced by use. As an example, one of the most common types of grasping neurons found in the ventral premotor cortex in monkeys are those that respond to a precision grip, a grip formation that is not seen in young infant monkeys, but is seen with increasing regularity as monkeys get older (Lemon, 1993). Rizzolatti and Luppino (2001) suggest that the matching between the visually observed characteristics of an object and appropriate motor programs occurs early in life and is accomplished through processes that associate the intrinsic visual properties of the object with the grips that are effective in interacting with them.

THE I NFERIOR PARIETAL CORTEX AND TOOL USE Hand positioning to pick up an object requires a posture adapted to the features of the object (e.g., size, shape), but picking up an object to actually use it also requires that the grip anticipate what action will be performed. Think about the difference in hand position used when holding a pencil to punch a hole in a piece of cardboard as opposed to picking up a pencil to write. The posterior parietal lobe is implicated in this function. Sirigu et al. (1995) describe a patient with a bilateral lesion in the posterior parietal lobe who had normal sensory and motor functions, yet had a great deal of difficulty grasping tools. Figure 1-9 illustrates some of the patient’s problems grasping common objects, such as a nail clipper, spoon, and scissors. At home she had difficulty using objects in such tasks as brushing her teeth, locking her door, and cutting meat. What was of particular interest in this patient was that if the examiner corrected the patient’s grasp and the object was placed in her hand appropriately, she could perform with normal movement kinematics. Further, if the patient was asked to just grasp an object and not use it, appropriate preshaping of the hand and wrist to the object’s physical characteristics was seen. It was the capacity to match the grasp to the object’s use that seemed to be missing in this patient. Apparently the posterior parietal cortex is important for this function. Another feature of skilled tool use is that when the hand uses a tool, the tool becomes an extension of the hand. When one writes, one is not aware of the pen as a tool separate from the hand. Rather, it is an integral

Cortical Control of Hand-Object Interaction • 15

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Figure 1-9 Spontaneous hand use of a woman with a bilateral disturbance of the posterior parietal lobe as she attempts to use a: (A) lighter, (B) nail clipper, (C) soup spoon, and (D) scissors (successive attempts). (Redrawn from Sirigu A, Cohen L, Duhamel J, Pillon B, Dubois B, Agid Y [1995]. A selective impairment of hand posture for object utilization in apraxia. Cortex, 31:41–55.)

part of the automatic movements that create the letters. It appears that the sense of the tool as an extension of the hand has a neurologic correlate that includes the tool into the body scheme of the hand. Working with monkeys, Iriki, Tanaka, and Iwamura (1996) pointed out that the visual receptive fields of neurons within the anterior intraparietal sulcus changed when the monkey used a rake to obtain food pellets (Figure 1-10). Soon after the monkey began to use the rake, the visual field was seen to change to not only cover the area around the hand but also to include the total length of the rake. This did not happen when the animal only held the tool or just moved a stick back and forth. That is, when the rake was used as a tool, the rake and the body schema of the hand came to be represented together. When imaging studies were done of humans picking up a small object with tongs or with just the fingers, the intraparietal sulcus was again implicated in the tool use task (Inoue et al., 2001). It appears that the anterior intraparietal sulcus is an important area concerned with the preparation and grasp of objects and may be particularly important for tool use. This area has strong connections with the

ventral premotor area, which also appears to be important for hand use. There is one other function of the parietal lobe related to object interaction that should be mentioned, the guidance of movements when exploring an object manually. The term “tactile apraxia” has been used to define a problem in this area (Pause et al., 1989). In patients with tactile apraxia, exploratory movements are described as slow and clumsy and may consist of only squeezing the object (Binkofski et al., 2001; Pause & Freund, 1989; Valenza et al., 2001). This problem has been seen in a variety of parietal lesions (Binkofski et al., 2001; Pause & Freund, 1989; Valenza et al., 2001), including the primary somatosensory cortex (Motomura et al., 1990; Tomberg & Desmedt, 1999). The problem does not appear to be related to the severity of any somatosensory disturbances that might be present. That is, a patient with a significant sensory loss may be better able to manipulate an object for identification than a patient with better-preserved sensation (Pause et al., 1989; Valenza et al., 2001). Problems moving her finger around objects in a manual form identification task was one area with which Katie had difficulty. She tended to just

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Part I • Foundation of Hand Skills A

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table

Food dispenser

Figure 1-10 A. Monkey using a rake to obtain a food pellet that was dispensed out of its reach from a container. B. Simple stick manipulation task in which the food pellet was delivered at a reachable distance as a reward for swinging the stick. (Redrawn from Obayashi S, Suhara T, Kawabe K, Okauchi, Maeda J, Akine Y, Onoe H, Iriki A (2001): Functional brain mapping of monkey tool use, Neuroimage 14: 853-861.)

hold the object. As one group of researchers said, “The parietal lobe is not only involved in the elaboration and further processing of somatosensory information, but also in the conception and generation of those motor programs required to collect this information.” (Pause et al., 1989, p. 1622).

SUMMARY AND THERAPEUTIC IMPLICATIONS This section reviews the covered information. The primary motor cortex is critical to the ability to move the fingers individually and speedily. Without this input, hand movements are characterized by varying degrees of muscle cocontraction so movements are stiff, awkward, and slow. This ability to “fractionate” movements of the hand is transmitted by the corticospinal tract, particularly through direct corticospinal connections to the motoneurons of hand muscles. Through intracortical connections of the various hand muscles in the primary motor cortex, movements used together come to be represented together. When a movement is performed, this action generates sensory feedback. Discrete information related to the movements is carried back to the primary sensory cortex by the dorsal columns. This information can then be fed back to the motor cortex via corticocortical connections so any necessary corrections of the movements can be made. Through practice, the correct combination and timing of muscles can be perfected through this mechanism. Once learned, feedback is much less important. This is not to say that everyday, learned movements are not dependent on sensory information. The ability to pick up an object and hold it with just

enough force so that it is not dropped is dependent on sensory input from the fingers. The exact placement of the fingers on an object after grasp is also dependent on sensory feedback. Humans have an important cortical loop for the control of skilled hand function and the interaction with objects, the primary motor cortex and primary sensory cortex connection (Figure 1-11). However, the described actions are relatively simple and human object use is not simple. The second cortical circuit between the posterior parietal lobe (particularly the anterior intraparietal sulcus) and the ventral premotor area is important in the selection of the appropriate grip patterns. As indicated, the inferior portion of the posterior parietal lobe receives both somatosensory information from the primary sensory cortex and visual information from the visual cortex, resulting in complex bimodal neurons (neurons that respond to both somatosensory and visual information). Vision information about an object provides information about the object’s size, shape, and orientation. This allows the hand to be preshaped to the object’s characteristics before contact. This visual information is transferred to the premotor area through corticocortical connections in which the appropriate grip pattern is chosen. The premotor area then sends this information to the primary motor cortex for the selection and timing of the necessary muscles. This in turn results in sensory information fed to the primary sensory cortex and back to the motor cortex, completing the circuit (see Figure 1-11). The anterior intraparietal sulcus of the posterior parietal lob also is important for incorporating the tool into the body schema of the hand, therefore making the tool an extension of the hand. It also should be noted that there are hand skills that have not been discussed in this chapter; many of these are covered in

Cortical Control of Hand-Object Interaction • 17

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B

Figure 1-11 A. Diagram of a somatosensory and a primary motor cortex circuit. (1) A message from the primary motor cortex is sent to the muscles via the corticospinal tract; (2) sensory feedback is sent through the dorsal column as a result of the movement (3) of sensory input to the primary somatosensory cortex; (4) sensory information is sent from the primary sensory cortex to the primary motor cortex for any necessary correction of the movement. B. Diagram of somatosensory, inferior parietal lobe, ventral premotor cortex, and motor cortex circuit. (1) Sensory information is sent to the inferior parietal lobe; (2) visual information also is transferred to the inferior parietal lobe; (3) information from the inferior parietal lobe is sent to the ventral premotor cortex; (4) the ventral premotor area transfers information to the primary motor cortex and from there to the corticospinal tract.

other chapters of this book (e.g., handedness, reaching, eye–hand coordination, and perceptual functions of the hand). This chapter has concentrated on the performance of the hand in hand–object interaction, and has not discussed the shoulder or postural support as background for these skilled movements. These are also important aspects of hand function. For example, Smith-Zuzovsky and Exner (2004) found that 6- and 7-year-old children who were positioned in furniture that was fitted to their size did significantly better on a test of in-hand manipulation than children using typical classroom furniture. In most natural movements the more proximal muscles provide the stability that allows skilled actions of the hand. Thus the corticospinal connections to proximal and distal muscles must cooperate (Turton & Lemon, 1999), but the roles of reach and postural functions are different and therefore so are the basic neural mechanisms that control them. The primary role of posture and the shoulder in skilled hand function is one of stability. If the shoulder lacks stability for hand function or the postural muscles cannot adequately support the trunk, then this needs to be addressed through mechanisms to increase stability and strength. Hand muscles also may need strengthening, but remember that the primary roles of the hand are to act, move, and perform with skill. If a child presents with shoulder instability, poor trunk support, and poor hand use, these should be worked on simultaneously. The hand should not wait until some minimal level of postural support is achieved. The choice of proper positioning and creative selection of activities can make it possible for the child to use his or her hands even when postural support is poor.

As discussed, the cortical reorganization responsible for skilled learning, particularly as it relates to hand– object interaction, is use dependent. It is through use that functional patterns of movement or the muscles necessary for the action come to be represented together. The same is true of patterns of somatosensory input. Surfaces that are used together come to be represented together. This happens through practice. Also as indicated, this structural reorganization is best accomplished through tasks that require skill or the learning of an activity. It also requires attention to the task. Passive movements and strength training are much less effective in driving this cortical reorganization. Children with poor hand skills, like Katie, often avoid or are so poor at fine motor tasks that they may actually get less practice than their peers. Skill requires attention to the activity and is facilitated when there is an interest in the outcome. Children with poor hand skills may need help to select and adapt to activities to meet their level of performance and interest. The art of therapy is being able to provide activities that challenge the child within the scope of his or her abilities and elicit the child’s enthusiastic cooperation.

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Augurelle A, Smith AM, Lejeune T, Thonnard J (2003). Importance of cutaneous feed back in maintaining a secure grip during manipulation of hand-held objects. Journal of Neurophysiology, 89:665–671. Bennett KM, Lemon RN (1996). Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. Journal of Neurophysiology, 75:1826–1842. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H (1999). A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. European Journal of Neuroscience, 11:3276–3286. Binkofski F, Dohle C, Posse S, Stephan KM, Heftner H, Seitz RJ, Freund HJ (1998). Human anterior intraparietal area subserves prehension: A combined lesion and functional MRI activation study. Neurology, 50:1253–1259. Binkofski F, Kunesch E, Classen J, Seitz RJ, Freund H (2001). Tactile apraxia: Unimodal apractic disorder of tactile object exploration associated with parietal lobe lesions. Brain, 124:132–144. Brandt BR (1996). Impaired tactual perception in children with Down’s syndrome. Scandinavian Journal of Psychology, 37:12–16. Brandt BR, Rosen I (1995). Impaired peripheral somatosensory function in children with Down syndrome. Neuropediatrics, 3:310–312. Brochier T, Boudreau MJ, Smith AM (1999). The effect of muscimol inactivation of small regions of motor and somatosensory cortex on independent finger movements and force control in the precision grip. Experimental Brain Research, 128:31–40. Butefisch CM (2004). Plasticity in the human cerebral cortex: Lessons from the normal brain and from stroke. Neuroscientist, 10:163–173. Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998). Rapid plasticity of human cortical movement representation induced by practice. Journal of Neurophysiology, 79:1117–1123. Darian-Smith I, Burman K, Darian-Smith C (1999). Parallel pathways mediating manual dexterity in the macaque. Experimental Brain Research, 128:101–108. Debowy DJ, Ghosh S, Ro JY, Gardner EP (2001). Comparison of neuronal firing rates in somatosensory and posterior parietal cortex during prehension. Experimental Brain Research, 137:269–291. deJong BM, Coert JH, Stenekes MW, Leenders KL, Paans AM, Nicolai JP (2003). Cerebral reorganization of human hand movements after dynamic immobilization. Neuroreport, 14:1693–1696. Denckla MB (1974). Development of motor co-ordination in normal children. Developmental Medicine and Child Neurology, 16:729–741. Edin BB, Westling G, Johansson RS (1992). Independent control of human finger-tip forces at individual digits during precision lifting. Journal of Physiology, 450:547–564. Ehrsson HH, Kuhtz-Buschbeck JP, Forssberg H (2002). Brain regions controlling nonsynergistic versus synergistic movements of the digits: A functional magnetic resonance imaging study. Journal of Neuroscience, 22:5074-5080. Evans AL, Harrison LM, Stephens JA (1990). Maturation of the cutaneomuscular reflex recorded from the first dorsal interosseous muscle in man. Journal of Physiology, 428:425–440.

Fadiga L, Craighero L (2003). New insight on sensorimotor integration: From hand action to speech perception. Brain and Cognition, 53:514–524. Fogassi L, Gallese V, Buccino G, Craighero G, Fadiga L, Rizzolatti G (2001). Cortical mechanisms for the visual guidance of hand grasping movements in the monkey: A reversible inactivation study. Brain, 124:571–583. Forssberg H, Eliasson AC, Kinoshita H, Johansson RS, Westling G (1991). Development of human precision grip I. Basic coordination of force. Experimental Brain Research, 85:451–457. Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994). Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport, 5:1525–1529. Godde B, Ehrhardt J, Braun C (2003). Behavioral significance of input-dependent plasticity of human somatosensory cortex. Neuroreport, 14:543–546. Hashimoto I, Suzuki A, Kimura T, Iguchi Y, Tanosaki M, Takino R, Haruta Y, Taira M (2004). Is there trainingdependent reorganization of digit representation in area 3b of string players? Clinical Neurophysiology, 115:435–437. Hikosaka O, Tanaka, M, Sakamoto M, Iwamura Y (1985). Deficits in manipulative behaviors induced by local injection of muscimol in the first somatosensory cortex of the conscious monkey. Brain Research, 325:375–380, Huntley GW, Jones E (1991). Relationship of intrinsic connections to forelimb movement representation in monkey motor cortex: A correlative anatomic and physiological study. Journal of Neurophysiology, 66:390–413. Hyvarinen J (1982). Posterior parietal lobe of the primate brain. Psychological Reviews, 62:1060–1129. Inoue K, Kawashima R, Sugiura M, Ogawa A, Schormann T, Zilles K, Fukuda H (2001). Activation in the ipsilateral posterior parietal cortex during tool use: A PET study. Neuroimage, 14:1469–1475. Inoue K, Wang X, Tamura Y, Kaneoke Y, Kakigi R (2004). Serial processing in the human somatosensory system. Cerebral Cortex, 14:851–857. Iriki A, Tanaka M, Iwamura Y (1996). Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport, 7:2325–2330. Iwamura Y (1998). Hierarchical somatosensory processing. Current Opinions in Neurobiology, 8:522–528. Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1985). Functional surface integration, submodality convergence and tactile feature detection in area 2 of the monkey somatosensory cortex. Experimental Brain Research, Suppl. 10:44–58. Jackson A, Lemon RN (2001). Motor control: Forcing neurons to change. Current Biology, 11:R708–R709. Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In J Long, A Baddeley, editors: Attention and performance IX. Hillsdale, NJ, LEA. Jeannerod M, Arbid M, Rizzolatti G, Sakata H (1995). Grasping objects: The cortical mechanisms of visuomotor transformation. Trends in Neuroscience, 18:314–320. Jeannerod M, Michel F, Prablanc C (1984). The control of hand movements in a case of hemianaesthesia following a parietal lesion. Brain, 107:899–920. Johansson RS, Westling G (1984). Role of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Experimental Brain Research, 56:550–564.

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activation in the human rolandic cortex using fMRI. Journal of Neurophysiology, 84:558–569. Morrongiello BA, Rocca PT (1989). Visual feedback and anticipatory hand orientation during infants’ reaching. Perceptual and Motor Skills, 69:787–802. Motomura N, Yamodori A, Asaba H, Sakai T, Swada T (1990). Failure to manipulate objects secondary to active touch disturbance. Cortex, 26:473–477. Mountcastle VB, Lynch LC, Georgopoulos A, Sakata H, Aguna C (1975). Posterior parietal association cortex of the monkey: Command functions for operation within extra personal space. Journal of Neurophysiology, 38:871–908. Muir RB (1985). Small hand muscles in precision grip: A corticospinal prerogative? In AW Goodwin, I DarianSmith, editors: Hand function and the neocortex. New York, Springer-Verlag. Nadler MA, Harrison LM, Stephens JA (2000). Acquisition of a new motor skill is accompanied by changes in cutaneomuscular reflex responses recorded from finger muscles in man. Experimental Brain Research, 134:246–254. Nakajima K, Maier MA, Kirkwood PA, Lemon RN (2000). Striking differences in transmission of corticospinal excitation to upper limb motoneurons in two primate species. Journal of Neurophysiology, 84:698–709. Nudo RJ, Milliken G, Jenkins WM, Merzenich MM (1996). Use dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. Journal of Neuroscience, 15:785–807. Obayashi S, Suhara T, Kawabe K, Okauchi T, Maeda J, Akine Y, Onoe H, Iriki A (2001). Functional brain mapping of monkey tool use. Neuroimage, 14:853–861. Paillard J (1993). The hand and the tool: The functional architecture of human technical skills. In A Berthelet, J Chavillon, editors: The use of tools by humans and nonhuman primates. Oxford, UK, Clarendon Press. Pascual-Leone A, Grafman J, Hallett M (1994) Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science, 263:1287–1291. Pause M, Freund H (1989). Role of the parietal cortex for sensorimotor transformation: Evidence from clinical observation. Brain Behavior and Evolution, 33:136–140. Pause M, Kunesch E, Binkofski F, Freund H (1989). Sensorimotor disturbances in patients with lesions of the parietal cortex. Brain, 112:1599–1625. Pavlides C, Miyashita E, Asanuma H (1993). Projection from the sensory cortex is important in learning motor skills in the monkey. Journal of Neurophysiology, 70:733–741. Pehoski C, Henderson A, Tickel-Degnen L (1997a). Inhand manipulation in young children: Rotation of an object in the fingers. American Journal of Occupational Therapy, 51:544–552. Pehoski C, Henderson A, Tickel-Degnen L (1997b). Inhand manipulation in young children: Translation movements. American Journal of Occupational Therapy, 51:719–728. Pereira H, Landgren M, Gillberg C, Forssberg H (2001). Parametric control of fingertip forces during precision grip lifts in children with DCD (developmental coordination disorder) and DAMO (deficits in attention, motor control, and perception). Neuropsychologia, 39:478–488. Plautz EJ, Milliken GW, Nudo RJ (2000). Effects of repetitive motor training on movement representation in

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adult squirrel monkeys: Role of use versus learning. Neurobiology of Learning and Memory, 74:27–55. Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR (1992). Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency-discrimination task. Journal of Neurophysiology, 67:1031–1056. Remple MS, Bruneau RM, VandenBerg PM, Goertzen C, Kleim JA (2001). Sensitivity of cortical movement representations to motor experience: Evidence that skill learning but not strength training induces cortical reorganization. Behavioral Brain Research, 123:133–141. Rizzolatti R, Camarda L, Fogassi M, Gentilucci M, Luppino G, Matalli M (1988). Functional organization of inferior area 6 in the macaque monkey: II. area F5 and the control of distal movements. Experimental Brain Research, 71:491–507. Rizzolatti G, Fadiga L (1998). Grasping objects and grasping action meaning: the dual role of monkey rostroventral premotor cortex (area F5). In JA Goode, editor: Sensory guidance of movement. Novartis Foundation Symposium, Chichester, UK, Wiley. Rizzolatti G, Luppino G (2001). The cortical motor system. Neuron, 31:889–901. Rouiller EM, Yu XH, Moret V, Tempini A, Wiesendanger M, Liang F (1998). Dexterity in adult monkeys following early lesions of the motor cortical hand area: The role of cortex adjacent to the lesion. European Journal of Neuroscience, 10:729–740. Sakata H, Iwamura Y (1978). Cortical processing of tactile information in the first somatosensory and parietal association areas in the monkey. In G Gordon, editor: Active touch. New York, Pergamon Press. Sakata H, Taira M, Kusunoki M, Murata A, Tsutsui K, Tanaka Y, Shein W, Miyashita Y (1999). Neural representation of three-dimensional features of manipulation objects with stereopsis. Experimental Brain Research, 128:160–169. Sakata H, Taira M, Murata A, Mine S (1995). Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. Cerebral Cortex, 5:429–438. Sanes JN, Donoghue JP (2000). Plasticity and primary motor cortex. Annual Review of Neuroscience, 23:393–415. Scheibel A, Conrad T, Perdue S, Tomiyasu U, Wechsler A (1990). A quantitative study of dendrite complexity in selected areas of the human cerebral cortex. Brain and Cognition, 12:85–101. Schieber MH, Poliakov AV (1998). Partial inactivation of the primary motor cortex hand area: Effects on individual finger movements. Journal of Neuroscience, 18:9038–9054. Schlaug G, Knorr U, Seitz R (1994). Inter-subject variability of cerebral activations in acquiring a motor skill: A study with positron emission tomography. Experimental Brain Research, 98:523–534. Shimazu H, Maier MA, Cerri G, Kirkwood PA, Lemon RN (2004). Macaque ventral premotor cortex exerts powerful

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Chapter

2

ANATOMY AND KINESIOLOGY OF THE HAND James W. Strickland

CHAPTER OUTLINE

EMBRYONIC DEVELOPMENT

EMBRYONIC DEVELOPMENT

Inspection of a normal newborn’s hands never ceases to evoke awe and wonderment. The tiny nails punctuating the ends of intricately formed fingers and opposable thumbs, each delicately marked with familiar patterns of joint wrinkles, immediately identify the newcomer as human. All of the ingredients that eventually provide an unbelievably extensive continuum of function from exquisitely fine dexterity to great power are present in the tiny waving arms and hands. However, the normal embryonic process through which the upper extremities develop is both predictable and consistent (Arey, 1980; Bora, 1986; Bunnell, 1944; Moore, 1982). Upper limb buds are discernible at 4 weeks of gestation. The scapula, humerus, radius, and ulna are apparent at 5 weeks as cartilage, and by 6 weeks upper arm, forearm, and hand divisions are present. Also at 6 weeks the webbed swellings of the three central digits appear and are soon followed by the two border digits. The metacarpals are present as cartilage, as are the proximal phalanges of the index through small fingers. Initially, each extremity is aligned longitudinally with the body trunk, but at 7 weeks the arms rotate outward and forward at the shoulder level to assume a hand-toface position with the flexor surface of the forearm and hand turned inward toward the body and the extensor surface turned outward. Elbows and wrists are slightly flexed. Innervation of the limbs has already occurred at this point, and vessels extend to the distal extremity. Muscles, muscle groups, joint hollows, and digital cleavages, including thumb differentiation, are also present at 7 to 8 weeks. Webbing between the digits diminishes, and the fingers and thumb are independent of each other by 8 weeks. Carpal bones are cartilaginous, and the os centrale fuses to the scaphoid at 8 weeks.

ANATOMY OF THE FULLY DEVELOPED HAND Osseous Structures Joints Muscles and Tendons Nerve Supply Skin and Subcutaneous Fascia Functional Patterns

One cannot expect to adequately understand the development and function of the hand and arm without a solid working knowledge of the intricate anatomic and kinesiologic relationships of the upper extremity, including the embryonic growth stages through which the extremity progresses. Only through comprehension of the normal formation and anatomy of the human hand can one adequately develop an appreciation for the disturbance in function that accompanies injury, disease, or dysfunction. It is appropriate, therefore that an early chapter in a book devoted to development of fine motor coordination be concerned with the embryology, anatomy, kinesiology, and biomechanics of the hand. Because it is impossible in this chapter to review in great detail the enormous amount of literature that has been written about these fields of knowledge, readers are directed to the Suggested Readings.

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Part I • Foundation of Hand Skills

For the remainder of gestation after 8 weeks, limb changes primarily involve growth of already present structures.

ANATOMY OF THE FULLY DEVELOPED HAND The anatomy of the hand must be approached in a systematic fashion with individual consideration of the osseous structures, joints, musculotendinous units, and nerve supply. However, it is obvious that the systems do not function independently, but that the integrated presence of all these structures is necessary for normal hand function. In presenting this material, this chapter strays into the important mechanical and kinesiologic considerations that result from the unique anatomic arrangement of the hand.

OSSEOUS STRUCTURES The unique arrangement and mobility of the bones of the hand (Figure 2-1) provide a structural basis for its enormous functional adaptability. The osseous skeleton consists of eight carpal bones divided into two rows: The proximal row articulates with the distal radius and ulna (with the exception of the pisiform, which lies palmar to and articulates with the triquetrum); the distal four carpal bones in turn articulate with the five

metacarpals. Two phalanges complete the first ray, or thumb unit, and three phalanges each comprise the index, long, ring, and small fingers. These 27 bones, together with the intricate arrangement of supportive ligaments and contractile musculotendinous units, are arranged to provide both mobility and stability to the various joints of the hand. Although the exact anatomic configuration of the bones of the hand need not be memorized in detail, it is important that one should develop knowledge of the position and names of the carpal bones, metacarpals, and phalanges and an understanding of their kinesiologic patterns to proceed with the management of many hand problems. The bones of the hand are arranged in three arches (Figure 2-2), two transversely oriented and one that is longitudinal. The proximal transverse arch, the keystone of which is the capitate, lies at the level of the distal part of the carpus and is reasonably fixed, whereas the distal transverse arch passing through the metacarpal heads is more mobile. The two transverse arches are connected by the rigid portion of the longitudinal arch consisting of the second and third metacarpals, the index and long fingers distally, and the central carpus proximally. The longitudinal arch is completed by the individual digital rays, and the mobility of the first, fourth, and fifth rays around the second and third allows the palm to flatten or cup itself to accommodate objects of various sizes and shapes. To a large extent the intrinsic muscles of the hand are responsible for changes in the configuration of the

Distal phalanx

Middle phalanx

Proximal phalanx

Metacarpal

Hamate Pisiform Triquetrum

A

Trapezoid Capitate Trapezium Scaphoid Lunate

Hamate Triquetrum

B

Figure 2-1 Bones of the right hand. A. Palmar surface. B. Dorsal surface. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

Anatomy and Kinesiology of the Hand • 23 Distal transverse arch

Proximal transverse arch

Distal transverse arch Longitudinal arch

A

B

Proximal transverse arch

Figure 2-2 A. Skeletal arches of the hand. The proximal transverse arch passes through the distal carpus; the distal transverse arch, through the metacarpal heads. The longitudinal arch is made up of the four digital rays and the carpus proximally. B. Proximal and distal transverse arches. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

osseous arches. Collapse in the arch system can contribute to severe disability and deformity. Flatt (1979, 1983, 1995) has pointed out that grasp is dependent on the integrity of the mobile longitudinal arches and when destruction at the carpometacarpal joint, metacarpophalangeal joint, or proximal interphalangeal joint interrupts the integrity of these arches, crippling deformity may result.

JOINTS The multiple complex articulations among the distal radius and ulna, the eight carpal bones, and the metacarpal bases comprise the wrist joint, whose proximal position makes it the functional key to the motion at the more distal hand joints of the hand. Functionally the carpus transmits forces through the hand to the forearm. The proximal carpal row consisting of the scaphoid (navicular), lunate, and triquetrum articulates distally with the trapezium, trapezoid, capitate, and hamate; there is a complex motion pattern that relies both on ligamentous and contact surface constraints. The major ligaments of the wrist (Figure 2-3) are the palmar and intracapsular ligaments. There are three strong radial palmar ligaments: the radioscaphocapitate or “sling” ligament, which supports the waist of the scaphoid; the radiolunate ligament, which supports the lunate; and the radioscapholunate ligament, which connects the scapholunate articulation with the palmar portion of the distal radius. This ligament functions as a checkrein for scaphoid flexion and extension. The ulnolunate ligament arises intra-articularly from the triangular articular meniscus of the wrist joint and inserts on the lunate and, to a lesser extent, the triquetrum. The radial and ulnar collateral ligaments are capsular ligaments, and V-shaped ligaments from the capitate to

the triquetrum and scaphoid have been termed the deltoid ligaments. Dorsally, the radiocarpal ligament connects the radius to the triquetrum and acts as a dorsal sling for the lunate, maintaining the lunate in apposition to the distal radius. Further dorsal carpal support is provided by the dorsal intracarpal ligament. These strong ligaments combine to provide carpal stability while permitting the normal range of wrist motion. The distal ulna is covered with an articular cartilage (Figure 2-3, C) over its most dorsal, palmar, and radial aspects, where it articulates with the sigmoid or ulnar notch of the radius. The triangular fibrocartilage complex describes the ligamentous and cartilaginous structure that suspends the distal radius and ulnar carpus from the distal ulna. Blumfield and Champoux (1984) have indicated that the optimal functional wrist motion to accomplish most activities of daily living is from 10° of flexion to 35° of extension. Taleisnik (1976a,b, 1985a,b, 1992) has emphasized the importance of considering the wrist in terms of longitudinal columns (Figure 2-4). The central, or flexion extension, column consists of the lunate and the entire distal carpal row; the lateral, or mobile, column comprises the scaphoid alone; and the medial, or rotation, column is made up of the triquetrum. Wrist motion is produced by the muscles that attach to the metacarpals, and the ligamentous control system provides stability only at the extremes of motion. The distal carpal row of the carpal bones is firmly attached to the hand and moves with it. Therefore during dorsiflexion the distal carpal row dorsiflexes, during palmar flexion it palmar flexes, and during radial and ulnar deviation it deviates radially or ulnarly. As the wrist ranges from radial to ulnar deviation, the proximal carpal row rotates in a dorsal direction, and a simultaneous

24

Part I • Foundation of Hand Skills Deltoid ligaments Space of Poirier

Lunotriquetral ligament

Radioscaphocapitate ligament Vestigial ulnar collateral ligament

Scapholunate ligament Radial collateral ligament

Ulnocarpal meniscus homologue

Radiolunate ligament (radiolunotriquetral)

Ulnolunate ligament (ulnolunate-triquetral) Radioscapholunate ligament (ligament of Testut and Kuenz)

A

C

H

Td

Tm

P Dorsal intercarpal ligament

1

Tq S L

Dorsal radiocarpal ligament (radiotriquetral)

7

4

2

3

5 6

B

C

Figure 2-3 Ligamentous anatomy of the wrist. A. Palmar wrist ligaments. B. Dorsal wrist ligaments. C. Dorsal view of the flexed wrist, including the triangular fibrocartilage. 1, Ulnar collateral ligament; 2, retinacular sheath; 3, tendon of extensor carpi ulnaris; 4, ulnolunate ligament; 5, triangular fibrocartilage; 6, ulnocarpal meniscus homologue; 7, palmar radioscaphoid lunate ligament. P, Pisiform; H, hamate; C, capitate; Td, trapezoid; Tm, trapezium; Tq, triquetrum; L, lunate; S, scaphoid. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

translocation of the proximal carpus occurs in a radial direction at the radiocarpal and midcarpal articulations. This combined motion of the carpal rows has been called the rotational shift of the carpus. It was once taught that palmar flexion takes place to a greater extent at the radiocarpal joint and secondarily in the midcarpal joint, but because dorsiflexion occurs primarily at the midcarpal joint and only secondarily at the radiocarpal articulation, this now appears to be a significant oversimplification. The complex carpal kinematics are beyond the scope of this chapter, and the reader is referred to the works of Weber (1988),

Taleisnik (1985a,b), Lichtman and Alexander (1988), and Cooney, Linscheid, and Dobyns (1998) to gain a thorough understanding of this difficult subject. The articulation between the base of the first metacarpal and the trapezium (Figure 2-5) is a highly mobile joint with a configuration thought to be similar to that of a saddle. The base of the first metacarpal is concave in the anteroposterior plane and convex in the lateral plane, with a reciprocal concavity in the lateral plane and an anteroposterior convexity on the opposing surface of the trapezium. This arrangement allows the positioning of the thumb in a wide arc of

Anatomy and Kinesiology of the Hand • 25

Central column Medial column

Lateral column

First metacarpal

A

Figure 2-4 Columnar carpus. The scaphoid is the mobile or lateral column. The central, or flexion extension, column comprises the lunate and the entire distal carpal row. The medial, or rotational, column comprises the triquetrum alone. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

B Figure 2-6 A. Multiple planes of motion (arrows) that occur at the carpometacarpal joint of the thumb. B. The thumb moves (arrow) from a position of adduction against the second metacarpal to a position of palmar or radial abduction away from the hand and fingers and can then be rotated into positions of opposition and flexion. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

Figure 2-5 Saddle-shaped carpometacarpal joint of the thumb. A wide range of motion (arrows) is permitted by the configuration of this joint. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

motion (Figure 2-6), including flexion, palmar and radial abduction, adduction, and opposition. The ligamentous arrangement about this joint, while permitting the wide circumduction, continues to provide stability at the extremes of motion, allowing the thumb to be brought into a variety of positions for pinch and grasp, but maintaining its stability during these functions. The articulations formed by the ulnar half of the hamate and the fourth and fifth metacarpal bases allow a modest amount of motion (15° at the fourth carpometacarpal joint and 25° to 30° of flexion and extension at the fifth carpometacarpal joint). A resulting “palmar descent” of these metacarpals occurs during strong grasp. The metacarpophalangeal joints of the fingers are diarthrodial joints with motion permitted in three

planes and combinations thereof (Figure 2-7). The cartilaginous surfaces of the metacarpal head and the bases of the proximal phalanges are enclosed in a complex apparatus consisting of the joint capsule, collateral ligaments, and the anterior fibrocartilage or palmar plate (Figure 2-8). The capsule extends from the borders of the base of the proximal phalanx proximally to the head of the metacarpals beyond the cartilaginous joint surface. The collateral ligaments, which reinforce the capsule on each side of the metacarpophalangeal joints, run from the dorsolateral side of the metacarpal head to the palmar lateral side of the proximal phalanges. These ligaments form two bundles, the more central of which is called the cord portion of the collateral ligament and inserts into the side of the proximal phalanx; the more palmar portion joins the palmar plate and is termed the accessory collateral ligament. These collateral ligaments are somewhat loose with the metacarpophalangeal joint in extension, allowing for considerable “play” in the side-to-side motion of the digits (Figure 2-9). With the metacarpophalangeal joints in full flexion, however, the cam configuration of the metacarpal head tightens the collateral ligaments and limits lateral mobility of the digits. This alteration in tension becomes an important factor in immobilization of the metacarpophalangeal joints for any length of time, because the secondary

26

Part I • Foundation of Hand Skills Collateral ligament (loose in extension) Hinge (anteroposterior motion)

Diarthrodial (multiplane motion)

Palmar plate

Membranous portion of palmar plate (folds in flexion)

Figure 2-7 Joints of the phalanges. The diarthrodial configuration of the metacarpophalangeal joint permits motion in multiple planes, whereas the biconcave-convex hinge configuration of the interphalangeal joints restricts motion to the anteroposterior plane. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

Cord portion of collateral ligaments

Cord portion of collateral ligaments

Accessory collateral ligament

Accessory collateral Palmar ligaments Palmar fibrocartilaginous fibrocartilaginous plates plates

Figure 2-8 Ligamentous structures of the digital joints. The collateral ligaments of the metacarpophalangeal and interdigital joints are composed of a strong cord portion with bony origin and insertion. The more palmarly placed accessory collateral ligaments originate from the proximal bone and insert into the palmar fibrocartilaginous plate. The palmar plates have strong distal attachments to resist extension forces. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

shortening of the lax collateral ligaments that may occur when these joints are immobilized in extension results in severe limitation of metacarpophalangeal joint flexion by these structures. The palmar fibrocartilaginous plate on the palmar side of the metacarpophalangeal joint is firmly attached

Collateral ligament (tight in flexion)

Figure 2-9 At the metacarpophalangeal joint level, the collateral ligaments are loose in extension but become tightened in flexion. The proximal membranous portion of the palmar plate moves proximally to accommodate for flexion. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Wynn Parry CB, et al. [1973]. Rehabilitation of the hand. London, Butterworth.)

to the base of the proximal phalanx and loosely attached to the anterior surface of the neck of the metacarpal by means of the joint capsule at the neck of the metacarpal. This arrangement allows the palmar plate to slide proximally during metacarpophalangeal joint flexion. The flexor tendons pass along a groove anterior to the plate. The palmar plates are connected by the transverse intermetacarpal ligaments, which connect each plate to its neighbor. The metacarpophalangeal joint of the thumb differs from the others in that the head of the first metacarpal is flatter and its cartilaginous surface does not extend as far laterally or posteriorly. Two small sesamoid bones are also adjacent to this joint, and the ligamentous structure differs somewhat. A few degrees of abduction and rotation are permitted by the ligament arrange-

Anatomy and Kinesiology of the Hand • 27 ment of the metacarpophalangeal joint at the thumb, which is of considerable functional importance in delicate precision functions. There is considerable variation in the range of motion present at the thumb metacarpophalangeal joints. The amount of motion varies from as little as 30° to as much as 90°. The digital interphalangeal joints are hinge joints (see Figure 2-7) and, like the metacarpophalangeal joints, have capsular and ligamentous enclosure. The articular surface of the proximal phalangeal head is convex in the anteroposterior plane with a depression in the middle between the two condyles, which articulates with the phalanx distal to it. The bases of the middle and distal phalanges appear as a concave surface with an elevated ridge dividing two concave depressions. A cord portion of the collateral ligament and an accessory collateral ligament are present, and the collateral ligaments run on each side of the joint from the dorsolateral aspect of the proximal phalanx in a palmar and lateral direction to insert into the distally placed phalanx and its fibrocartilage plate (Figure 2-10). A strong fibrocartilaginous (palmar) plate is also present, and the collateral ligaments of the proximal and distal interphalangeal joints are tightest with the joints in near full extension. The stability of the proximal interphalangeal joint is ensured by a three-sided supporting cradle produced by the junction of the palmar plate with the base of the middle phalanx and the accessory collateral ligament structures (see Figure 2-10). The confluence of ligaments is strongly anchored by proximal and lateral extensions called the checkrein ligaments. This system

Cord

Collateral ligament

Accessory Palmar plate Checkrein ligaments

Cord Accessory

Checkrein ligaments

Collateral ligament

Palmar plate

Figure 2-10 Strong, three-sided ligamentous support system of the proximal interphalangeal joint with cord and accessory collateral ligaments and the fibrocartilaginous plate, which is anchored proximally by the checkrein ligamentous attachment. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Eaton RG [1971]. Joint injuries of the hand. Springfield, IL, Charles C Thomas.)

has been described as a three-dimensional hinge that results in remarkable palmar and lateral restraint. A wide range of pathologic conditions may result from the interruption of the supportive ligament system of the intercarpal or digital joints. At the wrist level, interruption of key radiocarpal or intercarpal ligaments may result in occult patterns of wrist instability that are often difficult to diagnose and treat. In the digits, disruption of the collateral ligaments or the fibrocartilaginous palmar plates produces joint laxity or deformity, which is more obvious.

M USCLES AND TENDONS The muscles acting on the hand can be grouped as extrinsic, when their muscle bellies are in the forearm, or intrinsic, when the muscles originate distal to the wrist joint. It is essential to thoroughly understand both systems. Although their contributions to hand function are distinctly different, the integrated function of both systems is important to the satisfactory performance of the hand in a wide variety of tasks. A schematic representation of the origin and insertion of the extrinsic flexor and extensor muscle tendon units of the hand is provided in Figures 2-11 and 2-15. The important nerve supply to each muscle group is reviewed in these figures and again when discussing the nerve supply to the upper extremity.

Extrinsic Muscles The extrinsic flexor muscles (see Figure 2-11) of the forearm form a prominent mass on the medial side of the upper part of the forearm: The most superficial group comprises the pronator teres, the flexor carpi radialis, the flexor carpi ulnaris, and the palmaris longus; the intermediate group the flexor digitorum superficialis; and the deep extrinsics the flexor digitorum profundus and the flexor pollicis longus. The pronator, palmaris, wrist flexors, and superficialis tendons arise from the area about the medial epicondyle, the ulnar collateral ligament of the elbow, and the medial aspect of the coronoid process. The flexor pollicis longus originates from the entire middle third of the palmar surface of the radius and the adjacent interosseous membrane, and the flexor digitorum profundus originates deep to the other muscles of the forearm from the proximal two-thirds of the ulna on the palmar and medial side. The deepest layer of the palmar forearm is completed distally by the pronator quadratus muscle. The flexor carpi radialis tendon inserts on the base of the second metacarpal, whereas the flexor carpi ulnaris inserts into both the pisiform and fifth metacarpal base. The superficialis tendons lie superficial to the profundus tendons as far as the digital bases, where they bifurcate and wrap around the profundi and rejoin over

28

Part I • Foundation of Hand Skills

Composite

Flexor digitorum superficialis Nerve: median Action: flexion of proximal interphalangeal and metacarpophalangeal joints

Superficial

Palmaris longus Nerve: median Action: tension of palmar fascia

Flexor carpi ulnaris Nerve: ulnar Action: flexion of wrist; ulnar deviation of hand

Flexor carpi radialis Nerve: median Action: flexion of wrist; radial deviation of hand

Flexor carpi ulnaris Palmaris longus Flexor carpi radialis

Pronator quadratus Nerve: median Action: forearm pronation

Pronator quadratus

Supinator Pronator teres

Supination

Pronation

Supinator Nerve: radial Action: forearm supination

Brachioradialis

Pronator teres Nerve: median Action: forearm pronation

Brachioradialis Nerve: radial Action: pronation or supination, depending on position of forearm

Figure 2-11 Extrinsic flexor muscles of the arm and hand. (Dark areas represent origins and insertions of muscles.) (From Fess EE, Gettle K, Philips CA, et al. (2005). Hand and upper extremity splinting. St Louis, Mosby. Modified from Marble HC [1960]. The hand, a manual and atlas for the general surgeon. Philadelphia, WB Saunders.)

Anatomy and Kinesiology of the Hand • 29

Flexor digitorum profundus Nerve: median—index and long ulnar—ring and small Action: flexion of distal interphalangeal, proximal interphalangeal, and metacarpophalangeal joints

Composite

Flexor pollicis longus Nerve: median Action: flexes interphalangeal and metacarpophalangeal joints of thumb

Deep

Figure 2-11—cont’d.

the distal half of the proximal phalanx as Camper’s chiasma (Figure 2-12). The superficialis tendon again splits for a dual insertion on the proximal half of the middle phalanges. The profundi continue through the superficialis decussation to insert on the base of FDP

FDS

FDP Camper's chiasma

FDS

Figure 2-12 Anatomy of the relationship among the flexor digitorum superficialis (FDS), flexor digitorum profundus (FDP), and the proximal portion of the flexor tendon sheath. The superficialis tendon divides and passes around the profundus tendon to reunite at Camper’s chiasma. The tendon once again divides before insertion on the base of the middle phalanx. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

the distal phalanx. The flexor pollicis longus inserts on the base of the distal phalanx of the thumb. At the wrist the nine long flexor tendons enter the carpal tunnel beneath the protective roof of the deep transverse carpal ligament in company with the median nerve. In this canal the common profundus tendon to the long, ring, and small fingers divides into the individual tendons that fan out distally and proceed toward the distal phalanges of these digits (Figure 2-13). At about the level of the distal palmar crease the paired profundus and superficialis tendons to the index, long, ring, and small fingers and the flexor pollicis longus to the thumb enter the individual flexor sheaths that house them throughout the remainder of their digital course. These sheaths with their predictable annular pulley arrangement (Figure 2-14) serve not only as a protective housing for the flexor tendons, but also provide a smooth gliding surface by virtue of their synovial lining and an efficient mechanism to hold the tendons close to the digital bone and joints. There is an increasing recognition that disruption of this valuable

30

Part I • Foundation of Hand Skills A-1

Flexor digitorum profundus

A-2

C-1 A-3 C-2 A-4

C-3

A-5

Digital flexor sheath

Flexor digitorum superficialis

Hypothenar muscles

Sheath of flexor pollicis longus Median nerve Thenar muscles

Ulnar artery Ulnar nerve

Transverse carpal ligament Radial artery

Figure 2-13 Flexor tendons in the palm and digits. Fibroosseous digital sheaths with their pulley arrangement are shown, as is a division of the superficialis tendon about the profundus in the proximal portion of the sheath. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

pulley system can produce substantial mechanical alterations in digital function, resulting in imbalance and deformity. Extension of the wrist and fingers is produced by the extrinsic extensor muscle tendon system, which consists of the two radial wrist extensors, the extensor carpi ulnaris, the extensor digitorum communis, extensor indicis proprius, and the extensor digiti quinti proprius (extensor digiti minimi) (Figure 2-15). These muscles originate in common from the lateral epicondyle and the lateral epicondylar ridge and from a small area posterior to the radial notch of the ulna. The brachioradialis originates from the epicondylar line proximal to the lateral epicondyle and, because it inserts on the distal radius, it does not truly contribute to wrist or digit motion. The extensor carpi radialis longus and brevis insert proximally on the bases of the second and third metacarpals, respectively, and the extensor carpi ulnaris inserts on the base of the fifth metacarpal. The long digital extensors terminate by insertions on the bases of the middle phalanges after receiving and giving fibers to the intrinsic tendons to form the lateral bands that are destined to insert on the bases of the distal phalanx. Digital extension, therefore results from a combination of the contribution of both the extrinsic and intrinsic extensor systems. The extensor pollicis longus

Figure 2-14 Components of the digital flexor sheath. The sturdy annular pulleys (A) are important biomechanically in guaranteeing the efficient digital motion by keeping the tendons closely applied to the phalanges. The thin pliable cruciate pulleys (C) permit the flexor sheath to be flexible while maintaining its integrity. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Doyle JR, Blythe W [1975]. American Academy of Orthopaedic Surgeons: Symposium on tendon surgery in the hand. St Louis, Mosby.)

and brevis tendons, together with the abductor pollicis longus, originate from the dorsal forearm and, by virtue of their respective insertions into the distal phalanx, proximal phalanx, and first metacarpal of the thumb, provide extension at all three levels. The extensor pollicis longus approaches the thumb obliquely around a small bony tubercle on the dorsal radius (Lister’s tubercle) and therefore functions not only as an extensor but as a strong secondary adductor of the thumb. The extensor indicis proprius also originates more distally than the extensor communis tendons from an area near the origin of the thumb extensor and long abductor. It lies on the ulnar aspect of the communis tendon to the index finger and inserts with it in the dorsal approaches of that digit. The extensor digiti quinti proprius arises near the lateral epicondyle to occupy a superficial position on the dorsum of the forearm with its paired tendons lying on the fifth metacarpal ulnar to the communis tendon to the fifth finger. It inserts into the extensor apparatus of that digit. At the wrist, the extensor tendons are divided into six dorsal compartments (Figure 2-16). The first compartment consists of the tendons of the abductor pollicis longus and extensor pollicis brevis and the second compartment houses the two radial wrist extensors, the extensor carpi radialis longus and brevis. The third compartment is composed of the tendon of the extensor pollicis longus and the fourth compartment allows passage of the four communis extensor tendons and the extensor indicis proprius tendon. The extensor

Anatomy and Kinesiology of the Hand • 31

Extensor carpi radialis longus and brevis Nerve: radial Action: extension of wrist and radial deviation of hand

Extensor indicis proprius Nerve: radial Action: extension of index finger

Extensor pollicis longus Nerve: radial Action: extension of interphalangeal joint and metacarpophalangeal joint of thumb

Extensor carpi ulnaris Nerve: radial Action: extension of wrist and ulnar deviation of hand

Composite

Extensor digitorum communis and extensor digiti quinti proprius Nerve: radial Action: extension of fingers

Figure 2-15 Extrinsic extensor muscles of the forearm and hand. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Marble HC [1960]. The hand, a manual and atlas for the general surgeon. Philadelphia, WB Saunders.) Continued

digiti quinti proprius travels through the fifth dorsal compartment and the sixth houses the extensor carpi ulnaris.

Intrinsic Muscles The important intrinsic musculature of the hand can be divided into muscles comprising the thenar eminence, those comprising the hypothenar eminence, and the remaining muscles between the two groups (Figure

2-17). The muscles of the thenar eminence consist of the abductor pollicis brevis, the flexor pollicis brevis, and the opponens pollicis, which originate in common from the transverse carpal ligament and the scaphoid and trapezium bones. The abductor brevis inserts into the radial side of the proximal phalanx and the radial wing tendon of the thumb, as does the flexor pollicis brevis, whereas the opponens inserts into the whole radial side of the first metacarpal.

32

Part I • Foundation of Hand Skills

Extensor pollicis brevis Nerve: radial Action: extension of metacarpophalangeal joint of thumb

Abductor pollicis longus Nerve: radial Action: abduction of thumb

Figure 2-15—cont’d.

First dorsal interosseous

Extensor digitorum communis

Extensor indicis proprius

Extensor digiti quinti proprius

Extensor pollicis brevis

Abductor digiti quinti Extensor pollicis longus

Extensor carpi ulnaris

Extensor carpi radialis longus and brevis

1 2 3

4

5 6

Abductor pollicis longus

2

3

4

5

1

Figure 2-16

6

Arrangement of the extensor tendons in the compartments of the wrist.

The flexor pollicis brevis has a superficial portion that is innervated by the median nerve and a deep portion that arises from the ulnar side of the first metacarpal and is often innervated by the ulnar nerve. The hypothenar eminence in a similar manner is made up of the abductor digiti quinti, the flexor digiti quinti brevis, and the opponens digiti quinti, which originate primarily from the pisiform bone and the pisohamate ligament and insert into the joint capsule of the fifth metacarpophalangeal joint, the ulnar side of the base of

the proximal phalanx of the fifth finger, and the ulnar border of the aponeurosis of this digit. The strong thenar musculature is responsible for the ability to position the thumb in opposition so that it may meet the adjacent digits for pinch and grasp functions, whereas the hypothenar group allows a similar but less pronounced rotation of the fifth metacarpal. Of the seven interosseous muscles, four are considered in the dorsal group (Figure 2-18, B) and three as palmar interossei (Figure 2-18, C). The four dorsal

Anatomy and Kinesiology of the Hand • 33

Abductor pollicis brevis Nerve: median Action: abduction of thumb

Flexor pollicis brevis Nerve: median—superficial ulnar—deep Action: flexion and rotation of thumb

Abductor digiti quinti Nerve: ulnar Action: abduction of small finger (flexion of proximal phalanx, extension of proximal and distal interphalangeal joints)

Opponens pollicis Nerve: median Action: rotation of first metacarpal toward palm

Adductor pollicis Nerve: ulnar Action: adduction of thumb

Flexor digiti quinti brevis Nerve: ulnar Action: flexion of proximal phalanx of small finger and forward rotation of fifth metacarpal

Figure 2-17 Intrinsic muscles of the hand. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Marble HC [1960]. The hand, a manual and atlas for the general surgeon. Philadelphia, WB Saunders.) Continued

interossei originate from the adjacent sides of the metacarpal bones and, because of their bipennate nature with two individual muscle bellies, have separate insertions into the tubercle and the lateral aspect of the proximal phalanges and into the extensor expansion. The more palmarly placed three palmar interossei

(Figure 2-18, C) have similar insertions and origins and are responsible for adducting the digits together, as opposed to the spreading or abducting function of the dorsal interossei. In addition, four lumbrical tendons (Figure 2-19, A) arising from the radial side of the palmar portion of the flexor digitorum profundus

34

Part I • Foundation of Hand Skills

Lumbricals Nerve: median—index and long ulnar—ring and small Action: supplements metacarpophalangeal flexion and extension of proximal and distal interphalangeal joints

Dorsal interossei

Composite

Dorsal interossei Nerve: ulnar Action: spread of index and ring fingers away from long finger

All interossei Nerve: ulnar Action: flexion of metacarpophalangeal joints and extension of proximal and distal interphalangeal joints

Palmar interossei

Palmar interossei Nerve: ulnar Action: adduction of index, ring, and fifth fingers toward long finger

Figure 2-17—cont’d.

tendons pass through their individual canals on the radial side of the digits to provide an additional contribution to the complex extensor assemblage of the digits. The arrangement of the extensor mechanism, including the transverse sagittal band fibers at the metacarpophalangeal joint and the components of the extensor hood mechanism that gain fibers from both the extrinsic and intrinsic tendons, can be seen in Figure 2-19, B, C. An oversimplification of the function of the intrinsic musculature in the digits would be that they provide strong flexion at the metacarpophalangeal joints and extension at the proximal and distal interphalangeal joints. The lumbrical tendons, by virtue of their origin from the flexor profundi and insertion into the digital extensor mechanism, function as a governor between the two systems, resulting in a loosening of the antagonistic profundus tendon during interphalangeal joint

extension. The interossei are further responsible for spreading and closing of the fingers and, together with the extrinsic flexor and extensor tendons, are invaluable to digital balance. A composite, well-integrated pattern of digital flexion and extension is reliant on the smooth performance of both systems; and a loss of intrinsic function results in severe deformity. Perhaps the most important intrinsic muscle, the adductor pollicis (Figure 2-18, A), originates from the third metacarpal and inserts on the ulnar side of the base of the proximal phalanx of the thumb and into the ulnar wing expansion of the extensor mechanism. This muscle, by virtue of its strong adducting influence on the thumb and its stabilizing effect on the first metacarpophalangeal joint, functions together with the first dorsal interosseous to provide strong pinch. The adductor pollicis, deep head of the flexor pollicis brevis, ulnar two lumbricals, and all interossei, as well as the

Anatomy and Kinesiology of the Hand • 35

Adductor pollicis Opponens digiti quinti

Abductor pollicis brevis

Flexor digiti quinti

Flexor pollicis brevis Transverse carpal ligament Opponens pollicis

Abductor digiti quinti

Flexor carpi ulnaris Pronator quadratus

A

4

3

2

Abductor digiti minimi

1

Dorsal interossei (1 to 4)

Ulnar nerve

Palmar interossei (1 to 3) 1

2

3

C

B Figure 2-18

Position and function of the intrinsic muscles of the hand.

hypothenar muscle group, are innervated by the ulnar nerve. Loss of ulnar nerve function has a profound influence on hand function.

Muscle Balance and Biomechanical Considerations When there is normal resting tone in the extrinsic and intrinsic muscle groups of the forearm and hand, the wrist and digital joints are maintained in a balanced position. With the forearm midway between pronation and supination, the wrist dorsiflexed, and the digits in moderate flexion, the hand is in the optimum position from which to function. It may be seen that muscles are usually arranged about joints in pairs so that each musculotendinous unit has at least one antagonistic muscle to balance the

involved joint. To a large extent the wrist is the key joint and has a strong influence on the long extrinsic muscle performance at the digital level. Maximal digital flexion strength is facilitated by dorsiflexion of the wrist, which lessens the effective amplitude of the antagonistic extensor tendons while maximizing the contractural force of the digital flexors. Conversely, a posture of wrist flexion markedly weakens grasping power. At the digital level, metacarpophalangeal joint flexion is a combination of extrinsic flexor power supplemented by the contribution of the intrinsic muscles, whereas proximal interphalangeal joint extension results from a combination of extrinsic extensor and intrinsic muscle power. At the distal interphalangeal joint the intrinsic muscles provide a majority of the

36

Part I • Foundation of Hand Skills Ulnar

Radial

Triangular ligament

Lateral band Slip of long extensor to lateral band

Dorsal extensor expansion

Sagittal bands Lumbrical muscle Long extensor tendon

Interosseous muscle

A Long extensor tendon Interosseous muscle

B

Sagittal bands

Dorsal extensor expansion Central slip of common extensor Lateral band

Flexor profundus tendon Lumbrical muscle Flexor digitorum superficialis

Long extensor tendon Sagittal bands Bony insertion of interosseous tendon on proximal phalanx

Interosseous muscle

Lumbrical muscle

Distal movement of extensor expansion during flexion

Lateral band

C Figure 2-19 A. Extensor mechanism of the digits. B, C. Distal movement of the extensor expansion with metacarpophalangeal joint flexion is shown.

Anatomy and Kinesiology of the Hand • 37 extensor power necessary to balance the antagonistic flexor digitorum profundus tendon. The distance that a tendon moves when its muscle contracts is defined as the amplitude of the tendon and has been measured in numerous studies. In actuality the effective amplitude of any muscle is limited by the motion permitted by the joint or joints on which its tendon acts. It has been suggested that the amplitude of wrist movers (flexor carpi ulnaris, flexor carpi radialis, extensor carpi radialis longus, extensor carpi radialis brevis, and extensor carpi ulnaris) is approximately 30 millimeters with the amplitude of finger extensors averaging 50 millimeters; the thumb flexor, 50 mm; and the finger flexors 70 millimeters (Figure 2-20). Although these amplitudes have been thought to be important considerations when deciding on appropriate tendon transfers, Brand (1974, 1999) has shown that the potential excursion of a given tendon such as the extensor carpi radialis longus may be considerably

0 mm

3 mm

16 mm

26 mm (S) 23 mm (P) 16 mm (S) 17 mm (P)

44 mm

55 mm

5 mm (P) 46 mm (S) 38 mm (P) 88 mm (S) 85 mm (P)

Figure 2-20 Excursion of the flexor and extensor tendons at various levels. The numbers on the dorsum of the extended finger represent the excursion in millimeters necessary at each level to bring all distal joints from full flexion into full extension. The numbers shown by arrows on the palmar aspect of the flexed digit represent the excursion in millimeters for the superficialis (S) and the profundus (P) necessary at each level to bring the finger from full extension to full flexion. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Verdan C [1979]. Tendon surgery of the hand. London, Churchill Livingstone.)

greater than the excursion that was necessary to produce full motion of the joints on which it acted in its original position. Efforts have been made to determine the power of individual forearm and hand muscles and a formula based on the physiologic cross section is generally accepted as the best method for determining this value. The number of fibers in cross section determines the absolute muscle power of a given muscle, whereas the force of muscle action times the distance or amplitude of a given muscle determines the work capacity of the muscle. Therefore a large extrinsic muscle with relatively long fibers such as the flexor digitorum profundus is found to be capable of much more work than is a muscle with shorter fibers such as a wrist extensor. Table 2-1 is an indicator of the work capacities of the various forearm muscles. It can be seen that the flexor digitorum profundus and superficialis have a significantly greater work capacity than do the remaining extrinsic muscles. The abductor pollicis longus, palmaris longus, extensor pollicis longus, extensor carpi radialis brevis, and flexor carpi radialis have less than one fourth the capacity of these muscles. Several mechanical considerations are important in understanding the effect of a muscle on a given joint. The moment arm of a particular muscle is the perpendicular distance between the muscle or its tendon and the axis of the joint. The greater the displacement of an unrestrained tendon from the joint on which it acts, the greater is the angulatory effect created by the increased length of the moment arm. Therefore a tendon positioned close to a given joint either by position of the joint or by a restraining pulley has a much shorter moment arm than a tendon that is allowed to displace away from the joint (Figure 2-21). In simplifying the biomechanics of musculotendinous function, Brand (1974, 1999) has emphasized that the “moment” of a given muscle is the power of the muscle to turn a joint on its axis. It is determined by multiplying the strength (tension) of the muscle by the length of the moment arm. Again, it can be seen that the distance of tendon displacement away from the joint is the critical factor and that it does not matter where the tendon insertion lies. The importance of the various anatomic restraints of the extrinsic musculotendinous units at the wrist and in the digits is magnified by these mechanical factors.

N ERVE SUPPLY In considering the nerve supply to the forearm, hand, and wrist, understand that these nerves are a direct continuation of the brachial plexus and that at least a working knowledge of the multiple ramifications of the

38

Part I • Foundation of Hand Skills

Table 2-1

MA

Normal

Work capacity of muscles

Muscle

Mkg 0.8

Extensor carpi radialis longus

1.1

PTE

A-4 C-1 A-3 C-2 C-3 A-5 IAPD

A-1

M

A

Flexor carpi radialis

A

A-2

IAPD PTE

Extensor carpi radialis brevis

90

0.9

B 1.1

Abductor pollicis longus

0.1

Flexor pollicis longus

1.2

Flexor digitorum profundus

4.5

Flexor digitorum superficialis

4.8

Brachioradialis

1.9

Flexor carpi ulnaris

2.0

Pronator teres

1.2

Palmaris longus

0.1

Extensor pollicis longus

0.1

Extensor digitorum communis

1.7

Abnormal MA

Extensor carpi ulnaris

1 % 2 A-4 1 % 2 A-2 IAPD

PTE

M

A

C

PTE

From Von Lanz T, Wachsmuth W (1970). Praktische anatomie. In JH Boyes, editor: Bunnell’s surgery of the hand, 5th ed. Philadelphia, Lippincott.

plexus is necessary if one is to fully appreciate the more distal motor and sensory contributions of the nerves of the upper extremity. Injuries at either the spinal cord or plexus level or to the major peripheral nerves in the upper extremity result in a substantial functional impairment for which splinting may be necessary. The median, ulnar, and radial nerves, as well as the terminal course of the musculocutaneous, are responsible for the sensory and motor transmission to the forearm, wrist, and hand. The superficial sensory distribution is shared by the median, radial, and ulnar nerves in a fairly constant pattern (Figure 2-22). This chapter is concerned with the most frequent distribution of

IAPD 90

D Figure 2-21 Biomechanics of the finger flexor pulley system. A. The arrangement of the annular and cruciate pulleys of the flexor tendon sheath. A, B, Normal moment arm (MA), the intra-annular pulley distance (IAPD) between the A-2 and A-4 pulleys, and the profundus tendon excursion (PTE), which occurs within the intact digital fibroosseous canal as the proximal interphalangeal joint is flexed to 90°. Annular pulleys: A-1, A-2, A-3, A-4, and A-5; cruciate pulleys: C-I, C-2, C-3. C, D, Biomechanical alteration resulting from excision of the distal half of the A-2 pulley together with the C-1, A-3, C-2, and proximal portion of the A-4 pulley. The moment arm is increased, and a greater profundus tendon excursion is necessary to produce 90° of flexion because of the bowstringing that results from the loss of pulley support. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Strickland JW [1983]. Management of acute flexor tendon injuries. Orthopaedic Clinics of North America, vol 14. Philadelphia, WB Saunders.)

these nerves, although it is acknowledged that variations are common. The palmar side of the hand from the thumb to a line passed longitudinally from the tip of the ring finger to the wrist receives sensory innervation from the median nerve. The remainder of the palm, as well as the ulnar half of the ring finger and the entire small finger, receives sensory innervation from the ulnar nerve. On the dorsal side, the ulnar nerve distribution again includes the ulnar half of the dorsal hand and the ring and small fingers, whereas the radial side is supplied by the superficial branch of the radial nerve. Some inner-

Anatomy and Kinesiology of the Hand • 39

Median

Median

Median

Ulnar Radial

Radial Ulnar nerve

A

Median nerve

Superficial branch of radial nerve

B

Figure 2-22 Cutaneous distribution of the nerves of the hand. A. Palmar surface. B. Dorsal surface. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

vation to an area distal to the proximal interphalangeal joints is supplied by the palmar digital nerves originating from the median nerve. The area around the dorsum of the thumb over the metacarpophalangeal joint is frequently supplied by the end branches of the lateral antebrachial cutaneous nerve. The extrinsic and intrinsic musculature of the forearm and hand is supplied by the median, ulnar, and radial nerves (Figure 2-23). The long wrist and digital flexors, with the exception of the flexor carpi ulnaris and the profundi to the ring and small fingers, are all supplied by the median nerve. The pronators of the forearm and the muscles of the thenar eminence, with the exception of the deep head of the flexor pollicis brevis and the adductor pollicis, which are innervated by the ulnar nerve, are also supplied by the median nerve. All muscles of the hypothenar eminence, all interossei, the third and fourth lumbrical muscles, the deep head of the flexor pollicis brevis, the adductor pollicis brevis, as well as the flexor carpi ulnaris and the ulnar-most two profundi, are supplied by the ulnar nerve. The radial nerve supplies all long extensors of the hand and wrist, as well as the long abductor and short extensor of the thumb, the supinator, and the brachioradialis of the forearm. When considering sensibility, one should remember that the hand is an extremely important organ for the detection and transmission to the brain of information relating to the size, weight, texture, and temperature of objects with which it comes in contact. The types of cutaneous sensation have been defined as touch, pain, hot, and cold. Although most of the nervous tissue

in the skin is found in the dermal network, smaller branches course through the subcutaneous tissue following blood vessels. Several types of sensory receptors have been described, and in most areas of the hand there is an interweaving of nerve fibers that allows each area to receive nerve input from several sources. In addition, deep sensibility from nerve endings in muscles and tendons is important in the recognition of joint position. The high interruption of the median nerve above the elbow results in a paralysis of the flexor carpi radialis, the flexor digitorum superficialis, the flexor pollicis longus, the profundi to the index and long fingers, and the lumbricals to the index and long fingers. In addition, pronation is weakened as a result of the loss of innervation of both the pronator teres and quadratus muscles and, most importantly, the patient loses the ability to oppose the thumb because of paralysis of the median nerve-innervated thenar muscle group. A more distal interruption of the median nerve at the wrist level produces loss of opposition and both lesions result in a critical impairment of sensation in the important distribution of that nerve to the palmar aspect of the thumb, index, long, and radial half of the ring finger. High ulnar nerve interruption produces paralysis of the flexor carpi ulnaris, the flexor profundi and lumbricals to the ring and small fingers and, most importantly, the interossei, adductor pollicis brevis, and deep head of the flexor pollicis brevis. The resulting loss of the antagonistic flexion at the metacarpophalangeal joints of the ring and small fingers permits

40

Part I • Foundation of Hand Skills

Proper palmar digital nerves

Common digital nerves Palmar nerves to thumb Motor (thenar) branch of median nerve Median nerve

A

Proper palmar digital nerves

Radial nerve lesions at or proximal to the elbow result in a complete wrist drop and inability to extend the fingers at the metacarpophalangeal joints. It should be remembered that paralysis of this nerve does not result in inability to extend the interphalangeal joints of either the thumb or digits because of the contribution to that function by the intrinsic muscles. The sensory deficit over the dorsoradial aspect of the wrist and hand resulting from radial nerve interruption is of much less significance than are lesions to nerves innervating the palmar side. Various combinations of paralyses involving more than one nerve of the upper extremity are frequently encountered; those of the median and ulnar nerve are the most common. High lesions of these two nerves produce paralyses of both the extrinsic and intrinsic muscle groups with total sensory loss over the palmar aspect of the hand. More distal combined median and ulnar lesions have their effect primarily on the intrinsic muscles, resulting in the most disabling deformities with metacarpophalangeal hyperextension, interphalangeal flexion, and thumb collapse. An inefficient pattern of digital flexion consisting of a slow distal-toproximal rolling grasp results from the loss of the integrated intrinsic participation.

SKIN AND SUBCUTANEOUS FASCIA Proper palmar digital nerve to fifth finger Common digital nerve to ring and small fingers

Motor (deep) branch of ulnar nerve

Ulnar nerve

B Figure 2-23 Distribution of the median (A) and ulnar (B) nerves in the palm. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

hyperextension at this level by the unopposed long extensor tendons, often resulting in a claw deformity. The loss of the strong adducting and stabilizing influence of the adductor pollicis combined with the paralysis of the first dorsal interosseous muscle results in profound weakness of pinch and produces a collapse deformity of the thumb, necessitating interphalangeal joint hyperflexion for pinch (Froment’s sign). More distal lesions of the ulnar nerve usually result in a greater degree of claw deformity because of the sparing of the profundi function of the ring and small fingers. Sensory loss after ulnar nerve interruption involves the palmar ring (ulnar half) and small fingers.

The palmar skin with its numerous small fibrous connections to the underlying palmar aponeurosis is a highly specialized, thickened structure with little mobility. Numerous small blood vessels pass through the underlying subcutaneous tissues into the dermis. In contrast, the dorsal skin and subcutaneous tissue are much looser with few anchoring fibers and a high degree of mobility. Most of the lymphatic drainage from the palmar aspect of the fingers, web areas, and hypothenar and thenar eminences flows in lymph channels on the dorsum of the hand. Clinical swelling, which frequently accompanies injury or infection, is usually a result of impaired lymph drainage. The central, triangularly shaped palmar aponeurosis (Figure 2-24) provides a semirigid barrier between the palmar skin and the important underlying neurovascular and tendon structures. It fuses medially and laterally with the deep fascia covering the hypothenar and thenar muscles, and fasciculi extending from this thick fascial barrier extend to the proximal phalanges to fuse with the tendon sheaths on the palmar, medial, and lateral aspects. In the distal palm, septa from this palmar fascia extend to the deep transverse metacarpal ligaments forming the sides of the annular fibrous canals, allowing for the passage of the ensheathed flexor tendons and the lumbrical muscles and the neurovascular bundles.

Anatomy and Kinesiology of the Hand • 41

Palmar aponeurosis (reflected)

Flexor digitorum superficialis

Sheath of flexor pollicis longus

Ulnar artery Ulnar nerve

Median nerve Thenar muscles

Transverse carpal ligament

As generally stated, power grip is a combination of strong thumb flexion and adduction with the powerful flexion of the ring and small fingers on the ulnar side of the hand. The radial half of the hand employing the delicate tripod of pinch among the thumb, index, and long fingers is responsible for more delicate precision function. An analysis of hand functions requires that one consider the thumb and the remainder of the hand as two separate parts. Rotation of the thumb into an opposing position is a requirement of almost any hand function, whether it is strong grasp or delicate pinch. The wide range of motion permitted at the carpometacarpal joint is extremely important in allowing the thumb to be correctly positioned. Stability at this joint is a requirement of almost all prehensile activities and is ensured by a unique ligamentous arrangement, which allows mobility in the midposition and provides stability at the extremes. As can be seen in Figure 2-25, the thumb moves through a wide arc from the side of

Figure 2-24 Palmar aponeurosis reflected distally reveals septa and underlying palmar anatomy.

Dorsally the deep fascia and extensor tendons fuse to form the roof for the dorsal subaponeurotic space, which, although not as thick as its palmar counterpart, may prove restrictive to underlying fluid accumulations or intrinsic muscle swelling.

FUNCTIONAL PATTERNS The prehensile function of the hand depends on the integrity of the kinetic chain of bones and joints extending from the wrist to the distal phalanges. Interruptions of the transverse and longitudinal arch systems formed by these structures always result in instability, deformity, or functional loss at a more proximal or distal level. Similarly, the balanced synergism–antagonism relationship between the long extrinsic muscles and the intrinsic muscles is a requisite for the composite functions necessary for both power and precision functions of the hand. It is essential to recognize that the hand cannot function well without normal sensory input from all areas. Many attempts have been made to classify the different patterns of hand function, and various types of grasp and pinch have been described. Perhaps the more simplified analysis of power grasp and precision handling as proposed by Napier (1955, 1956) and refined by Flatt (1979, 1983, 1995) is the easiest to consider.

Figure 2-25 Progressive alterations in precision grasp with changes in object size. Adaptation takes place primarily at the carpometacarpal joint of the thumb and the metacarpophalangeal joints of the digits. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

42

Part I • Foundation of Hand Skills

the index finger tip to the tip of the small finger, and the adaptation that occurs between the thumb and digits as progressively smaller objects are held occurs primarily at the metacarpophalangeal joints of the digits and the carpometacarpal joint of the thumb. For power grip the wrist is in an extended position that allows the extrinsic digital flexors to press the object firmly against the palm while the thumb is closed tightly around the object. The thumb, ring, and small fingers are the most important participants in this strong grasp function, and the importance of the ulnar border digits cannot be minimized (Figure 2-26). In precision grasp, wrist position is less important, and the thumb is opposed to the semiflexed fingers with the intrinsic tendons providing most of the finger movement. When the intrinsic muscles are paralyzed, the balance of each finger is markedly disturbed. The metacarpophalangeal joint loses its primary flexors, and the interphalangeal joints lose the intrinsic contribution to extension. A dyskinetic finger flexion results in which the metacarpophalangeal joints lag behind the interphalangeal joints in flexion. When the hand is closed on an object, only the fingertips make contact rather than the uniform contact of the fingers, palm, and thumb that occurs with normal grip (Figure 2-27). Certain activities may require combinations of power and precision grips, as seen in Figure 2-28. Pinching between the thumb and either the index or long finger is a further refinement of precision grip and may be classified as tip grip, palmar grip, or lateral grip (Figure 2-29), depending on the portions of the phalanges brought to bear on the object being handled. In these functions the strong contracture of the adductor pollicis brings the thumb into contact against the tip or sides of the index or index and long fingers with digital

Figure 2-26 Strong power grip imparted primarily by the thumb, ring, and small fingers around the hammer handle with delicate precision tip grip employed to hold the nail. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

A

B Figure 2-27 A. Normal hand grasping a cylinder. Uniform areas of palm and digital contact are shaded. B. Intrinsic minus (claw hand grasping the same cylinder). The area of contact is limited to the fingertips and the metacarpal heads. (From Brand PW [1999]. Clinical mechanics of the hand, 2nd ed. St Louis, Mosby.)

resistance imparted by the first and second dorsal interossei. The size of the object being handled dictates whether large thumb and digital surfaces, as in palmar grip, or smaller surfaces, as in lateral or tip grasp, are used. Flatt (1972) has pointed out that the dual importance of rotation and flexion of the thumb is often ignored in the preparation of splints, which permit only tip grip because the thumb cannot oppose the pulp of the fingers to produce palmar grip. The patterns of action of the normal hand depend on the mobility of the skeletal arches, and alterations of the configuration of these arches are produced by the balanced function of the extrinsic and intrinsic muscles. Whereas the extrinsic contribution resulting from the large powerful forearm muscle groups is more important to hand strength, the fine precision action imparted by the intrinsic musculature gives the hand an enormous variety of capabilities. Although one need

Anatomy and Kinesiology of the Hand • 43 original unabridged work may be found in Fess EE, Gettle KS, Philips CA, Janson JR (2005). Hand and upper extremity splinting: Principles and methods, 3rd ed. St Louis, Mosby.

REFERENCES

Figure 2-28 Power grip used to hold the squeeze bottle with precision handling of the bottle top by the opposite hand. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby.)

A

B

C

Figure 2-29 Types of precision grip. A. Tip grip. B. Palmar grip. C. Lateral grip. (From Fess EE, Gettle K, Philips CA, et al. [2005]. Hand and upper extremity splinting. St Louis, Mosby. Modified from Flatt AE [1974]. The care of the rheumatoid hand, 3rd ed. St Louis, Mosby.)

not specifically memorize the various patterns of pinch, grasp, and combined hand functions, it is essential to understand the underlying contribution of the various muscle-tendon groups, both extrinsic and intrinsic, to these activities.

ACKNOWLEDGMENTS I am extremely grateful to Gary W. Schnitz for many of the excellent illustrations used in this chapter. This chapter has been edited by Elaine Ewing Fess, MS, OTR, FAOTA, CHT for inclusion in this book. The

Arey L (1980). Developmental anatomy, 7th ed. Philadelphia, WB Saunders. Basmajian JU (1980). Electromyography—dynamic gross anatomy: A review. American Journal of Anatomy, 159:245–260. Bell-Krotoski J (1990). Light touch-deep pressure testing using Semmes-Weinstein monofilaments. In J Hunter, L Schneider, E Mackin, A Callahan, editors. Rehabilitation of the hand, 3rd ed. St Louis, Mosby. Blumfield RH, Champoux JA (1984). A biomechanical study of normal functional wrist motion. Clinical Orthopedics, 187:23–25. Bora FW (1986). The pediatric upper extremity. Philadelphia, WB Saunders. Brand PW (1974). Biomechanics of tendon transfer. Orthopedic Clinics of North America 5:202–230. Brand PW, Hollister A (1999). Clinical mechanics of the hand, 3rd ed. St Louis, Mosby. Bunnell S (1944). Surgery of the hand. Philadelphia, JB Lippincott. Cooney W, Linscheid R, Dobyns J (1998). The wrist diagnosis and operative treatment. St Louis, Mosby. Flatt AE (1972). Restoration of rheumatoid finger joint function. III. Journal of Bone & Joint Surgery, 54A:1317–1322. Flatt AE (1979). The care of minor hand injuries. St Louis, Mosby. Flatt AE (1983). Care of the arthritic hand. St Louis, Mosby. Flatt AE (1995). The care of the arthritic hand, 5th ed. St Louis: Quality Medical Publishing. Lichtman D, Alexander A (1988). The wrist and its disorders. Philadelphia, WB Saunders. Long C, Conrad MS, Hall EA, Furler MS (1970). Intrinsicextrinsic muscle control of the hand in power grip and precision handling. Journal of Bone & Joint Surgery, 52A:853–867. Moberg E (1958). Objective methods of determining the functional value of sensibility of the hand. Journal of Bone & Joint Surgery, 40B:454–476. Moore KL (1982). The developing human: Clinically oriented embryology, 3rd ed. Philadelphia, WB Saunders. Napier J (1955). The form and function of the carpometacarpal joint of the thumb. Journal of Anatomy, 89:362. Napier JR (1956). The prehensile movements of the human hand. Journal of Bone & Joint Surgery, 38B:902–913. Taleisnik J (1976a). Wrist anatomy, function, and injury. American Academy of Orthopedic Surgeons’ Instructional Course Lectures, vol. 27. St Louis, Mosby. Taleisnik J (1976b). The ligaments of the wrist. Journal of Hand Surgery [America] 1:110–118. Taleisnik J (1985a). The wrist. New York, Churchill Livingstone. Taleisnik J (1985b). Carpal kinematics. In The wrist. New York, Churchill Livingstone.

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Taleisnik J (1992). Soft tissue injuries of the wrist. In JW Strickland, AR Rettig, editors: Hand injuries in athletes. Philadelphia, WB Saunders. Weber ER (1982). Concepts governing the rotational shift of the intercalated segment of the carpus. Orthopedic Clinics of North America, 15:193–207. Weber ER (1988). Physiologic bases for wrist function. In D Lichtman, A Alexander, editors: The wrist and its disorders. Philadelphia, WB Saunders.

SUGGESTED READINGS Chase RA (1973). Atlas of hand surgery. Philadelphia, WB Saunders. Chase RA (1984). Atlas of hand surgery, vol. 2. Philadelphia, WB Saunders. Clemente CD (editor) (1990). Gray’s anatomy of the human body, 14th ed. Philadelphia, Lea & Febiger. Hollingshead HW (editor) (1982). Anatomy for surgeons, vol 4. The back and limbs. New York, Harper & Row.

Kaplan EB (1965). Functional and surgical anatomy of the hand, 2nd ed. Philadelphia, JB Lippincott. Landsmere J (1976). Atlas of anatomy of the hand. Edinburgh, Churchill Livingstone. Mackin E, Callahan A, Skirven TM, Schneider L, Osterman AL (editors) (2002). Hunter, Mackin, & Callahan’s rehabilitation of the hand and upper extremity, 5th ed. St Louis, Mosby. Matsen FA, Fu FH, Hawkins RJ (1993). The shoulder: A balance of mobility and stability, Rosemont, IL, American Academy of Orthopedic Surgeons. Morrey BF (2000). The elbow and its disorders, 3rd ed. Philadelphia, WB Saunders. Rasch P, Burke R (1990). Kinesiology and applied anatomy, 9th ed. Philadelphia, Lea & Febiger. Rockwood CA, Matsen FA, Wirth MA, Lippitt SB (editors) (2004). The shoulder, 3rd ed. Philadelphia, WB Saunders. Zancolli E (1968). Structural and dynamic basis of hand surgery. Philadelphia, JB Lippincott.

Chapter

3

NORMAL AND IMPAIRED DEVELOPMENT OF FORCE CONTROL IN PRECISION GRIP Ann-Christin Eliasson

CHAPTER OUTLINE DEVELOPMENT OF MOVEMENT CONTROL THEORIES LEARNED MOVEMENTS AFFERENT INFORMATION Proprioception Touch BASIC COORDINATION OF FORCES DURING GRASPING Development of Manipulatory Forces DEVELOPMENT OF ANTICIPATORY CONTROL Weight Size Friction ORGANIZATION OF SENSORIMOTOR CONTROL IMPAIRED FORCE CONTROL AND CLINICAL IMPLICATIONS Force Coordination Anticipation of the Properties of Objects Sensory Information Used for Force Control SUMMARY

The hand is an effective tool that is used in many different tasks of daily life. The successful performance of manual skills in daily life depends on a complex process incorporating several different aspects of a person’s capability (Figure 3-1). The usefulness of the hand is highly dependent on cognition because one has to understand the value of using one’s hands for a

meaningful purpose. Then the task to be performed has to be encoded and translated into purposeful actions, and these must be performed in the appropriate order. In the last decade, considerable attention has been given to the development of prehensile force control during the manipulation of objects in both healthy children and children with cerebral palsy (CP), as well as attention deficit hyperactivity disorder (ADHD) and other kinds of dysfunctions related to the central nervous system (CNS). It is known that integration of somatosensory information is crucial for the fine tuning of motor commands, force regulation, and the build up of memory strategies for grasping and manipulating objects. Coordination of movements and somatosensory control develop rapidly during the first years of life. The refinement continues for many years, and adult-like sensorimotor control is not attained until the early teenage years. If somatosensory control is dysfunctional, a person is observed to be clumsy to a greater or lesser degree. Furthermore, people’s perceptions have an effect on their performance of manual skills because their sensory impressions should be translated into meaningful information even for the very simplest of tasks. The perceptual system provides information about the position of the hand in space, as well as the position of the target, both of which are important for goal-directed movement. Finally, the musculoskeletal components are crucial for motor output. Although any movement a person brings about is highly dependent on how the CNS plans and organizes the movement, the contractile components of the muscles, bones, and joints are the effectors of the planned movement. Another cognitive aspect is motivation, which is closely related to attention and concentration, and all of which have an influence on the successful performance of manual skills. A reduced focus on a task almost certainly limits the ability to learn. Thus self-efficacy

45

46

Part I • Foundation of Hand Skills Motivation

Sensorimotor system

Cognition Task-comprehension

Perception

Attention Task-focus Hand use

Muscles and skeletal system Self-efficacy

Figure 3-1 Descriptive illustration of components influencing children’s ability to use their hands. (From Eliasson AC (2004). Improving the use of the hands in daily activities: aspects of the treatment of children with cerebral palsy. Physical and Occupational Therapy in Pediatrics, 25:37–60.)

and body image have an impact on one’s ability to perform tasks. Although the performance of manual skills is complex, this chapter discusses how the sensory information received about an object is increasingly well integrated with motor processing during development, leading to smooth, coordinated movements of the hand. This chapter also describes how impairment, mainly arising from CP, but also from dysfunctions such as those seen in children with ADHD and developmental coordination disorder (DCD) affects sensorimotor control of the hand. Dysfunction or impairment of the CNS almost always affects hand function. There is a continuum of decreasing hand function from being somewhat clumsy to having severe impairment. It seems that the diagnosis is less important; it is the grade of impairment or dysfunction that is crucial. Children with CP have different degrees of impaired hand function. Some children only have difficulty performing differentiated finger movements or in-hand manipulation, whereas others have severe impairments that make it impossible even to grasp an object. Most children with ADHD have fairly good hand function, but when DCD is present also, the clumsiness is more apparent. Regardless of the degree of severity, decreased hand function has an impact on children’s daily self-care or school activities, and it affects their engagement in play or leisure. The ability to analyze a child’s capacity to use his or her hands and compare the child’s capabilities with the complexity of the task is a prerequisite for intervention planning. This chapter explains the underlying causes of the impairment or clumsiness apparent in children with impairment or dysfunction in their CNS. By understanding the mechanisms normally responsible for controlling movements, intervention that takes into consideration the mechanism controlling manual skills can be planned. Some examples of this are given later in this chapter.

DEVELOPMENT OF MOVEMENT CONTROL THEORIES At the beginning of this century, sensory stimuli were thought to be responsible for the generation of movements. This concept was based on studies by Mott and Sherrington (1895) on deafferented monkeys. By transecting the dorsal roots, researchers cut sensory fibers and left the motor fibers intact. The complete sensory loss resulted in permanent abolishment of almost all voluntary movements, especially in the distal segments. A model was proposed in which the movements were generated by chain reflexes; the sensory information from the first muscle contraction elicited the subsequent spinal reflex. This reflex origin of movement was disputed by Brown (1911), who studied locomotion in spinal cats. He suggested instead a central origin in which neuronal networks could generate basic locomotor activity in the absence of sensory information (half center model). The task of the afferents was restricted to modifying and compensating for ongoing movements. However, it took quite a long time before this idea was confirmed. Nowadays there are several elegant studies that indicate that innate neural networks control rhythmic motor behavior in a variety of species such as locusts, lampreys, and cats (Forssberg, Grillner, & Halbertsma, 1980; Forssberg et al., 1980; Grillner, Wallen, & Brodin, 1991; Wilson, 1964). Neural networks, called central pattern generators (CPGs), consist of a group of interneurons that interact in an organized manner to produce a motor act. Detailed knowledge of how one CPG operates has been demonstrated in the lamprey, a primitive vertebrate fish. The lamprey is especially suited for such studies because the spinal cord survives in vitro for several days, and neurons involved in the locomotor network for swimming are visible under the micro-

Normal and Impaired Development of Force Control in Precision Grip • 47 scope, which facilitates microelectrode recording. The swimming can be initiated by stimulation of specific areas in the brainstem, sensory stimuli if some skin areas are left innervated, and bath-applied excitatory amino acids. Information about the networks also has been used for computer simulation (Grillner et al., 1991). The central origin of motor behavior has been further demonstrated in other rhythmic movements, such as mastication, swallowing, and respiration (Feldman & Grillner, 1983; Lund & Olsson, 1983; Miller, 1972). Swallowing occurs after the denervation of muscles activated early in the sequence, indicating that the brain sets the motor program for the whole motor act in advance. However, this does not diminish the importance of afferent signals for modulation and learning of movements. Movements are activated by efferent signals from several higher levels of the CNS, which are modulated by afferent signals from the sensory system and by visual, auditory, and somatosensory information. There are many reasons to believe that the human nervous system is organized in the same way. Spontaneous movements in the human fetus appear from the eighth gestational week, just after the first functional synapses between neurons are developed. The movements seem to be generated by neural networks, and the afferents may not be needed for initiating the movements but are used mainly to adjust and compensate for disturbances (de Vries, Visser, & Pechtl, 1982; Okado, 1980, 1981). Innate motor programs, such as breathing, sucking, and swallowing, function at birth. The complex pattern of infant stepping also is innate, but this program is immature in the newborn and cannot be used for independent walking until the child has learned to control and adjust the patterns to external conditions. The system develops both through practice and by the process of maturation, in which connections with higher central and afferent sensory input continue to be established. This is the concept from which new therapeutic approaches are developed.

LEARNED MOVEMENTS Voluntary movements in humans are complex. It is difficult to demonstrate a simple fixed pattern from a CPG, although skilled movements appear to depend on a set of motor programs. According to Brooks (1986), “Motor programs are a set of muscle commands that are structured before the motor acts begin and that can be sent to the muscles with the correct timing so that the entire sequence can be carried out in the absence of peripheral feedback” (p. 7),

or, in other words, can follow an initial plan. In welllearned, fast movements the trajectory exactly follows this initial plan. The initiation and termination are

planned together, and the movements are almost impossible to stop until completed. This is true, for example, when throwing a ball and in more complex actions, such as typing. Even continuous movements of moderate speed, such as handling well-known objects, are programmed but allow some amount of sensory feedback. Both kinds of movements are called anticipatory or feed-forward controlled movements, with the characteristic bell-shaped, single-peaked velocity profile (see later discussions). Slow movements generally are not programmed, allowing time for correction of the ongoing movement by afferent signals, and demonstrated by a discontinuous velocity profile (Brooks, 1986). The motor programs are learned by practice when the afferent information adjusts the ongoing movement and updates the motor program for the final movement. The importance of sensory information is demonstrated by birdsong learning in the European chaffinch. Normally, the young birds are exposed to singing by their mothers but do not start singing themselves until 10 months of age. If the birds are not exposed to the adult song, they produce only rudimentary sequences. If the birds are exposed to adult song during the first 4 months of life and then isolated from songs during the month after, they start to sing properly. This indicates that auditory experience is necessary for the motor program to be fully developed. If the birds are deafened after 4 months but before they start to sing, they sing in a very awkward way. Deafening after they start to sing, however, does not affect the song. This indicates that birds also must compare the initial motor program for singing with the actual song, that is, afferent information also is necessary to be able to learn to use the program of singing. The afferent information corrects the song and updates the program, which could be used without afferent feedback when the song was established (Konishi, 1965; Nottebohm, 1970).

AFFERENT INFORMATION The importance of afferent information is seen in patients with large sensory fiber neuropathies, in which the large afferent fibers generating proprioceptive and tactile information degenerate. Unless these patients see their limbs, they do not know their position and cannot detect limb motion. When reaching toward a target without seeing the moving hand, they make large errors; if they look at the hand before reaching, the hand comes closer to the target. This indicates that these patients can compensate for the lack of somatosensory information visually and also use vision to program the reaching in advance. Because the patients cannot stop the movement precisely at the desired

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target, information from various receptors in the skin is essential for precise movements (Ghez et al., 1990). Impaired sensation is also common in children with hemiplegic CP and has to be taken into account when planning treatment.

PROPRIOCEPTION The proprioceptive system gives information about the stationary position of the limbs (limb position sense) and movements of the limb (kinesthesia). The latter information is mediated from tendon organs and muscle spindles and also from receptors in the skin, sensitive to skin stretch. The tendon organ signals information about the strength of muscle contraction, increased signaling indicating increased tension. Signals from the muscle spindle regulate the length of the muscle fibers. The receptors are rather complicated and, despite intensive research, their function is not fully understood. It has been agreed, however, that the muscle spindle is responsible for small changes in muscle contraction, which may be important for force regulation during the grasping act. There are muscle spindles in almost all skeletal muscles, and they mediate information mainly through 1a afferents to the spinal cord. The muscle spindle also has efferent innervation to intrafusal muscle fibers, in which the primary and secondary endings set the sensitivity to the afferent signals. The different contractions of intrafusal muscle fibers are probably crucial for the information sent to the CNS. Alpha and gamma motor neurons are co-activated by central mechanisms to maintain the sensitivity of the muscle spindles throughout the range of almost all movements. There have been different models for the coactivation of alpha and gamma motor neurons, but it appears that descending commands activate both, as demonstrated by Vallbo (1970) in studies of microneurography. The afferent signals are used to update and correct the motor programs, and the information can be used in a conscious way to give knowledge about the limb movement and position in space.

TOUCH The tactile system is used to discriminate between different surfaces and shapes and also provides sensory input to the CNS, which regulates the force of the muscles during grasping and holding of objects. Touch transmits nerve impulses from mechanoreceptors to the CNS via axons with different diameters. Large fibers with a fast conduction rate mediate tactile sensation from the skin, whereas thin fibers with a slow conduction rate mediate sensation of pain and temperature. The receptors mediating tactile sensation can be classified on the basis of their receptive fields and

morphology: Two receptor types, Meissner and Pacini corpuscles, are fast adapting; Meissner corpuscles have small, sharply delineated sensory fields; and Pacini corpuscles have large and diffuse sensory fields. Two other types of receptors that are slow-adapting units are Merkel corpuscles, with small and sharply delineated sensory fields, and Ruffini corpuscles, with large and diffuse fields. Mechanoreceptors with small receptive fields are suitable for fine spatial discrimination because they have a high sensitivity over the entire field, whereas mechanoreceptors with large receptive fields have a central area of high sensitivity and decreased sensitivity in the border of the receptive field. Because there are about 17,000 tactile units in the hand and approximately 70% of them have small receptive fields, it can be postulated that the tactile system of the hand is highly developed to detect small movements and discriminate among different surfaces (Johansson & Vallbo, 1983). People explore the surface of an object by manipulation of the fingers. The difference between exploring known and unknown surfaces is the speed of the finger movements (Roland, Ericsson, & Widen, 1989). A relevant movement for exploring the different surfaces of an object is by touch through digital manipulation, whereas a more adequate way to explore the shape is by rotation of the wrist and bimanual hand activity. The fingertips are very sensitive to tactile information, and tactile discrimination occurs early during development. One-year-old children can recognize dissimilar objects, and they are able to use the two different exploratory maneuvers for objects differing in texture or shape (Ruff, 1984). Newborn monkeys can distinguish different textures by choosing the texture that gives milk (Carlson, 1984). These examples indicate that, despite an immature nervous system, there is early interaction between somatosensory signals and motor output.

BASIC COORDINATION OF FORCES DURING GRASPING During the last decade Johansson and Westling (1984, 1987, 1988, 1990) have studied grasping movement to understand how somatosensory information is integrated with motor control. In adults, movements of the hand and fingers are precise and the forces of the fingers well controlled. This is not an innate behavior; in fact, these functions develop during early childhood and may be dysfunctional if there is impairment in the CNS (Eliasson & Gordon, 2000; Eliasson, Gordon, & Forssberg, 1991, 1992, 1995; Forssberg et al., 1991, 1992, 1995, 1999; Gordon et al., 1992).

Normal and Impaired Development of Force Control in Precision Grip • 49 Most grasping acts involve lifting and holding objects, grasping with the fingers, and lifting with the arm. The object seen in Figures 3-2 and 3-3 measures grip force from each grip surface (thumb and index finger), a combined vertical load force by strain-gauge transducers, and vertical movement by a photoresistor (Eliasson et al., 1991). With this instrument it has been possible to define different phases of the lift and under-

Figure 3-2

stand how they are linked to produce smooth movements. When grasping the instrument, there is a short delay before the vertical load force starts to increase. This preload phase is important for establishment of the grasp. During the loading phase the grip and load forces increase in parallel until the instrument starts to move. The rates of grip and load forces have mainly bell-shaped profiles (see later discussion) adjusted to

Child lifting the experimental object.

Figure 3-3 Experimental instrument in which the grip surfaces are exchangeable and the weight can be covaried without any visual changes.

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the weight, size, and frictional character of the surface of the object. After the loading phase there is a transition phase, in which the lift reaches the final position and the forces are well adjusted to the current properties of the object. In the final static phase the object is held in the air (Figure 3-4). Tactile information triggers different motor commands and links the different phases together. The different types of receptors respond differently during the lift, which has been demonstrated by microneurography from single tactile units innervating the glabrous skin of the fingers. Fast-adapting receptors send bursts of impulses when first touching an object,

1 Year

at the beginning of the loading phase and at lift-off but are silent during the static phase. Slow-adapting receptors send impulses continuously during the static phase (Johansson & Vallbo, 1983). This ability makes it possible to handle small fragile objects without crushing them. To investigate how separate components affect the grasping act, the object has a slot in which blocks of different weights may be inserted while the visual appearance remains constant; the contact pads can be covered with silk or sandpaper, each having different frictional character, and the size can be adjusted by boxes of different size attached to the instrument (see Figure 3-3).

6 Years

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Figure 3-4 Superimposed traces of representative lifts performed at different ages and in three children with cerebral palsy with various degree of severity. Grip force, load force, position, and grip force rate are shown as functions of time. When lifting the object, the grip force starts to increase; then the grip force and load force increase until the object starts to move. When the forces overcome gravity, the signal measuring position increases, followed by a static phase when the object is held in the air. (Modified from Forssberg H, Eliasson AC, Kinoshita H, Johansson RS, Westling G [1991]. Development of human precision grip. I. Basic coordination of force. Experimental Brain Research, 85:451–457; Forssberg H, Eliasson AC, Redon-Zouiteni C, Mercuri C, Dubowitz L [1999]. Impaired grip-lift synergy in children with unilateral brain lesions. Brain, 122:1157–1168.)

Normal and Impaired Development of Force Control in Precision Grip • 51

DEVELOPMENT OF MANIPULATORY FORCES During the loading phase, just before the movement starts, the grip and load forces are generated in parallel for coordinated movements. This parallel increment of both grip and load force increases with heavier objects, resulting in prolonged latency until lift-off. If the contact surface changes, the grip force increases more for slippery materials compared with rough materials, whereas the load force remains the same. Still the forces increase in parallel but with different slope. This parallel force generation forms a lifting synergy to simplify movements (Bernstein, 1967). It develops from the second year when the pincer grasp is fully developed. Smaller children cannot generate grip and load forces in parallel; they initiate forces sequentially. This is clearly seen in Figure 3-5; most of the grip force increases before the onset of load force. The force rate profile is irregular and has several peaks in young children, whereas older children and adults perform mainly a bell-shaped force rate profile, adjusted to the

weight of the object at lift-off, indicating anticipatory controlled movements (Brooks, 1986; Forssberg et al., 1991). Small children also have more variation than adults because they cannot repeatedly produce similar movements. However, 1-year-old children can use tactile and proprioceptive information to adjust the forces by sensory feedback during the static phase. All phases are prolonged, and the different phases are not triggered elegantly as in adults (Forssberg et al., 1995). There is an increased difference between thumb and finger contact, probably because of an immature ability to adjust the finger toward the object’s size (von Hofsten & Ronnquist, 1988). This uncoordinated movement in small children is likely attributable to immature motor output and sensory processing. There is rapid development until age 2. The refined coordination then progressively develops until leveling out at ages 4 to 6 and continues gradually until the teenage years, when the lifts are completely adult-like (see Figure 3-4) (Forssberg et al., 1991).

Grip Force 2N

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HEMIPLEGIA

Figure 3-5 Grip force during the preload and the loading phase (before lift-off) is plotted against load force in children of different ages and children with cerebral palsy. Trials are superimposed for each subject. (Modified from Forssberg H, Eliasson AC, Kinoshita, H, Johansson RS, Westling G [1991]. Development of human precision grip. I. Basic coordination of force. Experimental Brain Research, 85:451–457; Eliasson AC, Gordon AM, Forssberg H [1991]. Basic coordination of manipulative forces in children with cerebral palsy. Developmental Medicine and Child Neurology, 33:661–670.)

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DEVELOPMENT OF ANTICIPATORY CONTROL Peak Grip Force Rate (N/s)

100

SIZE Anticipatory control also is predicted from visual information about an object’s size (Gordon et al., 1991a,b). When the object is kept proportional to the volume,

60 40 20

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WEIGHT When the weight of the object is varied but the visual appearance remains constant, adults typically scale the grip and load force rates based on earlier experience of the object’s weight. This is indicated by higher grip and load force rates for heavier objects. The forces are decreased at lift-off to harmonize with the weight of the object. The anticipatory mechanism can be further demonstrated when lifting an unexpectedly light object. For example, if one lifts an unopened but empty can of soda, the lift will probably be too high because a heavier can is expected. However, this occurs only once for the same can. Somatosensory information adjusts the forces to the object’s actual weight during the static phase and updates the internal representation of the object for a smooth movement the next time the object is lifted. Children cannot handle this type of situation as efficiently as adults. However, despite uncoordinated force generation and large variation of grip and load force rates, 2-year-old children start to scale the forces toward different weights. It takes several years until the anticipatory control of weight is fully developed. Children between the ages of 6 and 8 are nearly adultlike although the variation is still larger than in adults (Figure 3-6). This indicates that anticipatory scaling of forces occurs in conjunction with maturation of coordinated movement (Forssberg et al., 1992).

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Anticipatory control of manipulation apparently requires the nervous system to efficiently use sensory information to integrate and store information for internal representation or memory representation of an object. This internal representation is necessary to produce rapid and well-coordinated transitions between the various movement phases because of a long delay between motor command and sensory feedback. This is true for reaching, grasping, and lifting movements, as well as for movement involving the whole body. In the lifting task the motor output is based on internal representation of the object’s properties learned by prior experience of the weight, friction, size, and haptic cues of the object (Gordon et al., 1991a,b; Johansson & Westling, 1990).

200 800

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Figure 3-6 Influence of the 200- and 800-g weight (400 g for 1- to 2-year-old children) in the constant lifting series for peak grip force rate (A) and peak acceleration (B). The means and standard error of means of the individual means for each subject indicate the major changes during development. (Modified from Forssberg H, Kinoshita H, Eliasson AC, Johansson RS, Westling G [1992]. Development of human precision grip. II. Anticipatory control of isometric forces targeted for object’s weight. Experimental Brain Research, 90:393–398).

there are appropriately scaled forces toward the expected weight relative to the volume. When only the size of the object is co-varied and the weight is kept constant, the employed grip force rate is higher for the larger than the smaller object. However, adults and older children perceive the small objects as heavier. This indicates a dichotomy between the perceptual and motor systems because of the size-to-weight illusion (Charpentier, 1891). People predict a big object to be heavier than a small one, yet this is not always true. This understanding of the discrepancy between size and weight and a proper scaling of the motor output starts to develop at 3 years. Children younger than 3 are not able to control the motor output according to size but do use a higher grip force rate for heavier

Normal and Impaired Development of Force Control in Precision Grip • 53 Safety Margin 300

sp si

250 200 Percent

objects. This suggests that the associative transformation between the object’s size and weight involves additional demands of cortical processes, requiring further cognitive development. In children 3 to 7 years of age the difference between large and small objects is greater than in adults. Older children seem capable of reducing the effect if it is not purposeful for manipulation, whereas younger children still strongly rely on visual information (Gordon et al., 1992).

150 100 50

FRICTION Tactile influence on the force coordination is available on touching an object, contrary to weight influence, which is not available until lift-off. Tactile information from fingertips triggers prestructured motor commands based on sensorimotor memories and adjusts the force coordination based on the friction of the contact surface. The employed grip forces are different when one holds a slippery bottle than when holding a tool covered with rubber, even if they have the same weight. When contact pads on the test object are altered by exchangeable contact surfaces of silk and sandpaper, the relationship between grip force and load force is changed before lift-off. In adults there is an initial adjustment to the new frictional condition during the first 0.1 second and secondary adjustments during the loading and static phases (Johansson & Westling, 1987). These adjustments are important in establishing an adequate safety margin, which prevents one from dropping the object. The ratio between grip and load force actually used, minus the slip ratio necessary to prevent the object slipping out of the hand, makes up the safety margin. One-year-old children have a larger safety margin than adults. Gradually, the safety margin decreases in conjunction with increased coordination and less variability during the first 5 years (Figure 3-7). Some children of 18 months can scale the grip force based on tactile information in the beginning of the lift. They have a higher grip force for slippery materials than for rough ones during consecutive lifts with the same friction. Several years are necessary before children can handle objects with different frictional surfaces in the same elegant way as adults. Children younger than 6 years of age, sometimes up to 10 or 12 years, need several lifts and a predictable order to adjust the grip force to the current friction and form an internal representation before setting the parameters of the programmed motor output. The difference between adaptation to weight and adaptation to friction is that frictional conditions appear directly upon touching the object, whereas weight information is likely more crucial for anticipatory control because the weight is not available until lift-off. Grip forces of high amplitude

0

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Figure 3-7 The mean and standard deviation of individual means of the safety margin for lifts with sandpaper and silk plotted for different age groups. The safety margin is expressed in percent of the slip ratio. Significant differences are indicated by an asterisk (p < 0.05). (Modified from Eliasson AC, Gordon AM, Forssberg H [1995]. Tactile control of isometric finger forces during grasping in children with cerebral palsy. Developmental Medicine and Child Neurology, 37:72–84.)

are a useful compensatory strategy to avoid dropping objects (Forssberg et al., 1995).

ORGANIZATION OF SENSORIMOTOR CONTROL These studies have enhanced our knowledge of the mechanisms underlying sensorimotor integration and anticipatory control in a grasping task. The model implies that for this manipulatory act visual, tactile, and proprioceptive information are integrated with memories of similar objects from previous manipulative experience. The appropriate muscles are then activated in the proper sequence based on the internal memory representation of the object, resulting in a well timed and coordinated grasping and lifting act. The act includes selection of motor programs that control orientation of the hand and the subsequent limb trajectories. These programs may be stored in sensorimotor (procedural or implicit) memory and used in an unconscious way, different from declarative (explicit) memory that is used in conscious recall of facts, events, and percepts (Squire, 1986) (see Chapter 6). The existence of sensorimotor memory has been demonstrated by disorders in higher brain function. It seems that networks involving cortical function, especially posterior parietal cortex, are important for anticipation. Jeannerod

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(1986) has described deficit in shaping the fingers toward the size of the object in patients with damage to the parietal area. The maturation of control mechanisms for the grasping movement continues throughout childhood. All measured parameters rapidly develop during the first years. Force coordination is poorly developed in 1year-old children; for example, they usually crush an ice cream cone, whereas children of 2 years manage quite well. There is a continuum of improvement of the parallel generation of grip and load forces as well as scaling of the forces toward the object’s different weight and friction. In 4-year-old children the motor output becomes less varied and more coordinated, in conjunction with a decreased safety margin. Children have more coordinated and adjusted movements and are able, for example, to carry a kitten and handle fragile objects. At that age there is even force scaling to the size of the object. However, the appropriate anticipatory scaling with acceleration of the lift to harmonize with the weight of the object is not developed until 6 to 8 years of age. Even so, there are still large variations in the ability to properly scale the forces according to frictional demands. It is not until ages 10 to 12 that scaling approaches adult levels. Efficient control of finger movements continues to develop until adolescence, when children can learn to play musical instruments and develop good handwriting with accurate speed. Obviously, there is parallel processing of cognitive functions and sensorimotor control during normal development. The maturation processes probably occur at many levels. Both the motor cortex and corticospinal tract with monosynaptic connections are important for precision grip and are highly related to force generation. In monkeys the monosynaptic projections to the spinal cord are not fully developed until the end of the first year (Lawrence & Hopkins, 1976). Myelination of the axons and increased conduction rate of cortical motor neuronal activity develop over several years and probably influence the temporal parameters of the lift (Muller, Hornberg, & Lenard, 1991). Because many areas of the brain are apparently involved in the grasping act, its full development obviously depends on establishment of appropriate synaptic connections between the cortex and all other areas associated with the act. These maturation processes are shown by reorganization of reflex responses with more efficient and faster triggering, which continues until adolescence (Evans, Harrison, & Stephens, 1990; Forssberg et al., 1991; Issler & Stephens, 1983). There are cortical networks mediating monosynaptic corticospinal projections to the motor neurons controlling distal muscles (Fetz & Cheney, 1980; Muir & Lemon, 1983), which

are active in fine manipulation and force regulation (Smith, 1981; Wannier, Toltl, & Hepp-Reymond, 1986). There may exist subcortical motor centers and even networks in the spinal cord important for storing certain motor acts; for example, the C3-C4 propriospinal system in cats can be used to mediate and update cortical commands for visually guided reaching (Alstermark et al., 1987). This provides several solutions for a particular movement through a wide range of central and peripheral inputs. During development there may be reorganization of networks in the spinal cord caused by increased descending control on premotor neurons. The descending control may break up the innate grasp reflex synergy allowing independent finger movement and may form a grip/lift synergy (Forssberg et al., 1991). Learning motor activities proceeds by trial and error; it is not really understood how the information from subsequent lifts is stored in memory to result in efficient programming. It is known that the anterior lobe of the cerebellum is involved in force regulation before a lift because the amplitude of the force is correlated with activity in neurons in this region, which has cutaneous and muscle afferent inputs from the hand (Espinoza & Smith, 1990). There are radical changes in synaptic activity, reflected in regional cerebral blood flow, during learning of motor sequence for finger movements. In the initial part of learning there is activation of the cortical areas, cerebellum, and structures providing information to those areas, namely the anterior language area and somatosensory association areas. As learning progresses, the activation in the language areas of the cortex disappears, leaving a reduced region in the somatosensory area, whereas different motor structures and the cerebellum show consistent increase in activity. This may mean that motor programs for motor sequence learning of finger movements are established and can be produced in a feed-forward strategy with less sensory information. It appears that memories are not stored in a single cell or in one particular cortical structure (Seitz et al., 1990).

IMPAIRED FORCE CONTROL AND CLINICAL IMPLICATIONS Clumsiness or impaired hand function may have different origins. The most common diagnoses of developmental disorders in children are ADHD, DCD, and CP. Although of different origin, they are all associated with more or less impaired force control during grasping (Eliasson et al., 1991; Forssberg et al., 1999; Pereira, Eliasson, & Forssberg, 2000). The dysfunction

Normal and Impaired Development of Force Control in Precision Grip • 55 could be seen as a continuum, with clumsy children at one end and severely impaired children with CP at the other. Children with CP have disturbed hand function because the primary or secondary lesions involve the sensorimotor cortex and the corticospinal tract, both of which have great implication for the performance of precision grips and for independent finger movement (Lawrence & Kuypers, 1968; Muir & Lemon, 1983) (see also Pehoski, Chapter 1). These children are known to be slow and weak with disturbed mobility of their finger movements (Brown et al., 1987; Ingram, 1966). In addition, they have different degrees of spasticity and tactile discrimination, especially those children with hemiplegic CP (Brown et al., 1987; Uvebrant, 1988). Little is known about the neural mechanisms that cause the impaired motor behavior in children with ADHD. The main problems are hyperactivity and poor attention, as indicated by the name, but about half of the children who have been diagnosed with ADHD also have motor problems (Barkley, 1990; Kadesjö & Gillberg, 1998). In particular, their fine motor skills are diminished (Szatmari, Offord, & Boyle, 1989; Whitmont & Clark, 1996), affecting, for example, their handwriting and performance on other highly skilled tasks (Doyle, Wallen, & Whitmont, 1995; Raggio, 1999). DCD is characterized by minor motor problems that occur as an isolated phenomenon in some children (American Psychiatric Association, 1994), which is to say that the minor motor problems appear without the symptoms attributable to ADHD but also can be found in conjunction with ADHD. These DCD children in the past were called “clumsy children” or children with motor coordination problems. The cause of the dysfunction is unknown but the group generally can be distinguished from typically developed children from the results of a test like the Movement ABC (Henderson & Sugden, 1992). As indicated, dysfunctioning prehensile force control is common to all children with ADHD, DCD, and CP.

FORCE COORDINATION When making a lift, the temporal pattern is rarely impaired in children with ADHD regardless of whether or not the ADHD is accompanied by DCD (Pereira et al., 2000); for children with CP, it is almost always disturbed to some degree. In these children the difference in the time at which the first finger or thumb makes contact with the object and the time at which the second finger makes contact is larger than in typically developing children, indicating disturbed coordination of finger movement and shaping of the fingers toward the size of the object, although there is a great deal of variation within the group, from almost as good

as the average of the control group to severely impaired (Eliasson et al., 1991; Forssberg et al., 1999). The parallel grip and load force typical of normal development rarely is seen. Instead, the forces increase sequentially with the grip force increasing before the load force (see Figure 3-5). Consequently, they do not produce the force rates in mainly bell-shaped profiles, but in stepwise, irregular, and extremely variable profiles (see Figure 3-4). However, this slow, sequential initiation of movements is an adequate strategy providing security in a manipulative task in which the coordination of force generation is not fully functional. For both groups of children (ADHD and CP), the grip force is larger and more unstable when performing a lift than it is for controls, in addition to which there is more variability between one lift and another (see Figure 3-4) (Eliasson et al., 1991). This large variability seems to be a characteristic of immaturity, as well as of dysfunction and impairment. It means that the children cannot repeat a task in the same way, or transfer the experience of performing one task to the performance of a similar one, making their performance unpredictable or clumsy. The relation between the development of force control and the severity of hand function has been demonstrated previously (Forssberg et al., 1999). However, the slow performance commonly observed in children with CP may be a good adaptation to their impairment. An example of the usefulness of such slow and sequential movement is evident when one considers the impaired release of the grasp. When efficiently putting down and releasing an object, including toys, the object has to be lowered and placed on a surface, not too quickly and not too slowly. This necessitates a low velocity of the movement close to the surface on which the object is to be placed (Figure 3-8). Then the force of the grasp ceases and the individual fingers are removed quickly and almost simultaneously. In a hemiplegic hand, a reversed pattern is found: The placement is performed fairly quickly, and the velocity of the movement is high upon making contact with the table, making the movement abrupt. Then it is hard for the child to decrease the force, resulting in a prolonged movement phase during which the fingers are released one at a time in an uncoordinated manner (see Figure 3-8) (Eliasson & Gordon, 2000). How can this knowledge be used in clinical practice? The case of a 4-year-old girl with hemiplegia playing with small plastic animals is one example. Every time she tried to lift and then place the horse, it fell. It was obvious that she was releasing the object too abruptly. By giving a simple instruction, “Straighten your fingers slowly,” she had the clue she needed to immediately

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Part I • Foundation of Hand Skills Control T0

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Figure 3-8 Grip force from the index finger (ind) and thumb (th), grip force rate, load force, load force rate, vertical position, velocity, and acceleration as a function of time for representative trials during object replacement and release for one child in the control group and one child with hemiplegia. The grip and load force rates are shown using a ±20 point numerical differentiation. Vertical lines indicate the initiation of vertical displacement (T0), object contact with the table (T1), release of one digit (T2) and then the opposing digit (T3). The measured force parameters are shown by arrows indicating peak velocity (F1), peak load force rate corresponding to table contact (F2), minimum grip force rate (F3), grip force at replacement (F4), grip force at table contact (F5), and grip force at load force zero (F6) (dashed line in the right traces). (Modified from Eliasson AC, Gordon AM [2000]. Impaired force coordination during object release in children with hemiplegic cerebral palsy. Developmental Medicine in Child Neurology, 42:228–234.)

succeed. By analyzing her performance in the light of the knowledge that the hand of the child with hemiplegic CP has impaired force coordination, the therapist was able to give the girl precise information. The therapist recognized that although she appeared to be slow when replacing the horse, she was not slow enough in the crucial part of the action—when she had to loosen her grasp. That part had to be performed even more slowly, and she was able to succeed by increasing her awareness of that part of the movement sequence. Normally this behavior is performed in an unconscious way (i.e., by implicit processes) (Gentile, 1998). However, after a lesion has occurred in the CNS, it may be necessary to use an explicit process, at least in the early stage of learning. Knowledge about normal and abnormal behavior and the ability to analyze the task made it possible to give precise instructions. The idea was to help the child to learn how her impaired nervous system works and give her a strategy that could enable her to perform this task successfully; then she might be able to use the same strategy when releasing other objects in different situations (Eliasson, 2005).

ANTICIPATION OF THE PROPERTIES OF OBJECTS During normal development small children are able to scale the force that needs to be applied when gripping an object even before the action starts, taking into account the weight and friction, as well as the size of the object. This happens even before the typical parallel force coordination with the mainly bell-shaped force rate profile is developed. Hardly any of the children with CP who were aged 6 to 8 years, or the children with ADHD plus DCD who were 9 to 15 years, scaled the force amplitude appropriately for different weights, whereas children with only ADHD anticipated the weight fairly well (Eliasson et al., 1992; Pereira et al., 2000). This indicates that a different type of dysfunction (diagnosis), at least on a group level, influences the ability to scale the motor output. Although children with ADHD plus DCD can apply an appropriate force the first time they lifted a familiar object such as a glass, or an unopened packet of milk, they cannot do this efficiently with an unfamiliar object, when they have only seen but not touched or lifted it (Pereira

Normal and Impaired Development of Force Control in Precision Grip • 57 et al., 2000). Appropriate force involves anticipatory scaling. That means that when heavier and larger objects such as an unopened packet of milk are to be lifted, the child increases the load force at a greater rate during the initial lifts than when lifting smaller light objects like the glass. Children with ADHD plus DCD are able to build up a memory representation of the object, although this is not as efficient as for typically developed children and adults. This deficient control was also demonstrated in a group of children with hemiplegic CP who were unable to scale the force output to match the weight of a previously lifted object until they had lifted the object at least 15 times. This has to be compared with the one or two times necessary in age-matched peers (Gordon & Duff, 1999). However, most participants with CP demonstrated anticipatory scaling when lifting familiar objects, which means that they are capable of learning by practice, despite having a dysfunctional nervous system. The question, then, is how this practice should be planned and performed. An investigation was carried out in another experiment in which children lifted novel objects that varied in weight in either a blocked series, with one weight being lifted several times, or a random series in which different weights were randomly assigned to be lifted (Duff & Gordon, 2003). Blocked practice resulted in greater differentiation of the force rates between objects during acquisition than random practice. However, both types of practice resulted in similar performance retention 24 hours later. These findings suggest that children with hemiplegic CP are able to build up internal representations that are used for anticipatory force scaling of novel objects, and that practice is valuable, although it appears that the type of practice schedule employed is not important. The importance of practice can be demonstrated by adolescents with hemiplegic CP who were practicing Frisbee golf using their hemiplegic hand. Being able to throw a Frisbee as well as possible toward a target requires the ability to plan the direction of the movement, use a certain amount of force, and release the grasp with exact timing. Playing Frisbee with a hemiplegic hand may seem crazy, but it was an activity practiced at a 2-week, 5-day-a-week day camp in which the adolescents were treated by Constraint Induced Movement Therapy (Eliasson et al., 2003). The goal of the Frisbee game was to traverse a 350-foot-long course, at the end of which was a basket. The object of the game was to use the fewest number of throws to get the Frisbee in the basket. Nine adolescents practiced 30 minutes for 7 days during the day camp. All adolescents improved at this game, and the number of throws needed to get the Frisbee into its basket

decreased from the first to the last day of camp, from 20 (range 14 to 35) to 14 (range 12–18) (Eliasson et al., 2003). It appears that it is possible to improve at Frisbee golf, as well as to learn to scale the force output during grasping applied to objects by practice, at least for these groups of children with CP.

SENSORY I NFORMATION USED FOR FORCE CONTROL Sensory information is essential for prehensile force control because it provides the nervous system with information about different aspects of the physical properties of objects in the immediate environment and, as described, it is used for anticipatory scaling and to adjust ongoing movements. Sensory impairments have been described for children with hemiplegic CP but have not been observed in children with diplegic CP or ADHD (Uvebrant, 1988). In children with hemiplegic CP, a decrease in two-point discrimination and stereognosia occurs in 50% to 70% of children. Processing of proprioceptive information also is impaired. This can be seen during vibration of a muscle, in which the muscle spindles are stimulated, giving rise to an illusion of arm movement; this illusion occurs in normal children, but only in 50% of children with CP (Tardieu et al., 1984). However, there is an unclear relationship between the perceived sensation of this kind and the ability to adjust the force output to match the physical properties of an object. All children with CP who participated in earlier studies perceived the difference between weight and frictional contact surfaces of the object to be lifted although some of them had decreased two-point discrimination and stereognosis. That is, almost all of them have decreased ability to transform sensory information into appropriate “settings” for a motor command. There was no simple correlation between two-point discrimination and ability to adjust the force output based on frictional condition of the object (Eliasson et al., 1995). This may indicate that two point discrimination needs to be processed at a higher level in the central nervous system than adjustment of forces for grasping. The children with CP should be able to rely on sensory feedback for grasping because, as mentioned, their anticipatory control is impaired. Relying on sensory feedback means that the forces increase in a steplike manner, permitting sensory feedback, until liftoff. This results in a prolonged loading phase for heavier objects, but fairly well-adjusted forces taking into account both the weight of the object and the friction of the contact surfaces during the static phase when the object is held still in the air (Eliasson et al., 1992, 1995). Yet there is large variation in the grip

Part I • Foundation of Hand Skills

force applied during the isometric force coordination, making the performance unpredictable and, of course, inconvenient for daily life. This is a common feature in the early development of all children, including children with different diagnoses (Eliasson et al., 1991; Brogren, Forssberg, & Hadders-Algra, 2001; Pereira et al., 2000). A way of solving this problem is to increase the safety margin to prevent objects from being dropped. This compensatory behavior was obvious in all the children with CP who were investigated. It is evidently a successful compensatory strategy for those with impaired sensory processing, lack of anticipatory control, and slow adaptation (Eliasson et al., 1995). However, it does make it difficult to handle fragile objects because there is a danger that the object will be crushed, and it also makes it difficult for children with CP to handle heavy objects because, in this case, a high level of force is needed and weakness is a common problem in children with CP. The question that needs to be addressed is: How can children with sensory dysfunction learn to handle objects as efficiently as possible? Sensory information is crucial for the performance of precise movements. Tactile information is the most important information for discrete finger movements, whereas proprioception is more important for reaching in different directions and handling objects of different weights. Tasks in which tactile information is crucial are, for example, buttoning up a shirt, picking raspberries, and opening a door with a key. For many bimanual tasks, having intact sensibility in only one hand does not terribly influence the task performance because people usually hold the object (an action requiring less sensory information) with their impaired hand and manipulate (requires efficient tactile regulation) with their dominant hand (Krumlinde-Sundholm & Eliasson, 2002). However, an important compensation for tactile disturbance is to use visual information. Vision strongly influences manipulatory actions and should not be overlooked when attempts are made to gain a deeper understanding of how the somatosensory systems influence manipulatory actions. The ability to use visual information as a form of compensation was seen when the results of hand surgery were evaluated. Children with CP and impaired sensibility tended to benefit more or at least as much from upper limb surgery as measured by a timed dexterity task than children with intact sensibility (Figure 3-9) (Eliasson, Ekholm, & Carlstedt, 1998). This probably has something to do with the ability to “see the grasp” being performed after surgery because before the surgery was performed, the hand was pronated, the wrist was flexed, and the thumb was in-palm, making it impossible to see the grasping act as it was conducted. After surgery, in contrast, the hand was more extended and supinated

Dexterity before and after surgery 140 120 100 Sec

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Impaired Sensibility

Figure 3-9 Dexterity, in seconds when moving 10 cubes and placing them on the opposite side of a vertical border on the table. Individual results of 11 subjects with normal two-point discrimination (2PD) and 14 with impaired 2PD before and after surgery. 2PD: 3 to 4 mm was tested for in a randomized order, their fingers were touched with a distinct but light touch with one or two points, 10 times on each finger. Before examination, the task was demonstrated for them to see and feel the differences between one and two points on both hands. Normal 2PD required at least eight correct answers on two of three digits. The time decreased 14.5 s (md) compared with 9 s (md) for children with normal sensation. (Modified from Eliasson A.C, Ekholm C, Carlstedt T [1998]. Hand function in children with cerebral palsy after upper-limb tendon transfer and muscle. Developmental Medicine in Child Neurology, 40:612–621.)

and the thumb was able to meet the fingers, making it possible to use vision to compensate for impaired sensibility. This may indicate that impaired sensation could be an indication for surgery, at least from one perspective. This is opposite to what commonly is recommended but has to be considered. One other important way to compensate for lack of control that should not be overlooked is to concentrate and pay deliberate attention to the performance of the task. The compensatory strategies are crucial, but they often make the children slower.

SUMMARY Motor control—meaning how the CNS controls movement—is complex, but by understanding the principles of how movements are organized, it is possible to use the knowledge that has been gained to plan intervention. By using this perspective we can help children to learn more about themselves and help them find more efficient ways to use their possibilities rather than focusing on the impaired or odd movement. An important perspective to put across is that there is nothing

Normal and Impaired Development of Force Control in Precision Grip • 59 wrong or right about a movement, rather, when there is a task that needs to be performed, it can often be done in a number of different ways. As therapists, we can help them to learn themselves by adopting strategies and ensuring that repetition consolidates improvements. Thus, if knowledge of motor control is used alongside the principles of motor learning, a new and useful concept of treatment results. In addition, it should be remembered that we do not know the relationship between the maturation of the CNS and the performance of different tasks; however, we do know that practice is necessary. Given this, it seems logical that a less efficient nervous system needs more practice than an appropriately functioning one. It is also known that improvement in any task strongly depends on motivation. Improvement induced by motivation is shown nicely in a task measuring pronation and supination of the hand: The children are induced to increase their range of movement by hitting a drum rather than by just performing the movement (van der Weel, van der Meer, & Lee, 1991). For the children concerned, it is the game itself that is the goal: They are not interested in the specific movement of arms and hands, and the therapist should remember this. For success in skills, the therapist should encourage children to find tasks they are motivated to repeat and learn, working on their possibilities rather than on their limitations. We have to bear it in mind that the task performance we see may look odd from a perspective of “normal” movements, but it may be a solution to a problem based on their way to handle their impaired nervous system

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D Ottoson (editors): Somatosensory mechanisms. London, Macmillan. Johansson RS, Westling G (1987). Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Experimental Brain Research, 66:141–154. Johansson RS, Westling G (1988). Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Experimental Brain Research, 71:59–71. Johansson RS, Westling G (1990). Tactile afferent signals in the control of precision grip. In M Jeannerod (editor). Attention and performance. Hillsdale, NJ, LEA. Kadesjö B, Gillberg C (1998). Attention deficits and clumsiness in Swedish 7-year-old children. Developmental Medicine and Child Neurology, 40:796–804. Konishi M (1965). The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Zeitschrift Tierpsychologie, 22:770–783. Krumlinde-Sundholm L, Eliasson AC (2002). Comparing tests of tactile sensibility: Aspects relevant to their use in testing children with spastic hemiplegia. Developmental Medicine and Child Neurology, 44:604–612. Lawrence DG, Hopkins DA (1976). The development of motor control in the rhesus monkey: Evidence concerning the role of corticomotoneuronal connections. Brain, 99:235–254. Lawrence DG, Kuypers HGJM (1968). The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain, 91:1–14. Lund JP, Olsson KA (1983). The importance of reflexes and their control during jaw movement. Trends in Neuroscience, 6:458–463. Miller AJ (1972). Significance of sensory inflow to swallowing. Brain Research, 43:147–159. Mott FW, Sherrington CS (1895). Experiments upon the influence of sensory nerves upon movement and nutrition of the limbs. Proceedings of the Royal Society of London. Series B: Biological Sciences, 57:481–488. Muir RB, Lemon RN (1983). Corticospinal neurons with a special role in precision grip. Brain Research, 261:312–316. Muller K, Homberg V, Lenard HG (1991). Magnetic stimulation of motor cortex and nerve roots in children. Maturation of corticomotoneural projections. Electromyography and Clinical Neurophysiology, 81:63–70. Nottebohm F (1970). Ontogeny of bird song. Science, 167:950–956. Okado N (1980). Development of human cervical spinal cord with reference to synapse formation in the motor nucleus. Journal of Comparative Neurology, 191:495–513. Okado N (1981). Onset of synapse formation in the human spinal cord. Journal of Comparative Neurology, 201:211–220. Pereira HS, Eliasson AC, Forssberg H (2000). Detrimental neural control of precision lifts in children with ADHD. Developmental Medicine and Child Neurology, 42:545–553. Raggio DJ (1999). Visuomotor perception in children with attention deficit hyperactivity disorder-combined type. Perception and Motor Skills, 88:448–450. Roland PE, Ericsson L, Widen L (1989). European Journal of Neuroscience, 1:3–18. Ruff HA (1984). Infants’ manipulative exploration of objects: Effects of age and object characteristics. Developmental Psychology, 20:9–20.

Normal and Impaired Development of Force Control in Precision Grip • 61 Seitz RI, Roland PE, Bohm C, Greitz T, Stone-Elander S (1990). Motor learning in man: A positron emission tomographic study. Neuroreport, 1:57–66. Smith AM (1981). The co-activation of antagonist muscles. Canadian Journal of Physiology and Pharmacology, 59:733–747. Squire LR (1986). Mechanisms of memory. Science, 232:1612–1619. Szatmari P, Offord DR, Boyle MH (1989). Ontario child health study: Prevalence of attention deficit disorder with hyperactivity. Journal of Child Psychology and Psychiatry, 30:219–230. Tardieu G, Tardieu C, Lespargot A, Roby A, Bret MD (1984). Can vibration-induced illusions be used as a muscle perception test for normal and cerebral-palsied children? Developmental Medicine and Child Neurology, 26:449–456. Uvebrant P (1988). Hemiplegic cerebral palsy: Aetiology and outcome. Acta Pediatrica Scandinavica Supplement, 345. Vallbo B (1970). Discharge patterns in human muscle

spindle afferents during isometric voluntary contractions. Acta Physiologica Scandinavica, 80:552–566. van der Weel FR, van der Meer ALH, Lee DN (1991). Effect of task on movement control in cerebral palsy: Implications for assessment and therapy. Developmental Medicine and Child Neurology, 33:419–426. von Hofsten C, Ronnquist L (1988). Preparation for grasping an object: Developmental study. Journal of Experimental Psychology: Human Perception and Performance, 14:610–621. Wannier TMJ, Toltl M, Hepp-Reymond M-C (1986). Neuronal activity in the postcentral cortex related to force regulation during a precision grip. Brain, 382:427–432. Wilson DM (1964). The origin of the flight-motor command in grasshoppers. In RF Qeiss (editor): Neuronal theory and modeling. Palo Alto, Stanford University Press. Whitmont S, Clark C (1996). Kinaesthetic acuity and fine motor skills in children with attention-deficit-hyperactivity disorder: A preliminary report. Developmental Medicine and Child Neurology, 38:1091–1098.

Chapter

4

PERCEPTUAL FUNCTIONS OF THE HAND Sharon A. Cermak

CHAPTER OUTLINE DEVELOPMENT OF HAPTIC PERCEPTION Haptic Perception in Infants Haptic Perception in Children Gender and Hand Differences in Haptic Recognition and Haptic Accuracy Summary and Implications for Practice FUNCTIONS CONTRIBUTING TO HAPTIC PERCEPTION Role of Somatosensory Sensation in Haptic Perception Role of Manual Manipulation and Exploratory Strategies in Haptic Perception Role of Vision and Cognition in Haptic Perception Summary and Implications for Practice EVALUATION OF HAPTIC PERCEPTION IN INFANTS AND CHILDREN HAPTIC PERCEPTION IN CHILDREN WITH DISORDERS Prematurity

used for carrying out everyday activities such as tying shoes or buttoning. As a perceptual organ it seeks and processes information such as when searching for a coin in a pocket. The two functions of the hand are closely intertwined. Rochat (1989) emphasized that “from the origin of development, action is under some perceptual or sensorimotor control and the picking up of perceptual information is somehow inherent in any performed act” (p. 871).

However, when the hand performs a practical action, its perceptual functioning is regulated by what is needed to achieve this action, whereas when the hand acts primarily as a perceptual system, its motor activity is primarily exploratory and information seeking. This chapter concerns the hand as a perceptual or information-seeking organ. Focus is on active touch (haptic perception) rather than passive touch. Passive touch involves only the excitation of receptors in the skin and underlying tissue; “active touch involves the concomitant excitation of receptors in the joints and tendons along with new and changing patterns in the skin” (Gibson, 1962, p. 482).

Brazelton has suggested that, whereas

Mental Retardation Brain Injury Learning Disabilities and Related Disorders Summary and Implications for Practice SUMMARY The hand has two closely related functions: It is both an executive and a perceptual organ (Bushnell & Boudreau, 1998; Gibson, 1988; Hatwell, Streri, & Gentaz, 2003; Lederman & Klatzky, 1998). As an executive organ it is

“passive touch may add to an infant’s ability to initiate and maintain control, active touch … acts as an alerter and as information. It helps the infant come to a receptive alert state and begin to process information” (Rose, 1990, p. 316).

Haptic perception deals with the retrieval, analysis, and interpretation of the tactile properties (e.g., size, shape, texture) and identity of objects through manual and in-hand manipulation (Bushnell & Boudreau, 1993; Hatwell, 2003). The process of tactile scanning is complex and includes the blending of feedback from tactile,

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kinesthetic, and proprioceptive sensations. The tactile spatial properties of objects are obtained through the retrieval of information about the relationship of the objects to the body and gravity during active manual exploration. The study of haptic perception has been closely associated with the study of visual perception. Researchers have attempted to gain insight into how we use our visual and haptic senses to function by comparing the ability to match objects through the use of vision and haptic manipulation. These studies typically require the subject to match a standard (test) object to a set of two or more comparison objects. If the subject is asked to do an intramodal comparison, both the standard and comparison objects are analyzed using the same sensory modality (visual or haptic sense). If the subject is asked to do an intermodal comparison, the standard object is analyzed using one sense and the comparison object(s) are analyzed using the other sense. In this chapter research methodology is specified as containing intramodal or intermodal matching, whereas the senses used appear in parentheses (standard comparison). For example, intermodal (haptic-visual) matching means that the haptic sense was used to analyze the standard or test object and the visual sense was used to select from among the comparison objects. The term multimodal exploration refers to the simultaneous use of the visual and haptic senses in object investigation. In this chapter the review of intramodal matching (matching using the same sensory system) is limited to haptic-haptic matching in which the subject feels the standard or test object and then feels several comparison objects to find the match. One goal of this chapter is to provide the reader with an understanding of selected aspects of haptic perception that may influence effective evaluation and treatment of children with suspected and identified impairments in haptic perception. Topics covered include the development of haptic perception, functions contributing to haptic perception, evaluation of haptic perception in infants and children, and haptic perception in children with neurologic disorders. The adult literature has been included to the degree to which it assists our understanding of the current status of the pediatric research.

DEVELOPMENT OF HAPTIC PERCEPTION HAPTIC PERCEPTION IN I NFANTS In the infant the hands and mouth are both potential sources of haptic information. The mouth can be used to gain information about the shape and substance of

objects (Ruff, 1989). Pecheux, Lepecq, and Salzarulo (1988) found evidence suggesting intramodal (haptichaptic) recognition of shapes inserted into nipples by 2 months of age. As the infant develops, the hands become a perceptual system that increasingly participates in the infant’s construction of knowledge (Bushnell & Boudreau, 1998; Hatwell, 1987). Manipulation of an object facilitates the learning of the object’s characteristics. During exploratory play of the first year, infants begin to learn about their environment, their bodies, and how their actions can effect change (Gibson, 1988). Current research has indicated that haptic abilities are much more efficient in infants than was thought in the past (Streri, 2003a). Use of the habituation paradigm adapted from vision research has shown that early intramodal (haptic-haptic) manual exploration in infants provides consistent haptic discrimination (Hatwell, 1987; Streri & Pecheux, 1986). In this paradigm infants are given shapes to manually explore with a screen preventing the infants from seeing their hands. The amount of interest the infant devotes to the object is measured by the amount of time the object is grasped, and as the infant habituates, he or she holds the object for shorter periods of time. Using two pairs of shapes, Streri and Pecheux (1986) observed a haptic habituation to a familiarized shape and a reaction to novelty (longer holding) when a new shape was presented to 4- and 5-month-old infants. This was noted in infants as young as 2 to 3 months (Streri, 1987). Streri and Pecheux (1986) reported that infants required a longer period of time to habituate to tactile stimuli than to visual stimuli and suggested that this may be explained, in part, because information can be obtained more quickly visually than tactually. In a similar haptic habituation paradigm, 6- and 7-monthold infants with severe visual impairments also were found to show haptic integration for shape and texture (Catherwood et al., 1998). Research with infants also has shown that young infants evidence intermodal integration. Rose, Gottfried, and Bridger (1978) concluded that 6-month-old infants could integrate visual and haptic perception as evidenced by their ability to visually recognize a shape after only tactile contact with it. Streri and colleagues completed a series of studies that supports even earlier development of visual-haptic integration and haptic object perception (Streri, 2003b; Streri & Gentaz, 2004; Streri et al., 2004; Streri & Molina, 1993; Streri & Spelke, 1988, 1989). For example, responses of 4- to 5-month-old infants to visual images of objects were assessed after bilateral object handling without opportunity for visual regard of the hands (Streri & Spelke, 1988, 1989). One object presented was two rings connected by a solid bar; the other object was two rings connected by a string. The infants produced

Perceptual Functions of the Hand • 65 different types of arm movements when holding the different objects. The infants were shown visual displays of two rings either connected or separated, which were moving as they typically did while the infants were holding them. The infants looked longest at the rings that were dissimilar to those that they had held. This was the expected response if the infants perceived the similarities between the rings that they held and moved and those that they saw moving. Streri and Spelke (1988) concluded, “infants evidently perceived connected or separated objects by detecting the patterns of common or independent motion that they themselves produced.” (p. 19).

They also noted that the infants held the objects for relatively long periods, as much as five times as long as they would have been expected to visually attend to an object. Because these 4-month-old infants were so competent at identifying objects tactually and visually, Streri and colleagues (Streri, 2003a; Streri & Spelke, 1988) questioned Piaget’s theory that vision and touch become integrated through haptic exploration of objects and suggested that this ability may be present without substantial experience in handling objects. In a recent study of cross-modal recognition in newborns, Streri and Gentaz (2004) have even suggested that under some limited conditions, newborns have the ability to extract shape in a tactile format and transfer it to a visual format, independent of common experience. Molina and Jouen (1998, 2001, 2003) also reported that newborns can discriminate between rough and soft textures and modify their grasping according to the texture of the grasped object.

HAPTIC PERCEPTION IN C HILDREN Much of the literature on haptic perception in children deals with the recognition of common objects (e.g., comb, penny) and shapes (e.g., circle, square, diamond). However, the hand also is used to gain information about other object properties, such as texture, hardness, size, weight, and spatial orientation. Each is discussed.

Recognition of Common Objects and Shapes One of the most well-known studies on the development of haptic perception in children is that of Piaget and Inhelder (1948/1967). They presented a series of solid (three-dimensional) common objects and cardboard cutouts of shapes (geometric figures and topologic forms) to a group of 2- to 7-year-old children and asked the children to feel each figure and then visually select the figure from among a set of figure drawings. The geometric figures used ranged from simple (e.g., circle, ellipse, square) to complex (e.g., star, cross, semicircle). Topologic forms were shapes with irregular

surfaces containing one or two holes or having openings or closings on their outer edges. These authors found that the ability of children to identify objects and shapes by touch progressively improved with increased age. Children 21⁄2 to 31⁄2 years of age were able to correctly recognize common objects but were unable to identify shapes. By 31⁄2 to 5 years of age children developed the ability to match topologic forms. Recognition of geometric figures emerged at 4 to 41⁄2 years with the ability to differentiate curvilinear (circle and ellipse) from rectilinear (square and rectangle) shapes. The ability to recognize geometric figures in greater numbers and levels of complexity was shown to progressively improve from 41⁄2 to 7 years of age. Benton and Schultz (1949) also studied intermodal (haptic-visual) matching of common objects in a group of 156 3- to 5-year-old children and found that performance progressively improved with age. Three-yearold children typically were able to recognize 50% of the items presented (mean 4.0 out of eight items). Fouryear-old children performed only slightly better than children in the 3-year-old age group (mean = 4.5). Near-perfect performance typically was found by 5 years of age, with most children correctly recognizing at least seven of the eight objects presented. Hoop (1971a) also studied intermodal (hapticvisual) matching at 31⁄2 to 51⁄2 years. Like Piaget and Inhelder, Hoop found the identification of common objects to be easier than the recognition of topologic forms and geometric figures. There was little variation in the ability of 31⁄2- to 51⁄2-year-old children to match topologic forms (means ranging from 2.3 to 2.6 out of a maximum score of 4). Miller (1971) reported a similar finding. The 3- and 4-year-old children in her study were able to identify fewer than half of the intermodally (haptic-visual matching) and intramodally (haptic-haptic matching) presented shapes. Like Piaget and Inhelder, Hoop found the recognition of topologic forms through intermodal (haptic-visual) matching to be easier than the identification of geometric figures. However, this has not been a consistent finding (Derevensky, 1979). Derevensky (1979) suggested that listing shapes as topologic or geometric may be an incorrect method of categorization, and suggested that it may not be whether a shape is topologic or geometric but the nature of the distinctive features that it contains that contributes to task difficulty. Another interesting finding was reported by Abravanel (1972), who noted that, in a series of intermodal (haptic-visual matching conditions, it was easier for 6- to 8-year-old children to identify solid (threedimensional) than flat (two-dimensional) geometric figures. She attributed this to possible variation in the usefulness of the manipulation strategies used by the children in shape exploration. This topic is discussed in depth in a later section of this chapter.

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Recently, Bushnell and Baxt (1999) examined haptic recognition of familiar versus unfamiliar objects. They found that 5-year-old children more accurately identified familiar than unfamiliar objects; however, this varied as a function of whether the matching was haptic-haptic or haptic-visual. For unfamiliar objects, haptic-haptic matching was more accurate than hapticvisual matching, whereas there was no difference for familiar objects. Familiar objects were identified more accurately than unfamiliar objects in a haptic-visual matching task, but there was no difference as a function of familiarity in the haptic-haptic matching task. A limitation of the study is that a ceiling effect was reached for familiar objects, with many participants achieving maximum scores. There is general agreement that the haptic perception of common objects is well developed by 5 years of age, and the ability of children to select geometric figures through intermodal (haptic-visual) matching emerges at about 4 years of age (Abravanel, 1972; Blank & Bridger, 1964; Hoop, 1971a; Micallef & May, 1979; Piaget & Inhelder, 1948/1967). Like the finding of Piaget and Inhelder, all of these studies have noted improvement in accuracy with increasing age. Moreover, with increasing age, children change their representation of objects from one based primarily on global shape to one that incorporates a balance of global shape and specific local parts (analytical mode) (Berger & Hatwell, 1993, 1995; Morrongiello et al., 1994). However, whereas some researchers reported that young children primarily used global strategies to categorize objects, others found that both children and adults primarily used analytic modes (Schwarzer, Kufer, & Willkening, 1999). Within this mode, Schwarzer found a developmental sequence in the attribute chosen for categorization of objects. They found that focusing on surface texture decreased with age and focusing on shape increased with age. Thus children preferred substance-related attributes, especially surface texture, whereas adults preferred the structure-related attributes, especially shape. This was consistent with Berger and Hatwell (1993), who also found a preference for surface texture as an analytic attribute.

Recognition of Texture, Size, and Weight Unlike shape or orientation, length, or localization in the environment, in which vision is superior to touch, texture perception is often as good haptically as visually (Gentaz & Hatwell, 2003). Haptic discrimination of texture, size, and weight has been shown to improve with increasing age in 4- to 9-year-old children (Gliner, 1967; Miller, 1986; Siegel & Vance, 1970). Gliner further found rough textures to be easier to identify than smooth textures, with third grade subjects showing a lower threshold (greater sensitivity) to texture stimuli than kindergarten subjects.

Intermodal (haptic-visual) discrimination of diameter and length has been reported to emerge at 4 years and continues to mature into adolescence, with variation in diameter being easier to recognize than variation in length (Abravanel, 1968a,b; Connolly & Jones, 1970; Hulme et al., 1983). When analyzing length, children found tasks requiring intramodal (vision or haptic) discrimination easier than those requiring intermodal (vision and haptic) discrimination for object comparison (Hulme et al., 1982, 1984). Research comparing children’s preference for the use of texture, size, and shape in object recognition suggests that there may be a developmental progression in preferential use of these sensory properties. Preference for the use of texture over shape in object identification during intramodal (haptic-haptic) matching tasks has been found to occur in young children (4 to 5 years of age) but not in older children (Berger & Hatwell, 1993, 1995; Gliner, 1967; Schwarzer et al., 1999; Siegel & Barber, 1973; Siegel & Vance, 1970), although Schwarzer and co-workers (1999) found that the exploratory strategy varied as a function of the task requirements and the feedback. Size has been shown to be more difficult to discriminate than texture in children 4 and 8 years old (Miller, 1986). Gliner and co-workers (1969) further found that the preference of kindergartners for texture over shape in object identification in an intramodal (haptic-haptic) matching task decreased as the textured surfaces became more difficult to identify. Preference for the use of shape over texture and size during intramodal (haptic-haptic) matching of objects was cited by Siegel and Vance (1970) and Gentaz and Hatwell (2003) in kindergarten through third-grade children. Adults preferred size or shape classification (Gentaz & Hatwell, 2003). Miller (1986) further found that variation in shape interfered with accuracy in identification of texture during intramodal (haptic-haptic) matching in 8-yearold children but not in 4-year-old children. She concluded that this might be because 4-year-old children ignored shape cues when texture was available for use in object discrimination. Thus it is possible that during tasks requiring haptic discrimination, children might use the sensory property that produced the strongest distinctive features. As the ability to recognize shapes improves with age, there might be increased preference for the use of shape over other properties for object identification because shape yields distinctive features that are more useful in object recognition than texture or size. If this hypothesis is correct, then the properties selected for use in object recognition might be age and task dependent. They might vary based on both the degree to which the distinctive features provided by the object were easy to identify and the developmental level of haptic perception (e.g., texture, shape, size) exhibited by the child being tested.

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Recognition of the Spatial Orientation of Objects Few studies have addressed the development of haptic spatial orientation in children. Perceptual awareness of the constancy of spatial location through the use of vision and haptic exploration has been shown to develop at an early age. Three-year-old children who were blind were able to identify common objects after 180 degrees of object rotation (Landau, 1991). Hatwell and Sayettat (1991) asked 4- to 7-year-old children to reseat a doll at a table inside a doll house after the child, the doll, the table, or the house was rotated. Many of the 4-year-old children were able to successfully reseat the doll in the initial location after rotation using intramodal (visual or haptic) exploration. An age-related increase in accuracy of doll placement occurred between ages 4 and 6 years. The shape of the table had no effect on task performance. Children of 41⁄2 years in a study by Abravanel (1968a) could visually recognize test objects facing up, down, or rotated but had difficulty when intermodal (haptic-visual) matching was necessary for task completion. Intermodal recognition of up-down was no better than chance until 5 years of age, and the identification of rotated figures was not possible until 6 years of age. Pick, Klein, and Pick (1966) used intramodal (visual-visual and haptic-haptic) matching tasks to study children’s ability to differentiate the up-down orientation of letter-like forms. They reported that the task could be performed more easily through the use of vision than touch. No relationship was found between subjects’ ability to perform the task through the use of vision versus touch, leading the authors to conclude that perhaps the method used in coding and discriminating spatial orientation is different for the two sensory modalities. However, it is also possible that some types of objects might just be better suited for processing through one sensory system than the other. For example, letter-like forms may represent a type of object that is easily processed through the visual system but not easily analyzed through the tactile system. In a recent review of research examining processing of spatial object properties and the oblique effect (whether orientation is perceived more accurately in the horizontal and vertical planes than the oblique plane), investigators concluded that gravitational cues play a role in the haptic perception of orientations in blindfolded (sighted) adults and children (Gentaz & Hatwell, 2003; Gentaz & Streri, 2004). This is similar to the oblique effect found for orientation with vision.

G ENDER AND HAND DIFFERENCES IN HAPTIC RECOGNITION AND HAPTIC ACCURACY Several studies have examined whether boys and girls perform differently in the accuracy of haptic perception and whether one hand is more accurate than the other.

Research generally has shown that boys and girls 3 to 14 years old display equal ability to recognize common objects, shapes, and words through intramodal (haptichaptic) and intermodal (haptic-visual) matching (Abravanel, 1970; Affleck & Joyce, 1979; Ayres, 1989; Benton et al., 1983; Benton & Schultz, 1949; Bushnell & Baxt, 1999; Cioffi & Kandel, 1979; Cronin, 1977; Etaugh & Levy, 1981; Gliner, 1967; Klein & Rosenfield, 1980; Kleinman, 1979; Witelson, 1976; Wolff, 1972). Occasionally boys have been identified as exhibiting greater skill than girls in the intramodal (haptic-haptic) matching of objects by texture, size, and shape (Gliner, 1967). In addition, Siegel and Barber (1973) found boys to display a stronger preference than girls for the use of form over texture in the intramodal (haptic-haptic) matching of shapes. Most studies conducted on normal adults have shown there to be no difference in the overall accuracy of haptic perception between men and women (Cronin, 1977; Kleinman, 1979; McGlone, 1980). When handedness is examined, children often display greater left- than right-hand skill in some forms of haptic perception (Hahn, 1987; Rose et al., 1998); however, the strength and age of onset of this difference vary among studies (Streri, 2003c). The finding of greater left- than right-hand skill on some tasks, particularly those requiring discrimination of meaningless shapes, has been viewed as related to right hemisphere superiority in the processing of spatial information (e.g., Witelson, 1974, 1976). In a recent meta-analysis of cerebral specialization of spatial abilities, Vogel, Bowers, and Vogel (2003) found a right-hemisphere preference when subjects were performing spatial orientation and manual manipulation tasks. However, because the age of onset of right–left hand differences varied widely across studies, it is inappropriate to interpret the presence or absence of a hand difference for stereognosis as being related to the maturity of hemispheric specialization for haptic perception in a given child. Consistent evidence of a right–left hand difference for stereognosis did not appear until adolescence.

SUMMARY AND I MPLICATIONS FOR PRACTICE The ability to distinguish the texture, shape, and substance of objects through the use of intramodal (haptic-haptic) and intermodal (haptic-visual and visual-haptic) exploration develops over a long period. It begins to emerge in early infancy and continues to mature into adolescence. Infants are amazingly adept at using haptic exploration with the mouth and hands to learn about objects in their environment. Early haptic discrimination using the mouth is seen at 1 month of age or even earlier, and haptic discrimination using the hands appears at 1 to

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2 months of age. Intermodal transfer of information between the haptic and visual senses begins at 4 to 6 months, although recent evidence suggests that even newborns have limited ability. This means that by the second half of the first year of life infants can explore an object using the hand and then recognize the same object as being similar or different using vision. Haptic perception improves with increasing age. Children find common objects easier to haptically recognize than topologic forms, geometric figures, or unfamiliar objects. At 21⁄2 years, children can identify many common objects through use of the haptic sense. Haptic recognition of common objects reaches full maturity by about 5 years. Intramodal (haptic) and intermodal (haptic and visual) identification of topologic forms and geometric shapes emerges at 3 to 4 years and continues to develop throughout childhood. With increasing age children are able to match forms or shapes having increasingly complex distinctive features. They also are able to move from recognizing only solid (three-dimensional) shapes to being able to also distinguish flat (two-dimensional) figures. Hapticvisual matching generally is better than visual-haptic matching. Thus in developing a program to enhance children’s haptic matching abilities it is best to start with familiar objects, with haptic-visual matching preceding visual-haptic matching. Like adults, children show greater left than right hand skill in some forms of haptic perception, possibly reflecting specialization of the right hemisphere for the processing of spatial information. However, the age at which hand preference for haptic processing emerges varies across studies. Although some authors suggest that haptic perception may be better in boys than girls, most studies have not found a difference. The literature contains less information about the development of sensory properties such as texture and weight in childhood. It is known that children find rough textures easier to match than smooth textures. The development of texture discrimination improves between 4 and 9 years, in part because tactile sensitivity increases during this time span (Gliner, 1967). The discrimination of diameter and length begins at about 4 years and continues into adolescence, with variation in diameter being easier to recognize than variation in length. Children as young as 3 to 4 years can recognize the spatial orientation of an object when the child or object has been rotated, but it is not until 5 to 6 years that children can haptically identify objects as facing up, down, or rotated. Children’s ability to haptically analyze objects having two or more tactile properties is limited. Rather than analyzing several sensory properties simultaneously as adults do, children appear to select one sensory property to use in object analysis. The sensory

property selected seems to be the one that is easiest for the child to recognize, perhaps because it exhibits the strongest distinctive features. For example, texture is preferred to shape and size in young children, whereas older children are more likely to match objects by shape than texture. In addition, the coexistence of several sensory properties in a given object can impair haptic discrimination at some ages. This finding suggests that haptic figure-ground may be an issue in haptic object discrimination, a factor that needs to be considered in the development of tests and training programs in haptic perception. We do not know whether the ability to distinguish objects by shape, size, texture, or weight develops sequentially or simultaneously. Research suggests that children develop the ability to discriminate all of these sensory properties, including texture, hardness, weight, and temperature. Thus it is logical to conclude that we should provide children with ample opportunity to analyze objects having varying sensory properties. When presenting activities designed to promote the development of haptic perception, we should vary objects by one sensory property and also offer objects with a combination of sensory properties. If the child has the opportunity to sort objects haptically in a variety of ways, he or she is likely to identify or sort objects using the sensory property that has the strongest distinctive features or use exploratory procedures or strategies that are most well developed in his or her repertoire. The sensory properties that the child consistently avoids using may be those that are most delayed and thus most in need of being addressed in treatment. Because little is known about the development of haptic figure-ground perception in children, we do not know if the finding of impaired haptic discrimination in multisensory haptic play activities is normal or a sign of impairment. However, we can be sensitive to the signs of haptic sensory overload in children. It is possible that playing with toys having several sensory properties may be disorganizing for some infants and children. When problems are seen, controlling the variety, as well as the quantity of sensory experiences may be necessary to elicit optimum performance during school and play activities.

FUNCTIONS CONTRIBUTING TO HAPTIC PERCEPTION Most haptic perception tasks are complex. Research suggests that various factors contribute to haptic perception, including somatosensory processing, manual and in-hand manipulation, and vision and cognition.

Perceptual Functions of the Hand • 69

ROLE OF SOMATOSENSORY SENSATION IN HAPTIC PERCEPTION Vierck (1978) proposed that sensory feedback processed through the dorsal columns may guide exploratory hand use. Although the firing of haptic neurons in the sensorimotor cortex often is credited for guiding exploratory hand use and contributing to the ability to recognize objects by touch, synaptic connections among many central nervous system (CNS) structures are involved in the process (Carpenter, 1991; Goodwin & Wheat, 2004; Mountcastle, 1976). Recent research examining neural substrates of tactile object recognition using functional magnetic resonance imaging (in adults) found that tactile object recognition involved a complex network including parietal and insular somatosensory association cortices, as well as occipitotemporal visual areas, prefrontal, and medial temporal supramodal areas, and medial and lateral secondary motor cortices (Reed, Shoham, & Halgren, 2004). Disruption in communication anywhere within this circuit logically could result in loss or impairment of the ability to explore objects with the hands. A synthesis of information derived from somatosensory receptors provides the hand with a dynamic picture of the body and its orientation in space (body scheme) (Gardner, 1988; Goodwin & Wheat, 2004). This internal picture of the body is thought to be used by CNS processes as a framework of the parameters of real-world time and space (Brooks, 1986). Upon this framework are scaled motor commands used in motor programming and executing complex sequenced movements. This internal picture of the body also is thought to serve as a template for interpreting the spatial properties of objects (Gibson, 1962). The precise detail of this internal picture of the body decreases and its spatial complexity increases with progressive afferent processing in the CNS (Brooks, 1986). Not only does somatosensory sensation contribute to the development of body scheme needed for the interpretation of the spatial properties of objects, but it also appears to be necessary for regulating manual and in-hand manipulation during active touch. Research with children with spastic hemiplegia found that deficient tactile sensitivity was strongly related to the manual dexterity needed for exploration (Gordon & Duff, 1999; Krumlinde-Sundholm & Eliasson, 2002). The sensory control of hand movements is discussed in Chapter 1. At present it seems sufficient to note that to actively retrieve somatosensory sensation from the environment during active touch the individual must be able to make rapid and frequent changes in the speed and sequencing of hand movements and regulate force during object manipulation (Hollins & Goble, 1988; Johnson & Hsiao, 1992). These elements of fine

motor coordination are thought to be related, in part, to the processing of tactile, kinesthetic, and proprioceptive sensations for their execution (Brooks, 1986; Case-Smith, 1995; Case-Smith, Bigsby, & Clutter, 1998; Duque et al., 2003; Gordon & Duff, 1999; Johansson & Westling, 1988, 1990).

ROLE OF MANUAL MANIPULATION AND EXPLORATORY STRATEGIES IN HAPTIC PERCEPTION Manual exploration and in-hand manipulation are critical for haptic perception and object recognition (Lederman & Klatzky, 1998, p. 27). It has been suggested that information from the motor commands generating exploratory actions generates corollary discharge or efferent copy and is involved in haptic perception, although the mechanisms are not well understood (Jeannerod, 1997). Interest in the role of in-hand manipulation and other forms of manual exploration in haptic perception was precipitated by the work of Gibson (1962) on active and passive touch. Using a set of geometricshaped cookie cutters, adult subjects either were allowed to actively manipulate the cookie cutters or the tactile stimuli were passively presented by the examiner (cookie cutters pressed or pressed and turned in the palm of the subject’s hand). The use of active touch contributed to greater accuracy in intermodal (hapticvisual) shape recognition than either of the passive touch conditions, although pressing and turning the cookie cutters in the subject’s hand (passive pressure with movement) yielded higher scores than the isolated use of passive pressure. Replication of Gibson’s study with children yielded similar findings (Haron & Henderson, 1985). Cronin (1977) also replicated Gibson’s study but obtained somewhat different results. She found that shape recognition by school-age children and young adults did not differ between active touch and passive touch (passive pressure with movement) conditions when tactile stimulation was restricted to the palm of the hand in all test conditions; however, the isolated use of passive pressure (passive pressure without movement) contributed to lower test scores than either of the other two test conditions. In addition, no difference between active touch and passive touch (pressure with movement) was found for the discrimination of texture and tactile maze learning in adults (Lederman, 1981; Richardson, Wuillemin, & MacKintosh, 1981). These findings suggest that it might be movement of the object over the skin surface that produces the tactile feedback needed for object recognition. Although movement of the object in the hand theoretically can be active or passive, it is most

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commonly produced actively, through the use of manual manipulation and exploratory strategies. This raises the question of how the pattern of tactile feedback generated by variation in the pattern of manual and in-hand manipulation affects the accuracy of object identification. In recent years several researchers have attempted to answer this question; their findings are discussed in the following section. See Chapter 8 for a detailed discussion of in-hand manipulation. Because most of the research on this topic has been done on adults, this section begins with a summary of the adult research followed by a review of the pediatric literature.

Haptic Manipulation Strategies in Adults In a series of studies, researchers (Klatzky, Lederman, & Reed, 1987; Lederman & Klatzky, 1987, 1990, 1998) found that adults were highly systematic in the manual exploration strategies they used. Adults performed “a variety of stereotypical hand movement patterns” (Lederman & Klatzky, 1998, p. 27), including lateral motion, pressure, static contact, unsupported holding, enclosure, and contour following, that Lederman and Klatzky called “exploratory procedures or EPs” (p. 27). These strategies were selected based on the particular object property the adult desired (e.g., hardness, texture, shape). Early research on the influence of manipulation strategies in object recognition was done by Davidson in a series of studies comparing the ability of sighted and congenitally blind subjects to recognize raised curved edges. Davidson (1972) and Davidson and Whitson (1974) found that when exploring concave, convex, and straight edges, subjects chose to use three manipulation strategies (gripping, pinching the edge, and sweeping the fingers over the top edge). Gripping (grasping the object in the hand) led to fewer errors in identifying the form of the curved edges in both blind and sighted subjects. Gripping was later found to be a useful strategy for obtaining a general understanding of the objects’ tactile properties (e.g., texture, weight, shape) (Klatzky et al., 1987; Lederman & Klatzky, 1987). The method of gripping (called enclosure in some studies) was modified to aid in differential discrimination of size and shape. Subjects preferred to grip with the whole hand when analyzing the size of objects and grip, with effort, the edges of the object using the fingers and palm when analyzing shape (Reed & Klatzky, 1990). Although gripping provided subjects with a general classification of object properties, other strategies often were used when refined analysis was needed. Contour following (moving the fingers around the edge of the object) was an optimum strategy for use in haptic shape recognition (Lederman & Klatzky, 1987). In a thorough analysis of strategies used in the

identification of geometric shapes, Kleinman and Brodzinsky (1978) found that subjects preferred to use a combination of manipulation strategies, including an initial scanning of the standard and comparison objects. This was followed by detailed simultaneous comparison of the standard and comparison objects (congruent feature comparison of analogous and mirror-image features and contour following). The initial time spent in scanning the objects was reduced as the shapes became more complex. Locher and Simmons (1978) found that haptic recognition of symmetric shapes was more difficult than the recognition of asymmetric shapes. Partial trace scanning (contour following along portions of the shape) was common for asymmetric shapes. More complex scanning strategies were used for the identification of symmetric shapes (several repetitions of partial and complete contour following). In a subsequent study Simmons and Locher (1979) found use of the trace scanning strategy (contour following around the complete shape several times using two fingers) to lead to greater accuracy in the identification of asymmetric shapes and the simultaneous apprehension scanning strategy (smooth, continuous movement of thumb and index fingers of both hands over opposite sides of the shape simultaneously) to lead to greater accuracy in the identification of symmetric shapes. The results of these studies suggest that the isolated use of contour following may not always be the most appropriate approach for use in the identification of shapes. It may be necessary to change manipulation strategies to adapt to variation in symmetry of distinctive features and complexity of the objects presented. Lederman and Klatzky (1987) analyzed manipulation strategies used for the identification of texture, hardness, weight, volume, and temperature. They found that the optimum manipulation strategy (which they termed exploratory procedures) for use in object identification differed for each tactile property (Table 4-1). Although contour following was necessary for accurate recognition of shape, several approaches could be used for the identification of most other tactile properties (Box 4-1). Preferred manipulation strategies remained unchanged when subjects were asked to determine the gradations of a given tactile property (texture, size, shape, and hardness) and when they needed to simultaneously sort pouches (fabric-covered shapes) by one to three of these tactile properties (Klatzky, Lederman, & Reed, 1989; Lederman & Klatzky, 1987). Enclosure (gripping) was commonly used for all tactile properties, with lateral motion being used primarily for the identification of texture, pressure being primarily used for the identification of hardness, and contour following being used primarily for the identification

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Table 4-1

Haptic procedures associated with acquiring knowledge about objects

Object Dimension

Exploratory Procedure

SUBSTANCE Texture Hardness Temperature Weight

Lateral motion Pressure Static contact Unsupported holding

STRUCTURE Weight Volume Global shape Exact shape

Unsupported holding Enclosure; contour following Enclosure Contour following

FUNCTION Part motion Specific function

Part motion test Function test

Data from Lederman SJ, Klatzky RL (1987). Hand movements: A window into haptic object recognition. Cognitive Psychology, 19:342–368.

BOX 4-1

Most Effective Strategies Used for Identification of Tactile Properties (Other Than Recognition of Shape)

1. Texture: lateral motion (moving the finger across the surface of the object) 2. Hardness: pressure 3. Weight: unsupported holding* 4. Volume: enclosure (gripping) 5. Temperature: static contact *Jiggling while holding the object aided in the discrimination of weight. Brodie EE, Ross HE (1985). Jiggling a lifted weight does aid discrimination. American Journal of Psychology, 98:469–471.

of shape and size. When pouches needed to be simultaneously sorted by two or three properties, the manipulation strategies were combined, with lateral motion and pressure often being merged into a single finger movement. When the properties of texture and shape needed to be analyzed, adults appeared to search for cues about texture before they searched for cues about the object’s shape (Lederman, Brown, & Klatzky, 1988). Subjects showed a preference for manipulation strategies that could simultaneously

analyze two tactile properties. Exploration time decreased when subjects used lateral motion and pressure to simultaneously discriminate texture and hardness and when they used gripping (enclosure) to simultaneously discriminate size and shape (Klatzky, Lederman, & Reed, 1989; Reed & Klatzky, 1990). This finding suggests that adults may prefer manipulation strategies that simultaneously explore multiple sensory properties. Not only do subjects select haptic manipulation strategies based on the tactile properties of objects, they also organize manipulation strategies into a sequence. Lederman and Klatzky (1990) found haptic exploration in adults consisted of a two-stage sequence. The first stage consisted of generalized exploration of the object using manipulation strategies such as gripping (enclosure) or unsupported holding (object resting in the palm of the open hand), strategies that provided awareness of the general tactile properties of the object. This was followed by a second stage of refined manipulation, in which the subject used more specialized manipulation strategies (e.g., contour following, lateral motion) to gain specific information about object characteristics. During the second stage the subject often alternated between different manipulation strategies to guide the retrieval of information about the object. In summary, results of research on haptic manipulation and exploratory strategies provide support for the hypothesis that the pattern of tactile feedback generated by variation in patterns of manual manipulation during active touch contributes to the accuracy of object recognition. Adults select manipulation strategies based on the tactile properties of the object being explored. Furthermore, they combine and sequence the use of these manipulation strategies in situations in which conditions require the simultaneous or sequential analysis of several tactile properties. The sophisticated haptic manipulation strategies seen in adults develop throughout childhood.

Haptic Manipulation Strategies in Infants Haptic exploration begins in early infancy. Neonates and young infants gain much information about objects from action with their mouth. At 2 and 3 months spontaneous interaction with a novel object starts with an oral contact (Rochat, 1989). Ruff and co-workers (1992) reported that oral exploration or mouthing increased until 7 months, and then decreased through 11 months in favor of manual manipulation. By 4 months, even though vision emerged as the initial modality of exploration, infants continued to frequently bring the object to their mouth. Spontaneous behavior by infants suggests increasing multimodal (visual and haptic) organization of exploration, with vision playing a growing role. According to Rochat (1989), the hands

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serve both transport and support functions, bringing the object alternately into the oral zone and the field of view for exploration. Ruff (1989) described a dual role of handling: the hands make information available to the eyes as the object is manipulated at the same time that the hands directly gather haptic information. In the first role the hands are used to manipulate the object and change the object’s location relative to the observer, such as turning the object around to provide different visual perspectives. In the second role the hands gather haptic information about the object, such as by pressing the object to determine its substance or rubbing a finger across the object to determine its texture or shape. Based on their developmental work, Bushnell and Boudreau (1991, 1993, 1998) suggested that the motoric capacities needed to perform exploratory procedures limit haptic perception in the young infant. In conjunction with the early development of multimodal exploration, the characteristics of object manipulation change from 2 to 5 months. At 2 to 3 months the infant’s manipulative behaviors are primarily limited to grasping movements, potentially informing the infant about the object’s substance, temperature, and size (Bushnell & Boudreau, 1991, 1993). Although slight finger movements are produced at 2 months, by 4 months the occurrence of fingering behavior increases significantly (Rochat, 1989). Because discrimination of texture requires isolated finger movements, texture discrimination does not begin until around 6 months of age. Before this, when both hands are involved in contacting an object, it is primarily for transporting the object to the mouth. Rochat (1989) noted that in young infants (2 to 4 months) bimanual coordination is initially linked to the oral system. This observation points to the importance of the mouth in the early manifestation of bimanual action in the context of object manipulation. The hand–mouth coordination seen in the 2- to 4-month-old infant is later combined with vision when behaviors such as fingering emerge. To more thoroughly assess how infants use object handling skills to gain information for recognition of specific object qualities, Ruff (1984) studied 6-, 9-, and 12-month-old infants and assessed the various manipulation strategies they used, including mouthing, fingering, transferring, banging, and object rotation. Fingering proliferated with increased age, particularly with objects that varied in texture. Ruff suggested that this fingering can be crucial for obtaining information about small object details. Hand use for object rotation also was noted to change, with all infants using a onehanded rotation pattern, in which the arm or wrist moves, but only older infants using two-handed object rotations. Ruff suggested that two-handed rotation can be particularly useful because with rotation the object does not have some parts covered by the hand. She

suggested that infants who cannot adjust their handling skills so they can finger objects rather than just hold them and infants who cannot effectively use two hands together may be limited in the complexity of information about objects that they can readily gather. Discrimination of shape does not occur until between 9 and 12 months when the infant learns to turn and rotate an object in two hands (Ruff, 1989). Given that adults use a flexible repertoire of exploratory strategies and that certain actions may be particularly useful for obtaining specific information about objects, the question also has been asked how, during development, young infants and children tailor their actions to explore objects (Palmer, 1989). Whereas earlier work has suggested that infants’ actions were not clearly related to object attributes (McCall, 1974), current research has found that exploratory action patterns are indeed influenced by object characteristics and that the actions of the infant are related in functional ways to the structure of the environment (Gibson, 1988; Hatwell et al., 2003). In a series of studies, Ruff (1980, 1984, 1989) examined the effect of object characteristics on infant manipulation strategies. In a study of 9- and 12month-olds, Ruff (1980) found that infants fingered objects with surface texture more than they fingered smooth blocks. Ruff (1984) investigated 6- to 12month-old infants’ manipulation of a range of objects varying in color, shape, texture, and weight and found that manual exploration was adapted to the visual and the tactual properties of the object. When infants were given objects that varied in shape, they rotated the objects and transferred them from one hand to the other hand; when objects had varying surface textures, infants fingered the objects, often scratching their surface. Weight change resulted in less looking and more banging than did other changes in object characteristics. In a more recent study Ruff (1989) found that by 7 to 9 months infants banged hard objects more than soft objects, banged more on hard surfaces than on soft surfaces, and fingered textured objects more than smooth objects. In a study of 12-month-old infants’ haptic exploration and discrimination, Gibson and Walker (1984) found that infants squeezed, rubbed, and pressed a spongy object more than a rigid object and banged the rigid object more than the spongy one. The results of these studies suggest that infants adjusted their manipulative behavior to the characteristics of objects. Palmer (1989) also found that infants 6, 9, and 12 months old tailored their actions to particular object and table characteristics. Palmer recorded the manipulative behavior of infants with 12 different objects of varying rigidity, texture, shape, weight, and sound potential using two different table surfaces (hard wood

Perceptual Functions of the Hand • 73 BOX 4-2

Actions Used by Infants in Object Exploration

Grasping Banging Fingering Mouthing Switching (hand to hand) Squeezing Rubbing Pressing Poking Slapping Scooting Dropping

and foam covered). Results indicated that infants made use of both object properties and table surface properties. For example, infants banged more on the wood surface. Age differences in actions were also noted. Palmer suggested that these differences may reflect developing action economy (e.g., waving the bell with a flick of the wrist rather than with the whole arm swing seen in younger infants), new exploratory systems (e.g., changing from mouthing to waving and banging), and increasing fine motor control (e.g., finger individuation). Case-Smith and co-workers (1998) examined 120 2- to 12-month-old infants and also found that infants’ grasp and manipulation strategies varied as a function of the objects’ haptic attributes (size, shape, contour, movable parts) and the child’s age. They found that objects with movable parts elicited more varied and mature manipulation strategies and suggested that objects with movable parts and multidimensional surfaces “facilitate haptic development and motor skill by affording the infant a variety of surfaces to explore and by sustaining the infant’s interest” (p. 108). Research suggests that even infants younger than 6 months detect an object’s perceptual features that enable particular actions (affordances) for hand and mouth. Rochat (1983, 1987) found that neonates showed differential oral and manual responding to objects varying in substance and texture. In a study of 3-month-old infants, Rochat (1989) noted that the characteristics of manual manipulation and exploration by the infant reflected some relation to the physical properties and affordances of the object (Box 4-2).

Haptic Manipulation Strategies in Children Research with children has focused primarily on analysis of the role of manipulation strategies in the development of haptic discrimination of shape and size (length). Results of these studies suggest that there is a

Table 4-2

Developmental progression for haptic discrimination of shapes and objects

Age Range

Haptic Strategy

21⁄2 to 4 years

Children may play with object (e.g., push), but there is no active manual exploration; grasping or touching of object is seen with palm being still when making contact with object; by 3 to 6 years child begins to make discoveries about discriminative features seemingly by chance

4 to 5 years

Exploration often remains passive, with object being grasped between palm and middle fingers; crude manual exploration begins; when manual exploration is seen, it is done in a global haphazard manner, which includes probing for distinctive features

5 to 6 years

Systematic use of both hands (palms and fingers) begins; isolated analysis of distinctive features without studying whole form can be observed

6 to 7 years

Use of systematic method of exploration can be seen; contour following is used

developmental progression in the acquisition of manipulation strategies, with the accuracy of object identification being related to the level of sophistication of the haptic manipulation strategies (Abravanel, 1968b; Hatwell, 2003; Hoop, 1971b; Jennings, 1974; Kleinman, 1979; Wolff, 1972; Zaporozhets, 1965, 1969). The description of the developmental progression of haptic discrimination of common objects and shapes in Table 4-2 is a summary of the work conducted by Piaget and Inhelder (1948/1967) and Zaporozhets (1965, 1969). Whereas haptic strategies of the 2- to 4-year-old child consist primarily of grasping the object, by age 6 to 7 years systematic exploration with contour following is noted. Abravanel (1968b) provided a description of the developmental progression in haptic manipulation of size (length) that was strikingly similar to that identified

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Examples of Manipulation Strategies

If children want: • To compare two objects for texture, they use a lateral motion, often with the index finger. • To compare hardness, they use pressure. • To examine temperature, they use static contact. • To examine volume of three-dimensional objects, they tend to embrace the object. • To compare weight, they tend to hold the object in their hand and lift it from the surface. Hatwell Y (2003). Manual exploratory procedures in children. In Y Hatwell, A Streri, E Gentaz (editors): Touching for knowing (pp. 67–82). Philadelphia, John Benjamins Publishing; Klatzky RL, Lederman SJ (2003). The haptic identification of everyday life objects. In Y Hatwell, A Streri, E Gentaz (editors): Touching for knowing (pp. 105–122). Philadelphia, John Benjamins Publishing; Klatzky RL, Lederman SJ, Metzger VA (1985). Identifying objects by touch: An “expert system.” Perception and Psychophysics, 37:299–302; Streri AF (2003a). Manual exploration and haptic perception in infants. In Y Hatwell, AF Streri, E Gentaz (editors): Touching for knowing (pp. 51–66). Philadelphia, John Benjamins.

for the analysis of common objects and shapes. She found that the youngest children in her study (3 to 5 years) typically used the palm of the hand, grasping and palpating the objects. By 5 years the children held the ends of the bar used for evaluating length. From 5 through 8 years children used the whole hand (palm with progressively increasing use of the fingers) for manipulation of the bar and displayed a systematic method of determining length. By 9 years, use of the palm was no longer seen; the fingers and fingertips were used for exploration. Researchers have shown that the manipulation strategy used by the child or adult varies as a function of the information to extract (Box 4-3) (Hatwell, 2003; Klatzky & Lederman, 2003; Klatzky, Lederman, & Metzger, 1985; Streri, 2003a). In summary, the results of studies that address analysis of strategies used in the recognition of common objects, shapes, and sizes, including lengths, suggest that manipulation strategies become more complex with increasing age, a maturational change that seems to contribute to the accuracy of haptic object recognition. The structural characteristics of the test materials influence the time spent in haptic exploration, perhaps because they contribute to task difficulty or they affect the complexity of manipulation strategies needed for object exploration. The effect of object characteristics on the use of manipulation strategies has been extensively addressed in infants, and

to a lesser extent in preschool and school-age children. Infants use a variety of actions in exploring objects (see Box 4-2). These actions vary as a function of the object and surface characteristics; that is, they are influenced by the perceptual affordances provided by the environment, as well as by the infants’ motor abilities.

ROLE OF VISION AND COGNITION IN HAPTIC PERCEPTION Vision McLinden and McCall (2002) emphasize that most skills and activities are performed with information from multiple modalities simultaneously. They discuss the role of vision in coordinating or integrating a wide range of sensory information. Warren and Rossano (1991) describe the important role that vision plays in the development of haptic perception. Noting that vision and touch are constant companions, Pears and Jackson (2004) discuss how the brain dynamically binds together visual and somatosensory information to construct accurate representations of objects in space, and emphasize the importance of this linkage for acting on objects in the world around us. Rochat (1989) noted a major link between vision and fine haptic exploration early in development and suggested that vision may serve as a potential organizer of multimodal exploration and object manipulation in infancy. This was based on research that indicated that fingering starts to manifest itself in coordination with vision. Refined object manipulation was more likely to occur when infants simultaneously looked at and manipulated objects. Thus it may be important for infants to see their hands during manual object manipulation. As further support of the role of vision as an organizing factor of object manipulation, Rochat (1989) cited developmental studies of congenitally blind infants, who exhibited drastic delays in the use of their hands as exploratory tools (Fraiberg, 1977). Even though congenitally blind toddlers spontaneously developed strategies such as object rotation (Landau, 1991), haptic exploration was primarily oral up to 3 to 4 years of age, much longer than was seen in sighted infants. Thus the use of vision in object exploration may be important for the development of haptic perception. However, this is not to say that haptic perception cannot be developed in the absence of vision. For example, Schellingerhout, Smitsman, and Van Galen (1997, 1998) examined the haptic exploratory procedures of surface textures in eight infants, 8 to 24 months old, who were congenitally blind. They found that younger infants showed a wide range of exploratory strategies and older infants used these strategies in a specific manner.

Perceptual Functions of the Hand • 75 Hatwell (1990) suggested that even sighted children between the ages of 3 months and 6 years have difficulty using their hands for retrieving haptic information independent of vision. She suggested that the motor functions of young children’s hands were primary, with the perceptual capabilities of the hands rarely used except as an adjunct to motor functioning. Hatwell noted that when vision was used, the hands primarily operated under this system of control. Ruff (1989) tempered this view by stating that it may be that the visual system guides exploratory behavior in the haptic system. In this sense, vision would not exclude the contribution from the haptic system as put forward by Hatwell (1987) but would constrain it. Ruff (1989) suggested that there was an “initial tightening of visual control over manipulation around 5 months of age [and] then the loosening of visual control sometime after nine months” (p. 313). Haptic manipulation with vision is important in the early learning of object characteristics and has two potential advantages. First, as infants look at an object they are manipulating, they see the object from different points of view and can learn about its properties. This is critical for the development of object recognition so that the infant or child can recognize an object in any orientation or in any context. Second, the infant acquires tactile and kinesthetic information about the object through active touch (Ruff, 1980, 1982; Streri, 1993, 2003a). Ruff (1980) suggested that movement is particularly important in helping infants to detect the properties of an object that does not vary despite changes in the object’s orientations. An important question is what type of movement is necessary. For example, the infant can produce different information about the object through his or her own movements such as through turning the head to look at the object, by moving the body around the object, or by holding, manipulating, and moving the object. Alternatively, the infant can get different views of an object when a parent carries the infant around the room, or when the object itself moves, as in a mobile, or when a parent moves the object, such as in the context of showing a toy to a child. Ruff (1980) hypothesized that object transformations that occur during movement allow for detection of object characteristics that would not be evident from observing a stationary object. She also suggested that, although both watching object movement and producing object movement were important in learning about objects, producing movement could yield the specific types of information sought and therefore was a more efficient way of learning about objects. The advantage to the individual doing the moving is that infants learn to recognize objects in the context of activity. Ruff (1980) found that 6-month-

old infants learned structural differences in objects only when they actually manipulated the objects; viewing object movement did not result in the learning of object characteristics. It should be emphasized that, in the manipulation condition, the infants also visually monitored their movements, thus obtaining tactile, proprioceptive, and visual information. Ruff proposed that the advantage of object manipulation may be in the simultaneous use of visual and tactile integration in learning about object qualities. The heavy use of vision in object identification seen in infants may continue into adulthood. Research comparing visual and haptic discrimination has shown visual matching to be consistently superior to haptic and intermodal (haptic-visual and visual-haptic) matching (Garbin, 1988; Hatwell et al., 2003). This finding has left the impression that vision may be more important than haptic discrimination in object identification. Nevertheless this may be an incorrect interpretation of the research findings. Klatzky and co-workers (1985) questioned this conclusion, stating that it might be inappropriate to use objects that can be easily interpreted by the visual system when evaluating functions of the tactile system. Rather than vision being superior to haptic manipulation, it would probably be more accurate to say that vision and somatosensory processing both play supportive roles in object identification. Although vision seems to be used by infants and young children to guide exploratory hand use, its purpose may not be to substitute for haptic perception but rather to guide the development of haptic manipulation and make the somatosensory input meaningful.

Cognition The development of infants’ and young children’s exploration of the environment is linked to their understanding and knowledge about the world (Bushnell & Boudreau, 1998; McLinden & McCall, 2002). Because cognition and vision are closely linked in haptic object identification, it is difficult to categorize certain functions, such as mental imagery, that involve both cognition and vision. The ability to use cognitive strategies (mental imagery and verbalization) to aid in haptic object recognition develops during childhood. Piaget and Inhelder (1948/1967) considered the ability to distinguish objects through the use of touch to be an external reflection of one’s capacity to transform tactile properties of objects into visual images (integrate visual and haptic information), although recently this view has been questioned. This ability to use visual imagery to improve haptic recognition and memory of objects is thought to contribute to children’s ability to recognize objects on tests of haptic perception and reproduce objects through drawing. In fact, research has shown that adults with high spatial ability and skill in

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mental imagery perform significantly better than their less skilled peers on tests of haptic perception (McCormick & Mouw, 1983). Verbalization (labeling of the haptic properties of objects) also has been found to aid in haptic object identification. Bailes and Lambert (1986) compared the ability of adults who were sighted and blind to determine if four segments of a stimulus figure matched a completed geometric design. The subjects who were sighted were faster and more accurate than the subjects who were blind. Adult subjects who used verbalization had better haptic accuracy scores than subjects who used a mixture of verbalization and mental imagery. Subjects who solely used mental imagery displayed the lowest haptic accuracy scores. Thus in some tasks, verbalization may be a more effective strategy than mental imagery, although both may be beneficial. The ability to use cognitive strategies (mental imagery and verbalization) to aid in haptic object recognition develops during childhood. Children 3 to 6 years of age often could not describe the strategies that they used to aid in haptic object identification (Blank & Bridger, 1964). By the fourth grade several solely used verbalization or mental imagery, whereas most relied on a mixture of verbalization and visual imagery to aid in haptic object identification (Ford, 1973). Adults were evenly mixed in their isolated use of verbalization and mental imagery, and combined use of the two cognitive strategies (Bailes & Lambert, 1986). Alexander, Johnson, and Schreiber (2002) examined the effect of 4- to 9-year-old children’s domain-specific knowledge on their performance in haptic comparison task. Children with varying levels of knowledge about dinosaurs haptically explored pairs of familiar (dinosaur) and unfamiliar (sea creature) models and were asked to state whether or not the pairs were identical. Older children correctly identified more pairs than younger children and explored models more exhaustively. Although dinosaur knowledge did not affect overall performance, it did affect the types of explorations that to some extent resulted in increased errors. Specifically, after exploring the first object, children with high knowledge about dinosaurs tended to form an initial hypothesis (e.g., based on one feature such as the beak) and then sought evidence to confirm this initial hypothesis by primarily exploring just the beak of the possible matches. In doing this, they ignored or failed to seek out evidence (e.g., exploring the dinosaur’s feet) that did not confirm their hypothesis.

SUMMARY AND I MPLICATIONS FOR PRACTICE Several functions contribute to the ability to perform haptic perception tasks. Because an individual performs poorly on tests of haptic perception does not mean that

somatosensory processing is impaired. Impairment in somatosensory processing, vision, visual perception, cognition, praxis, and any factor that may alter fine motor coordination has the potential to lower performance on tests of haptic perception. Determining the reason for a child’s poor test performance is a necessary prerequisite for effective treatment planning. In the clinic we may be able to gain some insight into the maturity of the somatosensory system by observing the tendency of infants to mouth and manipulate novel objects. Although infants use vision extensively in object exploration, we should expect to see a combination of visual and oral or manual exploration during play in infancy. Although research indicates that optimum performance in haptic identification is seen when manual manipulation is used for object identification, haptic perception can be partially assessed without active manipulation. Research has shown that placement of the object in the palm of the hand and movement of the object across the skin’s surface improves object recognition. Thus the therapist can occlude the child’s vision, move the object across the center of the palm, and then ask the child to identify the object by visual matching or verbal response. Analysis of the quality of the haptic manipulation strategies used during test performance also provides useful diagnostic information. The preferred manual manipulation and exploratory strategies of adults vary for objects with different tactile properties. The manipulation strategy used affects the accuracy of object identification. Research suggests that the development of haptic manual manipulation and exploratory strategies begins early in life, because infants use specific manipulation strategies to explore specific sensory properties. During childhood these manipulation strategies grow in complexity with increasing age. We do not know whether children with problems in haptic perception and fine motor coordination fail to use appropriate manipulation strategies because they have difficulty in the selection or execution of haptic manual manipulation and exploratory strategies. However, it is generally recognized that the immature haptic manipulation strategies seen in young children contribute to poor object recognition (Abravanel, 1968b; Derevensky, 1979; Hatwell, 2003; Hoop, 1971b; Jennings, 1974; Wolff, 1972; Zaporozhets, 1965, 1969). Early haptic exploration in infancy is done with the mouth. It is more than a year before mouthing is primarily replaced by manual manipulation. We cannot overemphasize the clinical importance of mouthing objects in infancy. Mouthing of objects not only seems to be important for decreasing oral hypersensitivity and facilitating oral motor development, but it also appears to be important for environmental learning and may

Perceptual Functions of the Hand • 77 contribute to the early development of bilateral hand use. Infants who exhibit little mouthing of objects should be evaluated to determine the cause of the delay. Even older children who exhibit tactile defensiveness and those with problems in haptic discrimination should be encouraged to engage in oral and manual exploration of objects. It takes creativity and close interaction with parents to find socially acceptable ways to encourage mouthing beyond infancy. Children also can show a prolonged need for mouthing of objects. If the behavior is caused by oral-tactile defensiveness or poor haptic discrimination, then mouthing should be encouraged. However, if the behavior is caused by impaired visual-haptic integration or poor purposeful use of objects, then treatment should be directed toward pairing vision and oral-manual manipulation during purposeful interaction with objects. A bigger challenge is seen in children with multiple handicaps and those who have severe impairment in motor function. We should help these infants incorporate mouthing of toys into daily play activities and find ways to attach toys to clothing and position equipment so that toys can easily reach the mouth. Vision is paired with haptic exploration of the hands throughout infancy and early childhood. Vision appears to guide the development of haptic manipulation strategies. It is not until later in life that vision and somatosensory sensations appear to take on separate but supportive roles in object identification and use. The importance of vision in the development of haptic manipulation is seen in blind infants. Whereas typical infants begin to replace mouthing with manual manipulation at about 4 months, blind infants continue to identify objects orally, with mouthing the dominant form of exploration until 3 or 4 years of age (Landau, 1991). Because vision appears to be necessary for the development of haptic manual manipulation, the use of haptic exploration with the hands should be specifically taught to blind infants; we cannot assume that, because the infant is not using vision, he or she will automatically use the hands for environmental exploration. Interplay between vision and haptic exploration seems to be needed for environmental learning in infancy and early childhood. Under the age of 5 or 6 years activities should be designed that pair vision and touch in addition to using the haptic sense alone. The identification of object features should be integrated in these activities. An exception is seen in children who overuse vision to guide hand use. For these children vision should, at times, be removed from the play activities to encourage the child to retrieve and use haptic information. Haptic object identification is made possible by combining vision and cognition. The use of visual imagery and verbalization helps improve haptic

memory and discrimination. We cannot assume that children will automatically learn cognitive strategies to aid in haptic task performance. For children with attention deficits, brain injury, and mental retardation, the interpretation and use of haptic information might be enhanced by teaching them to use cognitive strategies such as mental imagery or verbalization techniques during task performance. In addition, we know that the ability to identify an object haptically proceeds not only from extracting information from the stimulus or object that is presented, but also by combining “presented information with expectancies based on context or previous experience” (Klatzky & Lederman, 2003),

called top-down processing. Thus providing a cue such as “this is a fruit,” in advance of giving the child an object to manipulate may result in improved performance.

EVALUATION OF HAPTIC PERCEPTION IN INFANTS AND CHILDREN Assessment of haptic perception can be considered from the perspective of standardized versus nonstandardized assessments and also analyzed according to product/process dimensions. Most of the standardized assessments examine the product; that is, the accuracy of haptic perception, and the number of items the child passed. Many of the nonstandardized assessments used primarily for research purposes examine the process, or the way the child approaches a task, and the effect of the nature of the task on haptic style or strategy. There are several standardized assessments to evaluate accuracy of haptic perception The Miller Assessment for Preschoolers (Miller, 1988) includes a stereognosis item that uses common objects for the younger (2- to 4-year-old) children and geometric shape matching for older (3- to 5-year-old) children. Although a specific score is not given for this item, percentile equivalents can be determined from the score sheet. The Sensory Integration and Praxis Tests (SIPT) (Ayres, 1989) make up a 17-test battery that assesses aspects of sensory processing (visual, tactile, vestibularproprioceptive) and praxis. They are standardized on children ages 4.0 to 8.11 years. This battery includes several tests that tap aspects of haptic abilities. The Manual Form Perception (MFP) test, which assesses stereognosis, has two components. The first component is a haptic-visual intermodal matching task in

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which the child feels a geometric shape without the use of vision and points to its visual counterpart from among a set of choices. The second aspect of the test is a haptic-haptic intramodal matching task in which the child feels a geometric shape with one hand and explores a set of five shapes to find its match with the other hand. The MFP test is a complex task that, when used in conjunction with the SIPT, contributes to identification of various problems including haptic perception, form and space perception deficit across sensory systems, problems in visualization, and somatodyspraxia. The haptic-haptic matching component of the test also reflects functional integration of the two sides of the body (Ayres, 1989). In the graphesthesia test (GRA) of the SIPT, the examiner draws a design on the back of the child’s hand and the child must reproduce that design with his or her finger. This is not truly a haptic perception task because the tactile input is received passively not through active manipulation. Nevertheless it is similar to many haptic perception tasks because the child needs to interpret designs received through moving touch applied to the hand and then signify knowledge of the design by a motor response. As with tests of haptic perception, fine motor coordination and motor planning abilities are necessary for optimal test performance (Ayres, 1989). Another standardized test that includes aspects of haptic perception is The Luria-Nebraska Neuropsychological Battery: Children’s Revision (Golden, 1987), a 149-item test battery designed to assess a broad range of neuropsychological functions in children ages 8 to 12 years. There are 11 different scales, one of which assesses tactile functions. The 16 items on this scale assess tactile localization, tactile discrimination, intensity, tactile spatial discrimination, direction of movement, identification of traced shapes and numbers, and identification of objects. The specific items on the Tactile Function Scale that address aspects of haptic perception include two items that assess stereognosis, in which the examiner places an object (quarter, key, paper clip, and eraser) in the child’s hand and the child must name the object. If word-finding difficulties are suspected, the examiner can place the four objects in front of the child along with four other objects and ask the child to point to the object he or she just felt. There are also four items that are similar to the graphesthesia test of the SIPT. In these items the child is required to recognize a cross, triangle, and circle drawn on the back of his or her wrist with a pencil. There are two items in which a number is written on the back of the wrist. In these items the child needs to know only that a number was drawn and need not identify the specific number. An overall score is provided for the Tactile Function Scale. Although there is not a specific score

for the items assessing haptic perception, the examiner can look at performance on these items. The LuriaNebraska Scales usually are administered by a neuropsychologist and, like the Sensory Integration and Praxis Tests, require special training. However, the knowledgeable therapist can use results of this test to aid in evaluation. All the preceding tests examine accuracy of haptic identification. The manipulation strategies used in haptic exploration are not examined. At present there is no standardized examination of exploratory strategies. However, the work of Zaporozhets (see Table 4-2) provides guidelines for the therapist wishing to examine this area. If, for example, a therapist notes that a 7-year-old child is using only grasping to examine complex shapes, he or she can infer that this child is using immature and inefficient strategies to gain information about objects. Exner (1992) developed a test to examine in-hand manipulation in children ages 18 months through 61⁄2 years. Although the emphasis of this work is on the hand as a motor instrument used to accomplish specific skilled fine motor tasks with vision present, the process of adjusting objects within the hand after grasp (in-hand manipulation) is critical to enable effective haptic manipulation to gain perceptual information about an object (Case-Smith & Weintraub, 2002). There are no standardized assessments to examine haptic identification of the material properties of objects such as weight, texture, or object features such as length. Research has indicated that individuals use different strategies to gain information about these object characteristics. For example, if children are asked to match objects on the basis of texture, they use lateral motion; if they are asked to match objects on the basis of hardness or firmness, they use pressure; if they have to match on the basis of shape, they tend to use contour following (Streri, 2003a). In working with children with disabilities, we should examine whether they vary the strategy used in exploring different object properties as do typical children (McLinden, 2004; McLinden & McCall, 2002). Although the typical child does not need or receive specific training in how to use the haptic sense, it may be necessary to explicitly teach haptic manipulation strategies in children with disorders (McLinden & McCall, 2002). For therapists wishing to assess haptic abilities in young infants, the best assessments at present are observational qualitative assessments rather than standardized testing, although it is important to use a standard protocol to compare infants and see change in haptic style over time. It has been reported in the literature that from 6 to 12 months there is a decrease in mouthing and an increase in fingering behavior (Ruff, 1980; Streri, 2003a). Thus if at 12 months an

Perceptual Functions of the Hand • 79 infant is bringing everything to the mouth, one could identify a delay in the use of the hands for manipulation. Similarly, Ruff (1980) noted that 9- and 12-month-old infants adjusted their behavior to the characteristics of objects and more often fingered textured objects with prominent surfaces than smooth objects. Thus one could incorporate giving infants both smooth blocks and blocks with textures and surfaces and observing their response to these different objects. The information on the role of manipulation in haptic perception also provides guidance for evaluation. Along with noting the frequency of mouthing and the integration of vision and haptic senses in object exploration in infancy and early childhood, note the manipulation strategy used during performance on tests of haptic perception. Because the identification of common objects matures by 5 to 6 years and can be accomplished with little to no haptic manipulation, common objects may be useful only for assessing pre–school-age children. Changes in the method of manipulation seen during testing may be a better indication of change in haptic perception than is change in the child’s accuracy score. Expanding our assessment beyond the identification of geometric shapes to include the testing of other tactile properties allows us to look at the maturity and flexibility of manipulation patterns and provides insight into the child’s ability to recognize the scope of sensory properties encountered during daily activities. Examination of whether children vary their strategy as a function of the task demand provides information about the type of information the child receives through his or her haptic sense. When assessing haptic perception in individuals with multiple disabilities, such as visual impairment or visual impairment plus other disabilities, McLinden (2004) and McLinden and McCall (2002) caution against relying only on norm-referenced assessments because children with disabilities have different experiences and often do not develop in the same sequence as typical children. However, they recognize that there are no assessments to assess haptic perception that are standardized for children with disabilities. They recommend considering developmental assessments in conjunction with criterion-referenced procedures and process-oriented approaches, and emphasize that it is critical to examine how children use their sense of touch in naturalistic or functional situations. McLinden (2004) recommends using an “adaptive tasks” approach that identifies the child’s use of or response to touch in daily activities. (See also the Scottish Sensory Centre for a discussion of systematic ways to observe a child’s response to touch for learning.) Finally, in examining haptic perception, it is critical to examine the child’s response or reaction to tactile sensory input because this has a significant impact on

the child’s willingness to explore objects through his or her sense of touch. Children who show sensory defensiveness, such as may be seen in children who were preterm as infants (Case-Smith, Butcher, & Reed, 1998), may be unwilling to use their hands to gain information about the environment (Ayres, 1989). Case-Smith (1991) reported that children with tactile defensiveness and poor tactile discrimination demonstrated less efficiency in in-hand manipulation tasks. Response to touch can be assessed observationally while administering standardized assessments of somatosensory perception such as the SIPT, through assessment of sensory processing using caregiver questionnaires (Brown & Dunn, 2002a,b; Dunn, 1999) or through protocols designed for use with children with disabilities (e.g., Assessing Communication Together) that suggest a structure for observing response to touch (Bradley, 1991 as cited in McLinden & McCall, 2002, p. 89).

HAPTIC PERCEPTION IN CHILDREN WITH DISORDERS PREMATURITY The characteristics of touch most fully explored in the infant are those related to social and emotional functioning, and research on the perceptual role of touch often proceeds separately from research on its social role (Rose, 1990). Recently the specific role of tactile stimulation has been examined, and numerous studies have investigated whether the preterm infant will benefit from changes in the quantity, quality, or patterning of stimulation in the environment (Field, 2002, 2003). The sensory organization and perceptual processing characteristics of the preterm infant also have been investigated. Rose and co-workers (Rose, Schmidt, & Bridger, 1976; Rose et al., 1980) examined the infants’ responsivity to (passive) tactile stimulation and their abilities to discriminate different intensities of such stimulation. Infants were assessed at 40 weeks’ gestational age, and, while sleeping, they were touched with plastic filaments of different intensities and their cardiac and behavioral responses were examined. Results indicated that preterm infants are significantly less responsive to tactile stimulation than are full-term infants. Rose, Gottfried, and Bridger (1978) also examined differences between preterm and full-term infants at 1 year of age in an active touch multimodal (haptic and visual) task using a habituation paradigm. Preterm infants did not show any evidence of cross-modal transfer, whereas full-term infants did show such transfer. These results indicate that full-term infants are

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able to gain knowledge about the shape of an object by feeling it and mouthing it and that they are able to make this information available to the visual system. They were able to do this even after only 30 seconds of handling or mouthing of the object. On the other hand, preterm infants did not seem to know that the object they saw was the same object they were exploring with their hand or mouth. Overall, preterm infants were limited in acquiring information; they showed evidence of difficulty perceiving passive touch and effectively using active touch to explore their world. Interestingly, lower-income full-term infants also showed poorer haptic-visual integration than did full-term middle-income infants. Recognition memory also has been studied in premature infants (Rose, 1983; Rose et al., 1988), who were found to have longer initial exposures and less recovery with novelty, indicating slower and perhaps less complete information processing. Poor haptic perception appears to be long lasting. Two follow-up studies examined the long-term outcomes of children who were born preterm. Somatosensory processing, including haptic perception, was impaired when the children were examined at school age (DeMaio-Feldman, 1994; Short et al., 2003). Another research paradigm that has been found to discriminate between high-risk infants and their typical peers is manipulative exploration. Early studies of exploratory behavior from a Piagetian perspective documented decreased manipulation in premature infants but interpreted the decreased action to be a reflection of a disordered motor system that provided inadequate or inaccurate information (Kopp, 1974). Kopp examined the performance of premature and fullterm 8-month-old infants who were clumsy and nonclumsy (based on reach and grasp). The coordinated group of infants showed significantly more exploration of objects, particularly more mouthing. The infants with poor coordination used more large arm movements and less object manipulation than the infants with good coordination. Kopp discussed the value of object manipulation in enhancing attention and providing information to infants. However, she also pointed out that infants with poor manipulation skills may give extra attention to motor actions, leaving less attention available for sensory or perceptual processing. More recent studies have focused on the attentional and organizational differences between preterm and full-term infants because early focused attention reflects active learning and predicts cognitive outcome (Lawson & Ruff, 2004). Preterm infants exhibit shorter duration of action and less directed information-seeking action. High-risk infants have also been found to have less organized action and attentional strategies in exploratory manipulation of objects (Ruff, 1986; Ruff

et al., 1984). It is not clear whether this disorganization is a purely motor phenomenon or relates to the ability to perceive environmental affordances and act on them.

M ENTAL RETARDATION Research conducted with individuals with mental retardation provides insight into the relationship between haptic perception and cognitive ability. Much of the research examining the relationship among cognitive abilities and haptic manipulation and motor skill has been done with children with Down syndrome (e.g., Brandt, 1996; Moss & Hogg, 1981). These studies generally reported that children with Down syndrome did not show as effective accommodation of their hands to objects after grasp and did not use haptic manipulation and exploratory strategies as readily as typical children. However, it is difficult to directly attribute these results to the child’s cognitive abilities because many of these findings can be attributed to the sensorimotor problems or other aspects of Down syndrome (Exner, 1991). For example, Brandt and Rosen (1995) found that children with Down syndrome demonstrated impaired peripheral somatosensory function (sensory nerve conduction velocities) and suggested that this may contribute to poor tactual perceptual performance. It is likely that, regardless of the cause of the delay, impairment in the ability to efficiently explore objects interferes with learning about key object properties (Exner, 1991). Jones and Robinson (1973) compared the performance of a group of children with mental retardation (mean IQ = 47) to an age-matched group of children with normal intelligence. Accuracy of intramodal (haptic-haptic) and intermodal (hapticvisual) discrimination of meaningless shapes was poorer for the children with mental retardation than for the children with average intelligence. However, other studies found that when children with mental retardation and typical children were matched for mental age, the between-group difference in accuracy of haptic recognition disappeared (Derevensky, 1976, cited in Derevensky, 1979; Jones & Robinson, 1973; Medinnus & Johnson, 1966). In fact, two studies identified subjects with mental retardation as performing better than normal mental age-matched controls in intramodal (haptic-haptic) and intermodal (haptic-visual) matching tasks (Hermelin & O’Connor, 1961; Mackay & Macmillan, 1968). Because matching subjects for mental age eliminated differences in haptic accuracy scores between children with mental retardation and typical children, it can be concluded that some aspects of higher cognitive processing are most likely necessary for task completion. In addition to verbal intelligence, haptic strategies have

Perceptual Functions of the Hand • 81 been found to affect test performance of individuals with mental retardation. Subjects with mental retardation have been known to display immature manipulation strategies during tests of haptic perception. The sophistication of haptic manipulation strategies has been shown to be closely related to cognitive ability because manipulation strategies tended not to differ between typical children and children with mental retardation when subjects were matched for mental age (Davidson, 1985; Davidson, Pine, & WilesKettenmann, 1980). An increase in sophistication of manipulation strategies has been shown to occur in close association with an increase in mental age within the population with mental retardation (Davidson et al., 1980). Evidence from research on children with mental retardation who were blind and sighted and age-matched controls suggests that experience may contribute to improved manipulation and thus accuracy of intramodal (haptic-haptic) matching in individuals with mental retardation, but experience alone cannot fully compensate for the effects of reduced cognitive ability (Davidson, Appelle, & Pezzmenti, 1981). These findings suggest that training can help improve the sophistication of manipulation strategies in individuals with mental retardation, but such improvement in hand function may be only partially effective in improving performance on tests of haptic perception.

BRAIN I NJURY Impairments in tactile perception frequently have been reported in children with a diagnosis such as cerebral palsy that indicates a known brain injury (Bolanos et al., 1989; Boll & Reitan, 1972; Cooper et al., 1995; Duque et al., 2003; Krumlinde-Sundholm & Eliasson, 2002; Reitan, 1971; Solomons, 1957; Tachdjian & Minear, 1958; Van Heest, House, & Putnam, 1993; Yekutiel, Jariwala, & Stretch, 1994) and with traumatic brain injury (Ayres, 1989). Stereognosis (haptic identification of shapes or common objects) is often cited among the tactile functions showing impairment. Intermodal (visual-haptic) matching of shapes also has been shown to be impaired in children with brain injury (Birch & Lefford, 1964). Solomons (1957) found that children with brain injury were also impaired in the haptic discrimination of size and texture, although they did not differ from typical children in their ability to haptically match objects by weight. Although Boll and Reitan (1972) cited no problems in haptic shape recognition, they noted that the children with brain injury performed poorly on a complex tactile performance task that required shape recognition for task completion. Rudel and Teuber (1971) compared the ability of typical children and children with brain injury to discriminate three-

dimensional shapes through the use of intramodal (haptic and visual) and intermodal (visual-haptic) matching. Reduced performance in the group with brain injury was seen only in the visual-visual and visual-haptic matching conditions. These authors noted that, unlike the typical controls, who tended to perform better on the test conditions that included the use of vision than on the one requiring solely the use of touch, the addition of visual cues did not seem to assist the subjects with brain injury to improve their test performance. This finding suggests that children with brain injury may have a problem in visual perception or visual-haptic integration. However, this conclusion should be interpreted with caution because the mental ages of the subjects in the group with brain injury were 11⁄2 to 2 years above that of the control group. It is possible that, if the subjects were more equally matched for mental age, greater impairment in haptic perception might have been found within the group with brain injury. The studies reviewed frequently used children with a mixture of diagnoses (e.g., cerebral palsy, encephalitis, traumatic head injury). Thus it was not surprising to find research that cited deficits in manual dexterity (e.g., finger tapping, grip strength, motor coordination) along with dysfunction in tactile perception in the children with brain injury (Boll & Reitan, 1972; Reitan, 1971). Solomons (1957) compared the ability of children with brain injury with and without fine motor impairment to perform tests of haptic perception. The children with brain injury with intact hand function were able to more accurately match objects by shape, texture, and size than the children with brain injury with fine motor impairment. Studies also have reported that deficits in tactile perception (including stereognosis) have been closely associated with poor hand function in children with cerebral palsy (Duque et al., 2003; Gordon & Duff, 1999; Tachdjian & Minear, 1958). In addition, stereognosis has been identified as a good predictor of upper-extremity surgical outcome within the population with cerebral palsy (Goldner & Ferlic, 1966).

LEARNING DISABILITIES AND RELATED DISORDERS Impairment in tactile perception also has been cited in children who display learning disabilities and related disorders, conditions in which clearly identifiable brain damage has not been found. Poor tactile and kinesthetic perception has been found in children with learning disabilities, language disorders, dyspraxia, autism, and developmental Gerstmann syndrome (Ayres, 1965, 1989; Harnadek & Rourke, 1994; Haron & Henderson, 1985; Johnson et al., 1981; Kinnealey, 1989; Kinsbourne & Warrington, 1963; Lord &

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Hulme, 1987; Spellacy & Barbara, 1978; Nyden et al., 2004), with stereognosis among the tactile tests used in some of these studies. Impairment in motor coordination often has been found to accompany poor tactile perception in children with learning disabilities and related disorders. Johnson and co-workers (1981) found children with language disorders performed more poorly than a group of typical children matched for age, IQ, and socioeconomic status on tests of tactile perception (simultagnosia, graphesthesia, and finger identification) and motor coordination (hopping, finger opposition, diadochokinesis, and putting coins in a box). Reports of children with developmental Gerstmann syndrome have commonly cited a pairing of impairment in finger identification and constructional praxis (including poor handwriting and difficulty drawing geometric shapes) (Benton & Geschwind, 1970; Kinsbourne & Warrington, 1963; PeBenito, 1987; Spellacy & Barbara, 1978). CaseSmith (1995) studied 30 preschool children with perceptual-motor problems and found that stereognosis (Manual Form Perception test of SIPT) correlated with Motor Accuracy, a test of fine-motor skill (r = 0.43). Several other authors also have linked deficits in somatosensory processing (including poor haptic perception) to problems in motor planning (praxis) (Ayres, 1965, 1969, 1971, 1972, 1977, 1989; Ayres, Mailloux, & Wendler, 1987; Gubbay, 1975; Hulme et al., 1982; Reeves & Cermak, 2002; Walton, Ellis, & Court, 1962). However, it is not clear whether impaired haptic perception contributes to poor motor planning, poor motor planning contributes to difficulty in haptic perception, or there is an ongoing interaction. There has been little research specifically designed to identify factors that may be contributing to impaired haptic perception in children.

SUMMARY AND I MPLICATIONS FOR PRACTICE The previous section provides evidence of the existence of problems in haptic perception in children born prematurely and those with a variety of disorders associated with brain injury and learning disabilities. Like much of the literature on haptic perception in children previously discussed, most of the research on haptic perception in children with disorders has been limited to the study of haptic discrimination of shape. The presence of problems in haptic discrimination of shapes does not mean that a child also has equal impairment in haptic discrimination of objects containing other sensory properties (e.g., texture and weight). Thus we cannot assume that because a child has problems discriminating shapes he or she has global impairment in haptic perception. Future research on children with disabilities needs to be directed toward the analysis of

haptic recognition of objects having a variety of sensory properties. Factors contributing to test performance (e.g., in-hand manipulation and attention) also should be addressed if we are to gain the information needed for effective intervention. It was interesting to note that the reduced sophistication of manual and in-hand manipulation strategies, seen with impairments in visual perception and visual-haptic integration were cited as possible contributing factors to poor haptic perception in all the conditions reviewed. Although reduced cognitive ability was considered only in children with mental retardation, attention deficits or related cognitive processing problems were cited as possible contributing factors to impairment in other populations.

SUMMARY Haptic perception in infants and children has been reviewed in depth in this chapter. It was the authors’ intent to provide an overview of the literature on the topic, with emphasis on material relevant to the evaluation and treatment of disorders in haptic perception in children with suspected and identified CNS dysfunction. The literature reviewed provides insight into the development of haptic perception and the identification of factors that may be contributing to impairment in haptic perception in some children. Haptic perception emerges in early infancy and continues to mature into adolescence. The infant initially uses oral exploration to learn about objects. The hands first transport objects to the mouth and later become a primary tool for haptic object exploration. Manual manipulation of objects begins with grasping and is later replaced by more specific manipulation patterns (e.g., fingering, banging) that are tailored to the physical properties of the object. Manual manipulation gradually replaces mouthing as the preferred method of object exploration. This is followed by a long period of development in which the accuracy of haptic object recognition improves and the complexity of manual manipulation and exploratory strategies increases. The accuracy of haptic object recognition is related to the choice of haptic manual manipulation and exploratory strategies. Vision appears to guide the development of manual manipulation and helps to bring meaning to the haptic information being retrieved by the hands. It is not until 6 years of age that children can easily explore objects with the hands without the assistance of vision. With time the hands develop the ability to retrieve information from the environment without the aid of vision, making it possible for vision and haptic sensory processing to take

Perceptual Functions of the Hand • 83 on separate supportive roles in daily function; however, visual imagery continues to be used by many people to aid in haptic object recognition. Research suggests that the ability to use cognitive strategies such as visual imagery and verbalization in the cognitive processing of haptic information develops with age. It appears to be related to intelligence, because there is an association between mental age and the accuracy of haptic object recognition. Review of the literature on haptic perception in children with disorders suggests that impairment in somatosensory processing, manual and in-hand manipulation, vision, visual perception, or cognition can contribute to deficits in haptic perception. Most of the tests currently used to assess haptic perception measure the product, the number of objects identified correctly. Yet process might be as important as, or even more important than, product when using the results of testing to guide treatment. Assessing the process means considering the quality of manual manipulation and exploratory strategies, along with the degree to which vision and cognitive strategies are being used in task performance. Therapists should be aware that the tests available to measure haptic perception in children assess only a segment of this function. Because a child shows impairment in shape recognition on a test of stereognosis does not mean that the same child will display problems in haptic discrimination of other sensory properties (e.g., weight, texture). We should consider developing tests of haptic perception that assess the breadth of haptic sensory properties found in objects. We also should develop tests that measure the process, as well as the product of task performance. We should test haptic discrimination of several sensory properties to determine the extent of dysfunction, and we should analyze the process of task performance to determine the reason for low test scores. We also should develop treatment strategies that will translate into improvement in the use of haptic perception in daily function.

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Chapter

5

REACHING AND EYE-HAND COORDINATION Birgit Rösblad

CHAPTER OUTLINE MATURE REACHING MOVEMENTS Movement Speed Transport and Grasp Phase Role of Vision Role of Proprioception Integration of Sensory Information

around the ball before the moment of contact, or we will fail to catch it. In other types of goal-directed arm movements the arm trajectory as such can be the goal, as when painting or drawing, but in a reaching movement the goal is to transport the hand to the target, with precision in both time and space. This chapter is organized in three parts: the first deals with the mature reaching movement, the second with the development of reaching in infancy, and the third with reaching in children with motor disabilities.

DEVELOPMENT OF REACHING DURING INFANCY Beginning to Master the Reach Coordinating the Body Parts Involved in the Reaching Movement

MATURE REACHING MOVEMENTS

Movement Planning

Reaching for an object means getting the hand from a starting position to the goal, the object. In doing this, the hand describes a trajectory. The word trajectory can be used in different ways, but here refers to the path taken by the hand as it moves toward a target and the speed as it moves along the path. The reaching trajectory has several characteristics that are discussed later.

Role of Sensory Information Movement-to-Movement Variability REACHING IN CHILDREN WITH MOTOR IMPAIRMENTS Movement Planning Feedback Control of Reaching Movements Adaptation of Reaching Movements The Movements of the Arms Are Coupled in Children with Hemiplegic Cerebral Palsy Our hands are extremely important tools for us in our everyday lives, and we are able to use them with grace and skill. To do so we have to be able to bring them to the right place at the right time. This can be illustrated with the example of catching a ball. To catch the ball successfully the hand has to be at the calculated meeting point at exactly the right time. Moreover, it must be prepared for the catch, with the fingers closing

MOVEMENT SPEED If the velocity of the hand during a reaching movement is plotted versus time as in Figure 5-1, one can see that the tangential velocity curve is bell shaped. The reaching movement is continuous with one single peak of velocity. In the last part of the reaching movement, when the hand is close to the target, the velocity is slow. This typical bell-shaped velocity curve is seen when the reach is carried on with, as well as without, visual feedback (Jeannerod, 1984; Morosso, 1981). This indicates that the reaching movement is programmed in advance of movement onset to a high degree.

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cm/s2

cm/s

1500

750

70 0

–750 0 0

200

400

600

ms Figure 5-1 Kinematic profiles of the transport component of a reaching movement. The heavy line depicts the velocity of the wrist (cm) as a function of time. This curve describes a single continuous movement with a single peak of velocity. The two peaks connected by the thin line depict the acceleration of the wrist (cm2) as a function of time. The positive peak constitutes one phase of acceleration and the negative peak one phase of deceleration, together forming one movement unit. (From Jeannerod M, et al. [1992]. Parallel visuomotor processing in human prehension movements. In R Caminiti, PB Johnson, Y Burnod [editors]: Control of arm movement in space. New York, Springer-Verlag.)

If one considers the reaching movement in terms of accelerations and decelerations, it can be divided into movement units. One phase of acceleration followed by a deceleration then can be said to constitute a movement unit (Brooks, 1976; von Hofsten, 1979). The movement paths within these movement units are relatively straight, and movement direction is changed in between units (von Hofsten, 1991). The number of movement units comprising a movement can be viewed as an index of its degree of programming. A movement consisting of only one movement unit, such as that depicted in Figure 5-1, then can be viewed as being entirely programmed before movement onset. However, if the movement is composed of many movement units, one can assume that it has been programmed several times during execution. A reaching movement, aimed at a stationary object, generally consists of one or two movement units, with the first covering the main part of movement duration. The choice of movement speed is crucial for how skillfully we manage to reach and grasp an object. A movement cannot be both fast and precise. Unconsciously we strive to optimize movement speed to suit

the activities we perform. When we reach out to pick a blueberry, movement speed is lower compared with that used in reaching for a ball we intend to throw. The decrease of accuracy when speed increases has been called the “speed-accuracy trade-off ” and is defined by Fitts’ law (1954). The minimum variance theory, put forward by Harris and Wolpert (1998), might explain this phenomenon. They argue that neuronal signals are corrupted by “noise” that increases with the size of the control signal. Therefore increased acceleration leads to increased variability in the final limb position and thus requires further corrective movements. This means that moving very fast can be counterproductive.

TRANSPORT AND G RASP PHASE Another way of viewing the reaching movement is to look for its functional components. Two distinct and coordinated movement components then can be identified (Jeannerod, 1984). The first component is a transportation phase, which brings the hand to the target. In this part of the movement mainly the proximal joints and muscles are involved. The second component is a grasp phase in which the hand is shaped in anticipation of contact with the object. This phase involves mainly the distal joints and muscles. One also can divide the visual information needed to successfully grasp an object into two categories. For the transport phase of the movement knowledge of the position of the object in the room is needed (the object’s extrinsic properties). With this information we can program the direction and extent of the movement. For the grasp phase, perception of the size and shape of the object is needed (the object’s intrinsic properties). There is evidence for independent planning of the two reaching phases (Loukopoulos, Engelbrecht, & Berthier, 2001). Although the grasp and transportation phase of the reach are separately controlled, these two components are coordinated so that the grasp phase starts during the transportation phase. To accomplish a smooth and coordinated grasp, the fingers must initiate the grasp well before encountering the object. Closing the hand too early or too late prevents capturing or makes the grasp impossible or awkward. During the transportation phase the fingers open to a maximum grip aperture. After this maximum opening the fingers start to close in anticipation of contact with the object (Jeannerod, 1981). The control strategy used by the central nervous system to coordinate these components remains largely unknown. However, it has been suggested recently that a simple spatial relation, based on the size of finger opening in relation to finger closing, might determine at what point during the reach the maximum grip aperture will occur (Mon-Williams & Tresilan, 2001).

Reaching and Eye-Hand Coordination • 91 The action we perform shapes our reaching or grasping movement. A small object requires longer reaching time than a larger object. The first part of the movement trajectory seems to be unaffected by object size, but for smaller objects extra movement time is spent in the last part of the movement, after peak acceleration. Moreover, the greater the precision required, the earlier the hand will anticipate the physical characteristics of the object (Marteniuk, MacKenzie, & Athenes, 1990). The hand opens more fully during the reach when reaching for a larger object, and always more than necessary (von Hofsten & Rönnquist, 1988). If the reach has to be carried out with high speed, the grip aperture is larger. Opening the hand more fully during a fast reach could be seen as a way of making sure that the object is successfully grasped despite the decreased movement accuracy (Wing, Turton, & Fraser, 1986).

ROLE OF VISION It is obvious that vision plays a very important role in our ability to reach out for objects. One need only imagine what it would be like to be blind to realize the importance of vision to reaching. Vision is the sense that provides us with information about the layout of the environment, and when reaching for an object, vision defines both the position and shape of the object. Seeing the environment gives us an opportunity to anticipate upcoming events and plan our movements in an anticipatory fashion. One example of this is the way we shape our hand before contact with an object. A blind person reaching for an object does not have this ability but has to touch the object first and then, guided by haptic information, shape the hand for grasp. If we cannot foresee upcoming events and plan our movements ahead of time, our movements will be uncoordinated of necessity. Given that visual information is important both for movement planning and execution, one may ask what should be seen and when during the movement we need that information. The answer to this seems to be that full visual information is optimal. Several studies show that we must be able to see the target both before and during a movement or movement quality is reduced (Berthier et al., 1996; Sarlegna et al., 2003). Moreover, if we can see our hand as we move it toward the target, movement accuracy and efficiency will be improved (Connolly & Goodale, 1999; Sarlegna et al., 2004; Saunders & Knill, 2003; Schenk, Mair, & Zihl, 2004). The minimum delay needed for visual information to affect the physical movement of the hand traditionally has been thought to be around 200 msec (Keele & Posner, 1968). Because many naturally occurring reaching movements take around 500 msec to com-

plete, the assumption has been that only low-velocity movements can be influenced by visual feedback. However, there is now considerable evidence that visual feedback might be as fast as 160 to l00 msec, and that we use online visual information to correct both slow and fast movements (Alstermark et al., 1990; Martin & Prablanc, 1992; Paulignan et al., 1991a,b; Saunders & Knill, 2003). Nevertheless, even if the movement is carried out without visual feedback, the main features of the reaching trajectory remain. One will still see the bellshaped velocity curve, as well as the coordination between movement speed and anticipatory hand shaping (Jeannerod, 1981). This indicates that to a high degree the reaching movement is programmed in advance of movement onset but can be modified during execution when necessary—that is, when endpoint accuracy is needed or if we reach for a target that moves in an unpredictable way.

ROLE OF PROPRIOCEPTION We have receptors in our muscles, tendons, joints, and skin that provide us with information about the positions and movements of our body parts. This is here termed proprioception, after Sherrington (1906). Although it is relatively easy to find out how we can move without vision or with degraded vision, proprioceptive information cannot be manipulated as easily. Instead, the research on the role of proprioception has focused on animal experiments and patients with sensory loss caused by diseases. One line of research has used deafferented monkeys. When their dorsal spinal roots are sectioned, the monkeys are deprived of sensation from the upper limbs but the motor nerves are unaffected. This technique was used in early experiments by Mott and Sherrington (1895). They reported that the monkeys’ limbs became useless after such operations and that the animals used their upper limbs only if forced to and then in an awkward way. They concluded that afferent information from the limbs was necessary for both movement initiation and control. Similar results also were reported by Lassek & Moyer (1953). However, later experiments with deafferented monkeys reported different results. Taub and Berman (1968) reported a clear improvement in motor function after the initial disability that resulted from the section of the nerves. The animals were able to reach for and grasp objects with a primitive pincer grip a few months after surgery. Recovery of function also has been reported by Knapp and co-workers (1963). Bossom and Ommaya (1968) have pointed out that motor pathways can be damaged easily during a rhizotomy and that this could be why the degree of recovery of function varied between studies.

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Despite the previous diversity in results, there are also similarities. Several investigators have found that, when forced to, the animals are able to use their deafferented limb. Animals that had both forelimbs deafferented regained function to a higher degree than those with only one deafferented forelimb, who could choose to use the normal hand. This latter effect has been called learned nonuse by Taub and Berman (1968) and was explained in terms of an inhibition of the deafferented limb. However, if the animals that had one limb deafferented were forced to use it because the normal limb was restrained, they recovered function to the same degree as the bilaterally deafferented animals (Bossom, 1974; Knapp et al., 1963). Yet another similarity among the reports is that the deafferented monkeys were capable of both initiating and carrying out motor acts, however uncoordinated. Studies of humans with sensory deficits seem to confirm this. Gordon and Ghez (1992) described patients with large-fiber sensory neuropathy in the following way: “These patients, although able to initiate and carry out complex movement sequences, were severely impaired in most functional activities. For example, none could drink water from a cup without spilling.”

The experiments by Ghez and co-workers (1990) provide us with important information about the role of proprioception in reaching movements. They studied the reaching movement in patients with sensory loss caused by large-fiber neuropathy. Without visual feedback the patients made large directional errors from movement onset and also were unstable at movement endpoint. When allowed to monitor the movement visually, they were able to substitute for the loss of proprioceptive information to some degree, and performance improved. However, Ghez and coworkers (1990) also studied the effect on movement accuracy when the patients were able to look at the limb before movement onset but not during the ongoing movement and found that this also improved function. This indicates that proprioception is not only important for feedback during the ongoing movement but also plays an important role for programming of movements by providing the nervous system with information about the current state of the body parts.

I NTEGRATION OF SENSORY I NFORMATION When we reach for an object both vision and proprioception provide information about hand position, and this information must be integrated to generate one single estimate of where the hand is in space (van Beers, Wolphert, & Haggard, 2002). This means that

the visual and proprioceptive systems have to be in correspondence with each other. One example of when they are not integrated involves wearing a pair of displacing prisms. If we then reach for an object, we perceive the object at a location displaced from its virtual position, and the reach is directed to this erroneous position. However, reaching actively toward the object several times rapidly reintegrates the visual and proprioceptive systems, and within a few minutes adaptation has occurred (Harris, 1965). This also can be experienced when one puts on a pair of new glasses. The distance to the ground seems to be changed, and it takes some minutes of walking before the visual system again is in agreement with the proprioceptive system. A recent study by van Beers and co-workers (2002) suggests that the extent to which vision and proprioception contribute to the control of reaching movements depends on the task. The brain weighs the information from each modality in a way that minimizes the uncertainty in perceived position. This suggests that we cannot say that one modality dominates the other and that the situation is better described as a flexible weighing of information from the modalities to obtain movement precision.

DEVELOPMENT OF REACHING DURING INFANCY BEGINNING TO MASTER THE REACH Observing a newborn baby’s arm movements, one might perceive them as random, performed without meaning. However, even at birth the infant is capable of movements that require some degree of sensory motor integration. Von Hofsten (1982) placed 5-day-old infants in a semireclining seat that gave good support to the trunk and head but allowed free movement of the arms. The infants were presented with a colorful tuft that moved irregularly and slowly in front of them. The infants’ arm movements were recorded with two video cameras, making it possible to calculate the arm trajectory in three-dimensional space. All infants noticed the tuft and were able to follow it with eye and head movements for varying periods. The infants’ forward extended arm movements, as well as looking behavior, were analyzed. When the infants were fixating the tuft, they aimed their reaching movements closer to it than when looking in another direction or closing their eyes. Thus a child only a few days old already has a rudimentary visual control of arm movements. Moreover, when initiating an aimed movement toward a visually fixated target, the infant must “know” where its arm is.

Reaching and Eye-Hand Coordination • 93 Because the neonate is fixating the target, the starting position of the hand must be defined proprioceptively. This indicates that the visual and proprioceptive spaces are to some degree already connected in the newborn infant. However, even though the infants aimed their reaching movements closer to the object while fixating on it, most of the time they did not touch it. Also, at this early age, even if they did touch the object, they were not capable of grasping it. Several months of experience of its the own body and with the environment still remain before the infant starts to become successful at reaching, at around 4 to 5 months of age (Gesell & Ames, 1947).

COORDINATING THE BODY PARTS I NVOLVED IN THE REACHING MOVEMENT Before the infant can reach for and grasp an object he or she must learn to coordinate the movements of the shoulder, arm, and hand. This complicated task of controlling movements over several joints, and accordingly a great number of movement possibilities, has been designated as the degrees of freedom problem (Bernstein, 1967). One solution to this problem is to reduce the degrees of freedom by keeping some of the involved joints in a stiff position. This also seems to be the strategy used by infants as they first start to reach for objects. Berthier and colleagues (1999) found that beginning reachers mainly use shoulder and torso rotation to move the hand to the target, while the elbow is kept in a stiff position. This reduces the complexity of the movement and thus increases the infant’s chances of successfully capturing the object. However, an obvious limitation of this strategy is that it restricts the infant’s possibility of placing the hand in an optimal position for grasping. Postural stability is yet another foundation for reaching movements. Van der Fits and colleagues (1999), who studied postural adjustments during arm movements in infants, found that when infants first start to reach successfully for objects the arm movements are accompanied by a large amount of postural activity. Already at this young age the pattern of activation showed some resemblance to that seen in adults, with an activation of the dorsal muscles before the ventral and a top-down recruitment of muscles. With increasing age the pattern of activation became more organized. Yet another study demonstrating the linkage between the development of posture and reaching was carried out by Rochat (1992). When the infants started to reach for objects, they tended to use both hands and later in development acquired one-handed reach. A successful object-oriented reach in a young infant is symmetric and synergistic with the hands meeting in

midline. Older infants often display an asymmetric onehand reach. He reported that when infants first attained the ability to sit without support they shifted toward reaching more with one hand so that the other could be used to maintain balance. Hopkins and Rönnqvist (2002) studied reaching behavior in infants aged about 6 months who were not yet able to sit without support. They compared the quality of the reaching movements when the infants were provided with firm postural support and when they were sitting in a commercially available chair. That the firm postural support resulted in a decrease in the number of movement units indicates that this extra support improved the reaching behavior. Clinical observations made by Grenier (1981) also indicate that postural control is important for coordinated arm movements and that if infants are supported appropriately at the neck and trunk they can perform coordinated arm movements at a much earlier age than is typical. Postural control does not only act by maintaining balance after it has been perturbed. We also have the ability to anticipate an upcoming situation that will perturb our balance and prepare ourselves by means of postural adjustments. There is some evidence that this anticipatory mode of counteracting upcoming forces on the body starts to operate during the first year of life. Von Hofsten and Woollacott (1989) showed that at 10 months of age children activated the muscles of the trunk before making voluntary arm movements. The integration between posture and voluntary control is an important prerequisite for coordinated arm and hand movements. Little is known of how children with motor impairments can integrate voluntary movements and posture, but it is possible that this is one contributory factor in these children’s fine motor disturbances.

MOVEMENT PLANNING As discussed, the reaching movement can be analyzed in terms of acceleration and deceleration. A phase of acceleration followed by a phase of deceleration then constitutes a movement unit. When the infants first start to reach and grasp, at around 4 months of age, the ability to plan the movement ahead of time is still poor. As a consequence of this, the movement path is awkward and crooked, and the trajectory consists of many movement units. This changes after the infant has practiced reaching for some time, and at around 1 year of age the number of movement units has decreased and the movement paths are straighter (Konczak & Dichgans, 1997; von Hofsten, 1991) (Figure 5-2). The ability to plan movements ahead of time, and not only react to what has already happened, is fundamental for movement skill. One example when this is

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Figure 5-2 Sagittal hand paths of one infant at four different ages illustrating the progression toward smoother and straighter movements. (From Konczak J, Dichgans J (1997). The development toward stereotypic arm kinematics during reaching in the first 3 years of life. Experimental Brain Research, 117:346–354.)

obvious is when we catch a ball that is thrown to us. To be able to do this we must predict the trajectory of the moving object and reach for the meeting point. Von Hofsten and Lindhagen (1979) found that at the age children start to reach successfully for stationary objects, they also can catch fast-moving ones. Eighteenweek-old infants were found to be able to catch objects that moved at 30 cm/sec. Most of the reaches were aimed at the meeting point from movement onset. This demonstrates an early emerging capacity for anticipatory control of reaching movements. That is, the infant does not reach toward where he or she first sees the object, but rather appears to be anticipating the point where the hand and the object will meet (Figure 5-3). The ability for anticipatory control develops substantially during the first year of life. One example of this is how the infant prepares the hand for the grasp. An adult reaching for an object shapes the hand to fit the properties of the object in anticipation of contacting it. Von Hofsten and Rönnquist (1988) studied the shaping of grip aperture as infants reached for objects. The 5- to 6-month-old children started to close the hand before making contact with the object, which indicates some anticipatory ability. However, these young infants did not adjust their grip aperture to match the object size, as did children at 9 months of age. At 13 months of age the infants started to close the hand earlier during the reach compared with the younger children and were comparable to adults in this respect. Infants 10 months of age also have been found to shape their hand to fit different shapes of objects before contact (Pieraut-Le Bonniec, 1990).

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Figure 5-3 Two views of the performance of a wellaimed reach by an infant who is 21 weeks of age. The frame on the bottom is the start of the reach. The interval between frames is 0.2 sec (digital clock reading in the upper portion of each frame). The child is directing the reach ahead of the object to the point at which the object will be at the end of the reaching movement. (From von Hofsten C [1980]. Predictive reaching for moving objects by human infants. Journal of Experimental Child Psychology, 30:369–382.)

When we as adults reach for an object the movement trajectory is not only affected by the size and shape of the object but also by what we intend to do with it after we have picked it up. We reach more slowly for an object that will be used in a precision task (e.g., fitting a coin in a slot) than for an object that will be used in a nonprecision task (e.g., throwing the coin in a bucket). Claxton, Keen, and McCarty (2003) studied 10-month-old infants to see if they also had this ability to plan a reaching movement in several segments. The

Reaching and Eye-Hand Coordination • 95 infants were encouraged to reach for a ball and then either throw it into a tub or fit it into a tube. Infants, like adults, reached for the ball faster if they were going to throw it as opposed to fit it into the tube. This shows that infants have an ability to take several steps into account when planning an activity. However, they did not show the more sophisticated signs of movement planning that adults do, such as a prolonged deceleration phase when reaching for an object that will be used in a precision task.

discussed in the preceding section suggest that young infants are able to use proprioceptive information and integrate it with visual information when reaching for objects. A similar result was found when reaching was studied in children 6, 7, and 8 years of age, in a situation in which the amount of visual information was varied. The children seemed to use visual information for control of arm movements in a manner similar to that of adults, although with less accuracy and speed (Rösblad, 1998).

ROLE OF SENSORY I NFORMATION

MOVEMENT-TO-MOVEMENT VARIABILITY

As discussed, visual information of the hands as well as the goal is necessary for movement accuracy. However, to a great extent we are able to replace visual information with proprioceptive and tactual information if the hand for some reason is out of sight or if we reach in the dark. Clifton and colleagues (1994) have in a series of studies investigated the ability in infants to reach for objects in the dark They showed that 6- to 7-month-old infants could contact sounding objects (Perris & Clifton, 1988) and that infants of 6 months could successfully reach for glowing objects (Clifton et al., 1994) and also reach for glowing objects that were moving in the dark (Robin, Berthier, & Clifton, 1996). For many years it has been assumed that young infants are more dependent on visual information for control of reaching movements than adults, and that their ability to use proprioceptive information for movement control is poor (Piaget, 1952). However, the studies

The infant has not yet learned the most efficient way of performing a movement and is still exploring the possibilities of its own body. Therefore he or she will perform a specific task, such as reaching for a toy, with significant movement-to-movement variability. In fact, being able to perform a specific task in a consistent manner is a prominent feature of movement skill. Figure 5-4, A shows the superimposed movement trajectories of a 1-year-old girl reaching for an object. In Figure 5-4, B the same task is performed by an 11year-old boy. Although the little girl grasps the object without difficulty, it is clear that she does not reach for the object with the same skill as the older boy does. Lhuisset and Proteau (2004), who studied reaching movements in children 6, 8, and 10 years old, found that although the children clearly planned the movements ahead of time, the planning processes were still more variable than for adults.

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Figure 5-4 The figures show that a young child performs a specific movement with high variability, whereas an older child has a more consistent movement pattern. A, Trajectory of the hand for a 12-month-old girl who is reaching repeatedly for the same object. B, How an 11-year-old boy performs the same movement. (From Eliasson AC, Rösblad B [2001]. Arm och handrörelser: Normal och avvikande utveckling. In E Beckung, E Brogren, B Rösblad [editors]: Sjukgymnastik för barn och ungdom. Teori och tillämpning. Lund, Studentlitteratur.)

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REACHING IN CHILDREN WITH MOTOR IMPAIRMENTS We still have limited knowledge concerning the ability to plan and control reaching movements in children with motor impairments. However, the knowledge we have from research carried out on normally developed children and adults can be used when asking questions about children with motor impairments. This section provides examples from this line of research.

MOVEMENT PLANNING A common finding in motor control research on children with motor impairments is that the ability for movement planning is impaired. One example of how the ability to plan reaching movements can be impaired comes from a study on reaching in children with attention deficit hyperactivity disorder (ADHD) (Eliasson, Rösblad, & Forssberg, 2004). To analyze the kinematics of the arm movement we used a digitizing tablet. The task for the children was to move a cursor on a computer screen with a hand-held digitizer on the tablet. Start and target positions on the screen were always visible during the movement. The screen cursor, however, could either be visible throughout the entire movement or blanked at movement initiation. Analysis showed that movement control was impaired in children with ADHD and that their problems were especially pronounced when the screen cursor was not visible on the screen. Because the children could not visually correct the movement when the screen cursor was blanked, results indicate a poorer motor programming in children with ADHD. Moreover, the children with ADHD performed jerky movements with higher peak accelerations than the control group of children. As discussed earlier in this chapter, the choice of movement speed is crucial for how skillfully we manage to reach for and grasp an object. The children with ADHD adopted higher movement speed compared with the typically developed children but this high speed was counterproductive and resulted in increased movement endpoint errors and further corrective movements. Similar results also have been found when the control of reaching movements in children with developmental coordination disorder (DCD) has been studied. Van der Meulen and colleagues (1991a,b) tested the ability in children with DCD to make precise arm movements. In a first study, the task for the child was to reach for a target as quickly and precisely as possible. In a second study, the ability to track a target that moved unpredictably was assessed. In both studies, the children were tested in situations in which they did or

did not receive visual feedback of the moving arm. Movement analysis indicated that the less efficient movements of the children with DCD could be explained by a less developed ability for anticipatory control.

FEEDBACK CONTROL OF REACHING MOVEMENTS Although it is a common finding that children with motor impairments show signs of impaired ability for movement planning, there are several exceptions to this. We studied the ability of children and young adults with myelomeningocele (MMC) to control reaching movements (Norrlin, Dahl, & Rösblad, 2004). As in the study on children with ADHD discussed in the preceding section, we used a digitizing tablet linked to a computer. Results showed that the ability to program reaching movements was similar in individuals with MMC and a control group of children. In both groups the velocity profiles were bell-shaped and also scaled proportionally to target distances, indicating efficient movement planning. The movement problems in the MMC group seemed to be related to the execution of the ongoing movement. The subjects with MMC showed more problems when they were provided with visual feedback during the entire movement, and thus being given the opportunity to make visual corrections of the trajectory. This suggests that the commonly occurring visual perceptual problems in individuals with MMC may contribute to their poor spatial movement precision. Kearney and Gentile (2002) performed a small but interesting study, on prehension in young children with Down syndrome. They compared the performance of 3-year-old children with Down syndrome (only three children were included) with 2- and 3-year-old typically developed children. The children with Down syndrome scaled the peak velocity to movement distance, which indicates ability for movement planning. However, they differed from both groups of typically developed children in that they performed the final part of the reaching movement with reduced efficacy, which indicates that these children mainly have problems with feedback control of the reaching movement.

ADAPTATION OF REACHING MOVEMENTS Our sensory motor system is highly adaptable. When we use a computer mouse we get used to the specific gain of that mouse and take this into account when we program the movements of hand that will transfer the mouse. If the gain of the mouse is changed we will under- or overshoot the target on the computer screen, but only a few times. The nervous system modifies the

Reaching and Eye-Hand Coordination • 97 programming of subsequent movements to prevent errors and motor adaptation occurs rapidly. Motor adaptation involves changes in the control of movements and can be seen as short-term learning. In everyday life we rapidly and frequently adapt our movements to changing conditions, such as when we switch to new cars with different transmission in the steering system or simply when we switch to a light hammer after having used a heavy one. Again, using the described experimental setup with a digitizing tablet linked to a computer, we investigated the ability in subjects with MMC to adapt reaching movements to a new visuomotor gain (Norrlin & Rösblad, 2004). This was done by first letting the subjects perform reaching movements at targets displayed on a computer screen. After having performed a number of trials (around 100) we changed the gain of the mouse. Directly after this gain change both the children or youths with MMC and the typically developed children overshot the target. However, within a few trials the control group of children had adapted to the new condition and performed movements of the same accuracy as before the change. However, the subjects with MMC needed considerably more time for short-term learning to occur and they had still not fully adapted after 30 trials with the new gain. However, when an unexpected gain change back to the initial condition was introduced after these 30 trials, both groups undershot the target. This indicates that some adaptation had occurred also in the children with MMC. More knowledge about the capacity for motor learning in children with motor impairments, as well as knowledge about the best conditions for learning, would be of great value when planning interventions.

THE MOVEMENTS OF THE ARMS ARE COUPLED IN C HILDREN WITH H EMIPLEGIC C EREBRAL PALSY A specific problem faced by children with hemiplegic cerebral palsy is that the movements of the arms and hands often are coupled. If the child is engaged in manual activities with one hand mirror movements frequently can be observed in the other hand. Typically, reaching movements in children with hemiplegia are performed with lower velocity in the impaired arm than in the unimpaired arm (Van Thiel & Steenbergen, 2001; Volman, Wijnroks, & Vermeer, 2002a,b). However, symmetric movements of the arms tend to improve the movement quality of the impaired hand, measured as speed and smoothness, but restrict the movements of the unimpaired hand, which adapts to the impaired one and accordingly moves more slowly (Utley & Sugden, 1998; Van Thiel & Steenbergen,

2001; Volman et al., 2002a). If the arms and hands are to make asymmetric movements, the movement control problems are amplified. A commonly occurring situation is that we reach out for and grasp an object with one hand while the other hand is occupied with holding another object. The effect that the mirror movements may have on the quality of reaching movement is yet to be investigated. When discussing results from studies of children with motor impairments, we point out that the variation within one specific diagnostic group is large. The movement problems within one diagnostic group could not be explained by one specific factor; however, the knowledge obtained from studies carried out on both normally developed children and children with motor impairments can provide us with knowledge about which processes might be disturbed and what to look for when assessing children.

REFERENCES Alstermark B, Gorska T, Lundberg A, Petterson L-O (1990). Integration in descending motor pathways controlling the forelimb in the cat. 16. Visually guided switching of target-reaching. Experimental Brain Research, 80:1–11. Bernstein N (1967). The coordination and regulation of movement. London, Pergamon Press. Berthier NE, Clifton RK, Gullapalli V, McCall DD, Robin D (1996). Visual information and object size in the control of reaching. Journal of Motor Behavior, 28:187–197. Berthier NE, Clifton RK, McCall DD, Robin DJ (1999). Proximo distale structure of early reaching in human infants. Experimental Brain Research, 127:259–269. Bossom I (1974). Movement without proprioception. Brain Research, 45:285–296. Bossom I, Ommaya AK (1968). Visuomotor adaptation to prismatic transformation of the retinal image in monkeys with bilateral dorsal rhizotomy. Brain, 91:161–172. Brooks VB (1976). Some examples of programmed limb movements. Brain Research, 71:38–47. Claxton LJ, Keen R, McCarty ME (2003). Evidence of motor planning in infant reaching behavior. Psychological Science, 14:354–356. Clifton R, Rochat P, Robin DJ, Berthier NE (1994). Multimodal perception in the control of infant reaching. Journal of Experimental Psychology: Human Perception and Performance, 20:876–886. Connolly JD, Goodale MA (1999). The role of visual feedback of hand position in the control of manual prehension. Experimental Brain Research, 125:281–286. Eliasson A-C, Rosblad B, Forssberg H (2004). Disturbances in programming goal-directed arm movements in children with ADHD. Developmental Medicine in Child Neurology, 46:19–27. Fitts PM (1954). The information capacity of the human motor system in controlling the amplitude of movement. Journal of Experimental Psychology, 47:381–391. Gesell A, Ames LB (1947). The development of handedness. Journal of Genetic Psychology, 70:155–175.

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Ghez C, Gordon I, Ghilardi MF, Christakos CN, Cooper SE (1990). Roles of proprioceptive input in the programming of arm trajectories. Cold Spring Harbor Symposia on Quantitative Biology, 55:837–847. Gordon I, Ghez C (1992). Roles of proprioceptive input in control of reaching movement. In H Forsberg, H Hirschfeldt (editors): Movement disorders in children. Medicine and Sport Science. Basel, Karger. Grenier A (1981). “Motoricite libelree” par fixation manuelle de la nuque au cours de premieres semaines de la vie. Archives Francaises de Pediatrie, 38:557–561. Harris CH, Wolpert DM (1998). Signal-dependent noise determines motor planning. Nature, 394:780–784. Harris CS (1965). Perceptual adaptation to inverted, reversed and displaced vision. Psychological Review, 72:419–444. Hopkins B, Rönnqvist L (2002). Facilitating postural control: Effects on the reaching behavior of 6-month-old infants. Developmental Psychobiology, 40:168–182. Jeannerod M (1981). Intersegmental coordination during reaching at natural visual objects. In I Long, A Baddeley (editors): Attention and performance. IX. Hillsdale, NJ, LEA. Jeannerod M (1984). The timing of natural prehension movements. Journal of Motor Behavior, 16:235–254. Kearney K, Gentile AM (2002). Prehension in young children with Down syndrome. Acta Psychologica, 112:3–16. Keele SW, Posner MI (1968). Processing visual feedback in rapid movement. Journal of Experimental Psychology, 77:155–158. Knapp HD, Taub E, Berman AI (1963). Movements in monkeys with deafferentated forelimbs. Experimental Neurology, 7:303–315. Konczak J, Dichgans J (1997). The development toward stereotypic arm kinematics during reaching in the first 3 years of life. Experimental Brain Research, 117:346–354. Lassek AM, Moyer EK (1953). An ontogenetic study of motor deficits following dorsal brachial rhizotomy. Journal of Neurophysiology, 16:247–251. Lhuisset L, Proteau L (2004). Visual control of manual aiming movements in 6- to 10-year-old children and adults. Journal of Motor Behavior, 36:161–172. Loukopoulos LD, Engelbrecht SE, Berthier NE (2001). Planning of reach-and-grasp movements: Effects of validity and type of object information. Journal of Motor Behavior, 33:255–264. Marteniuk RG, MacKenzie CL, Athenes S (1990). Functional relationships between grasp and transport components in a prehension task. Human Movement Science, 9:149–176. Martin O, Prablanc C (1992). Online control of hand reaching at undetected target displacements. In GE Stelmach, I Requin (editors): Tutorials in motor behavior: II, Amsterdam, Elsevier. Mon-Williams M, Tresilan JR (2001). A simple rule of the thumb for elegant prehension. Current Biology, 11:1058–1061. Morosso P (1981). Spatial control of arm movements. Experimental Brain Research, 42:223–227. Mott FW, Sherrington CS (1895). Experiments upon the influence of sensory nerves upon movement and nutrition of the limbs. Proceedings of the Royal Society, B57:481–488. Norrlin S, Dahl M, Rösblad B (2004). Control of reaching movements in children and young adults with

myelomeningocele. Developmental Medicine and Child Neurology, 46:28–33. Norrlin S, Rösblad B (2004). Adaptation of reaching movements in children and young adults with myelomeningocele. Acta Paediatrica, 93:922–928. Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1991a). Selective perturbation of visual input during prehension movements. 1. The effect of changing object position. Experimental Brain Research, 83:502–512. Paulignan Y, Jeannerod M, MacKenzie C, Marteniuk R (1991b). Selective perturbation of visual input during prehension movements. 2. The effect of changing object size. Experimental Brain Research, 87:407–420. Perris EE, Clifton RK (1988). Reaching in the dark toward sound as a measure of auditory localization in infants. Infant Behavior and Development, 11:473–491. Piaget J (1936/1952). The origins of intelligence in children. New York, Norton. Pieraut-Le Bonniec G (1990). Reaching and hand adjusting to target properties. In H Hloch, HI Hertenthal (editors): Sensory-motor organization and development in infancy and early childhood. Netherlands, Kluwer. Robin DJ, Berthier NE, Clifton RK (1996). Infants’ predictive reaching in the dark. Developmental Psychology, 824:835. Rochat P (1992). Self-sitting and reaching in 5- to 8month-old infants: The impact of posture and its development on eye-hand coordination. Journal of Motor Behavior, 24:210–220. Rösblad B (1998). Roles of visual information for control of reaching movements in children. Journal of Motor Behavior, 29:174–182. Sarlegna F, Blouin J, Bresciani J-P, Bourdin C, Verchr J-L, Gauthier GM (2003). Target and hand position information in the online control of goal-directed arm movements. Experimental Brain Research, 151:524–535. Sarlegna F, Blouin J, Vercher J-L, Bresciani J-P, Bourdin C, Gauthier GM (2004). Online control of the direction of rapid reaching movements. Experimental Brain Research, 157:468–471. Saunders JA, Knill DC (2003). Humans use continuous visual feedback from the hand to control reaching movements. Experimental Brain Research, 152:341–352. Schenk T, Mair B, Zihl J (2004). The use of visual feedback and on-line target information in catching and grasping. Experimental Brain Research, 154:85–96. Sherrington CS (1906). The integrative action of the nervous system. New Haven, CT, Yale University Press. Taub E, Berman AJ (1968). Movement and learning in the absence of sensory feedback. In SJ Freedman (editor): The neurophysiology of spatially oriented behaviour. Homewood, UK, Dorsey Press. Utley A, Sugden D (1998). Interlimb coupling in hemiplegic cerebral palsy during reaching and grasping at speed. Developmental Medicine and Child Neurology, 40:396–404. van Beers RJ, Wolphert DM, Haggard P (2002). When feeling is more important than seeing. Current Biology, 12:834–837. van der Fits IBM, Klip AWJ, van Eykern LA, Hadders-Algra M (1999). Postural adjustments during spontaneous and goal-directed arm movements in the first half year of life. Behavioral Brain Research, 106:75–90. van der Meulen JH, Denier van der Gon JJ, Gielen CC, Gooskens RH, Willemse J (1991a). Visuomotor performance of normal and clumsy children. I. Fast goal-

Reaching and Eye-Hand Coordination • 99 directed arm movements with and without visual feedback. Developmental Medicine and Child Neurology, 33:40–54. van der Meulen JH, Denier van der Gon JJ, Gielen CC, Gooskens RH, Willemse J (1991b). Visuomotor performance of normal and clumsy children. II. Armtracking with and without visual feedback. Developmental Medicine and Child Neurology, 33:118–129. Van Thiel E, Steenbergen B (2001). Shoulder and hand displacement during hitting, reaching, and grasping movements in hemiparetic cerebral palsy. Motor Control, 2:166–182. Volman MJM, Wijnroks A, Vermeer A (2002a). Bimanual circle drawing in children with spastic hemiparesis: effect of coupling modes on the performance of the impaired and the unimpaired arms. Acta Psychologica, 110:339–356. Volman MJM, Wijnroks A, Vermeer A (2002b). Effect of task context on reaching performance in children with spastic hemiparesis. Clinical Rehabilitation, 16:684–692. von Hofsten C (1979). Development of visually directed

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COGNITION AND MOTOR SKILLS Ashwini K. Rao “Perhaps the most incomprehensible thing about the world is that it is comprehensible.” Albert Einstein

CHAPTER OUTLINE CASE SCENARIO MOTOR SKILLS ARE ADAPTIVE What Is the Overall Framework for Understanding Movements? INTRODUCTION TO COGNITIVE CONTRIBUTIONS TO MOTOR SKILLS COGNITIVE PROCESSES IN MOTOR SKILLS Attention Perception Concept Formation (Knowledge) Memory SKILL ACQUISITION (LEARNING) EPILOGUE: RELATIONSHIP BETWEEN COGNITIVE AND MOTOR DEVELOPMENT SUMMARY

Through the course of evolution, the importance of the hand to the organism has increased tremendously. We use our hands to reach out and grasp and manipulate objects, write and draw, make gestures, and create and use tools. Thus our hands are not only used for manipulation skills, but also for communication. The greater importance of hand skills in humans is reflected in an increase in the area of the brain dedicated to hand movement. In addition, cognitive capacity (broadly defined as the collection and organization of information into knowledge) has increased through the course of evolution. This is also reflected in the increase in size of frontal lobe structures in humans when compared with nonhuman primates.

Although the extent of brain structures has increased along with our functional repertoire of hand and cognitive skills, this in no way implies that there is a simple cause-and-effect relationship between brain and behavior. In fact, research on the neural control of movement has shown that although specific areas of the brain are involved in the control of hand movements, the performance of movements in turn influences development of the same neural structures. Thus structure (brain areas involved in hand control) and function (behavioral repertoire of manipulative skills during functional tasks) are intertwined and influence each other through development. Manipulation skills are some of the most complex motor skills and require the coordination of many systems. Within the motor system, manipulative skills require the coordination of many different segments of the body that allow for adapting the hand to grasp different objects and application of precise amounts of force on objects that allow for successful manipulation of objects during functional activity (Flanagan, Haggard, & Wing, 1996). Coordination becomes even more complicated when we consider the cognitive components (e.g., memory, attention, perception) that have to work in concert with the emerging motor skill.

CASE SCENARIO Consider this simple scenario. Jimmy, a 2-year-old typically developing child, is sitting at a table, reaching out to grasp a glass full of water so as to bring it toward his mouth. This simple functional act, one that is carried out by children with seemingly effortless ease, nevertheless is extremely complicated and poses several challenges to a developing system such as Jimmy’s. This

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task highlights the numerous processes that can be categorized as cognitive-perceptual aspects of motor control. Even before beginning the movement of reaching for the glass, Jimmy’s visual processes provide his nervous system with tremendous information about the glass: how far the glass is from him, where the glass is placed on the table with reference to his body, the shape of the glass, how much water is in the glass, the consistency and estimated weight of the glass. The responses to these questions constitute processes called perception and representation. In addition to these perceptual processes, the association of visual input from the glass with symbols about objects provides information that is stored as object knowledge, useful for identification and classification. This information is stored in memory, which can be retrieved at any time. Furthermore, the size and apparent weight of the glass determine whether Jimmy picks up the glass with one or two hands. Such decision making is based on memory of prior interactions with objects. Once Jimmy grasps the glass, his visual and haptic (tactile) processes provide his system with information about the weight of the glass and how the movement of bringing the glass to his mouth displaces the water in the glass. As Jimmy repeats the process of grasping glasses of various sizes, shapes, and weights, and transporting the glass toward his mouth on different occasions, his nervous system internalizes rules about how his movement affects the liquid in the glass through a process of trial and error. This process is called learning and is an essential cognitive skill that enables Jimmy not only to retain the knowledge of how to grasp and lift a given glass, but also generalizes (transfers) this skill to enable successful interactions with various objects.

MOTOR SKILLS ARE ADAPTIVE Motor skills are composed of discrete or sequential movements that are organized in a precise manner to achieve a specific action goal. Sugden and Keogh (1990) described motor skills as “movements that are intentional, goal directed, organized, and adaptive.” This description highlights a few important aspects of motor skills that are particularly important for manipulative skills: 1. The intentional nature of movement indicates a process of planning, which involves cognitive processes 2. The precise nature of movements indicates that movement execution needs to fulfill constraints of the task, and

3. Goal directed indicates that movements, in general, are executed to accomplish a particular action. There are instances in which the goal of the action is a specific set of movements, as in a dance performance. In this chapter, however, we are concerned primarily with manipulative skills that are executed to achieve an action goal (e.g., feeding, object manipulation, writing).

WHAT IS THE OVERALL FRAMEWORK FOR U NDERSTANDING MOVEMENTS? Movements are one of the primary means by which humans interact with the environment and act on the environment. Thus an understanding of movement has to take into consideration an understanding of the nature of the environment in which movements take place. Shumway-Cook and Woollacott (2001) have suggested that movement emerges through an interaction of the performer (including biomechanical constraints of our musculoskeletal system), the task (which can range from body stability to manipulation), and the environment. According to Gentile (2000), the structure of a task determines the demands placed on the performer. Given that different tasks pose different challenges for the performer, it is imperative to begin with an understanding of tasks. Gentile proposed an analysis of tasks that categorized tasks based on their functional role and the environmental context (Gentile, 1972). Based on the functional role, tasks can either specify body orientation (which includes body stability and body mobility) or manipulation of objects. With reference to environmental context, tasks can be categorized as those that are performed in closed environments, which remain stable from trial to trial, or those that are performed in open environments which change from trial to trial. On the basis of this classification, Gentile proposed a taxonomy of tasks that has helped us understand tasks and the challenges they pose, and also as a basis for evaluation and intervention in clinical practice (Gentile, 1992, 2000).

INTRODUCTION TO COGNITIVE CONTRIBUTIONS TO MOTOR SKILLS The importance of cognition in motor skill acquisition and development is well established. However, the reverse also has been proposed: that perceptual motor activity is a mechanism for cognitive development. However, the importance of cognition to motor skills depends on the theoretical orientation that is used.

Cognition and Motor Skills • 103 Some of the major theoretical orientations in the literature are the Piagetian approach (Piaget, 1952), the behaviorism approach of Skinner (1953), the ecological approach of Gibson (1979) and more recently, the information processing approach that has been reformulated within the relatively new discipline of cognitive neuroscience (Gentile, 2000; Thelen, 1995). Each of these approaches is discussed briefly. For the purpose of this chapter, the cognitive neuroscience approach is used. Piaget considered that motor activity was necessary to the development of knowledge about the environment. Knowledge development was believed to be a function of the interaction between neural structures and the environment. According to Piaget, cognitive functions develop through knowledge gained as a result of action, which early in development is based on innate reflexes (Piaget, 1952). Based on this approach Piaget proposed a stage-like developmental process in which new skills are learned based on skills previously learned in development. For Piaget, infant motor activity played a major role in cognitive development. Object manipulation was believed to be critical for the child’s learning about object properties. The manipulation of objects is important as a way of facilitating mental activity, which is believed to be the key for learning object characteristics. Overall, in this approach, cognitive-neural development is thought to play an important role in development of skills, whereas factors outside the performer (i.e., the environment) are not emphasized. This is in stark contrast with the behavioral approach, pioneered by Skinner and his colleagues, which emphasized the role of reinforcement from the environment as a primary driving factor in development (Skinner, 1953). Development, according to this framework, occurs through the responses of the performer and the reinforcement she or he receives through the environment. One approach that differed from these two approaches was proposed by Gibson (1979). In this approach action is not a precursor to perception. Rather, perceptual information is actively sought through coordinated systems of action, some of which are already functioning in this capacity at birth. This approach proposed that most of the information needed for the control of motor skills was contained in the flow of sensory afference (visual or haptic). Development was thought to be a process whereby the performer learns not so much to improve his or her movement skill per se, but to learn to use the information contained in the sensory flow. Although this approach explained some of the behaviors seen during development, it did not highlight the role of neural structures in the developmental process.

The emerging approach in motor development is one that developed out of the information processing theories and current theories in motor control. Much of this approach was influenced by Bernstein, a Russian physiologist, who proposed that movements emerge through the interaction among the performer, the impact of movements made by the performer, and the environment (Bernstein, 1967). Within motor development, the application of this approach was pioneered by Esther Thelen (1995). In this approach, movements are proposed to emerge through the cooperative interaction of many body parts and the environment, rather than from a one-to-one mapping between neural structures and movements. Because movements are slightly different from trial to trial (even when the same muscles are activated), Bernstein proposed that actions were planned at a more abstract level. This is particularly true because it is impossible for the nervous system to program all the force-related contextual interactions ahead of time. Thelen (1995) argued that cognition and motor skills emerge from a dynamic process in which the performer learns the match among herself, her movements, and the environment and how the various component parts are coordinated to produce skillful movement. Thus early in the development of a skill, a high degree of variability is seen in the behavior. Rather than seen as an undesired outcome, variability is seen as functional, and is exploited in the generation of solutions. With development, the macrostructure of the movement (the visible motor output) becomes less variable and more stable, but this stability arises as a result of maintaining variability at a microstructural level, which refers to the forces generated and the patterns of muscular contraction (Manoel Ede & Connolly, 1995). With this framework in mind, we explore the different constituents of cognitive skill and their relationship to motor skills. Although an attempt is made to present the most pertinent and current literature on infants and young children, at some points results from adult studies are presented when little or no evidence is available from the developmental literature.

COGNITIVE PROCESSES IN MOTOR SKILLS In this section, we discuss a few important components of cognition critical to the successful generation of motor skills. Attention, perception, concept formation, memory, and learning are briefly discussed. Although each component is discussed separately for clarity, one should understand that in the development of motor skills, many of these components interact with each

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other and may assume differential importance depending on the demands of the task.

ATTENTION Attention is a fundamental aspect of all human activity. We are able to perceive stimuli and act on them better when we attend to the stimulus of interest and ignore extraneous stimuli. Our sensory systems receive a tremendous amount of information. If we did not have a mechanism to filter unwanted stimuli, we would encounter sensory overload. At any given moment, we are aware of only a few stimuli that are functionally important to the task at hand, and our awareness is limited by our capacity for processing information. Thus functional attention is selective by definition. Attention can be defined by examining its constituent parts of arousal, capacity, and selectivity (Plude, Enns, & Brodeur, 1994). Arousal refers to the momentary level of excitation in the information processing system that helps tune our cognitive systems to optimally receive information. Capacity refers to the actual capacity of our information processing system. It is generally accepted that humans can process a certain amount of information at any given moment. Finally, selectivity refers to the ability of the system to allocate resources so as to focus on certain stimuli and not others. Selective attention is a multidimensional process, involving components of orienting, filtering, searching and expecting (Plude et al., 1994). From an early age, infants show preference for orienting their vision to attend to certain stimuli while ignoring others (Maurer & Lewis, 1991). In fact, neonates spend more time attending to their mothers’ face than the faces of strangers, even when other sensory cues, such as smell and auditory cues, are excluded (Bushnell, Sai, & Mullin, 1989). The orienting response is variable and not developed early in life, presumably because the neural structures that control such behavior (e.g., the superior colliculus) are not fully developed. Nevertheless, the evidence suggests that infants demonstrate beginning capabilities for selective orientation to preferred stimuli. Another aspect of selective attention is that infants show a preference for novel stimuli rather than stimuli that have been present in the environment. Most of us have observed infants paying more attention to new faces in comparison with familiar faces. This phenomenon is known as habituation and refers to the decrease in the amount of visual attention (time spent on a stimulus) devoted to more familiar stimuli (Bertenthal, 1996; Ruff, 1986). Ruff found that the amount of time spent in examining novel stimuli decreases as the infant becomes familiar with an object and suggests that the

time spent on novel stimuli may be influenced by the arousal properties of the object. Although infants have some capability in orienting to stimuli, as shown in the preceding paragraphs, their ability to devote attention resources to actively search for objects of interest does not develop until early school years (Cohen, 1981). Similarly, the skill of paying attention to stimuli that has already been experienced develops during the early school years. This phenomenon, known as priming, refers to the fact that we are able to better attend to stimuli that has been presented before, even if for a short period of time. Priming also explains how certain stimuli are recalled easily because of prior exposure (Plude et al., 1994). To summarize, attention is a fundamental aspect of cognitive skills that is related to perception and memory. When we consciously attend to a sensory stimulus, our perception is matched to information stored in our memory (priming or recognition). Attention is an active process in which certain stimuli in the environment are given preference over others depending on their perceived importance to the demands of the task being performed.

PERCEPTION Perceptual processes constitute an important part of cognitive contributions to motor skills. Perception can be defined as a process of collecting information from the environment based on vision, touch, hearing, and muscle and joint proprioceptors to construct an internal representation of space and the body (Kandel, 2000). Thus our perception is created through an active process of searching for and attending to stimuli based on our sensory organs. All pertinent information is then used in the construction of an internal representation. Historically, perception was thought to emerge from a developmental process as infants and young children developed their repertoire of sensorimotor behaviors (Piaget, 1952). The current view, however, challenges this notion and proposes that different sensory inputs converge into a unified representation that precedes thought and action (Marr, 1982). The emerging framework from the cognitive neurosciences proposes that there may be at least two independent and parallel perceptual processes: one that is used in the recognition of objects and the other used for the guidance of movements (Goodale et al., 1994). Thus visual information about an object in the environment is processed by separate neural pathways and used for different purposes (Bertenthal, 1996; Goodale & Westwood, 2004). The system for the identification of objects, also called the ventral stream, is proposed to project from the visual cortex to the temporal lobe. The system for

Cognition and Motor Skills • 105 action, also called the dorsal stream, is proposed to project from the visual areas to the posterior parietal cortex. Although most of the evidence for this proposal comes from neurophysiological studies from nonhuman primates, neuropsychological studies in humans with focal cortical lesions, and imaging studies in adults (Goodale & Westwood, 2004), some authors have proposed that such a dissociation may be present during development (Johnson, 1990). There are fundamental differences in these two subsystems that support the notion that they operate independently. First, the system for the guidance of movement is proposed to work in a prospective manner because actions are directed toward information present at the time. Von Hofsten has argued that actions occur through dynamic interactions between an organism and the environment that occur in a future-oriented manner (von Hofsten, 1993, 2004). For example, in reaching for objects, infants begin to crudely adjust the orientation of their hand to match the orientation of the object even before grasping the object of interest (von Hofsten & Fazel-Zandy, 1984). Such adjustments are made in an anticipatory (prospective) manner to maximize success at reaching objects. This is in contrast with the system that is used for object identification in which the information is retrieved from a representation that is stored in memory (Goodale et al., 1991, Goodale et al., 1994). Second, the difference between these systems pertains to the manner in which the information is structured in the brain. All sensory information is structured and represented in a format of coordinates called a coordinate system. Although the information used for perception and identification of objects is structured in a coordinate system centered on the environment (or world centered), information that is used for the guidance of movement is structured in body coordinates (Goodale & Westwood, 2004). This is because perception of objects requires that the observer be able to identify object features correctly independent of his or her position vis-à-vis the object. In contrast, sensory information used for guidance of movement is structured in body centered coordinates (Soechting & Flanders, 1992). This is because sensory information used for movement ultimately has to be converted into patterns of muscle activation that will move the arm to the desired object. Because specification of movement parameters ultimately has to match egocentric coordinates of muscle action, it seems likely that such information is stored in body-centered coordinates. Third, these two systems also differ in terms of the nature of conscious processing involved. The system that deals with object perception and identification processes visual information in a conscious manner because the observer is required to actively attend to

the stimulus. In contrast, the system that deals with guidance of movement processes information subconsciously. We are not conscious about processing sensory information when manipulating objects. Perhaps the best evidence for this dissociation comes from studies of patients with brain lesions who are unable to perform conscious processing necessary in identification of objects but nevertheless are able to reach out and grasp them (Goodale et al., 1991). For instance, patients with lesions of the ventral stream (pathways from the primary visual cortex to the temporal lobe structures) are unable to identify objects but are able to reach out and grasp objects with problems. Patients with lesions of the dorsal stream (the posterior parietal cortex) show the opposite deficit: They are able to identify objects but are unable to reach out and grasp them (Goodale & Westwood, 2004). Thus converging evidence from animal studies and human lesion studies suggest that information for perception and action are processed independently. The system involved in perception perhaps develops later as it involves conscious processing of knowledge from memory, skills that develop as a child learns language.

Perceptual-Motor Processes We must perceive in order to move, but we must also move in order to perceive. (Gibson, 1979) This statement, from one of the most influential psychologists in the area of perception, highlights the reciprocal relationship between perception and action. According to Gibson (1979) perceptual systems have adapted to use information pertinent to actions that are readily available in the environment. For instance, perceptual-motor systems use visual information available in the optic array, haptic information from hands as they explore objects, and proprioceptive information available from muscles and joints. Although movements are adapted in response to perceptual processes, the reverse is true as well. Such reciprocity was shown in a study that tested crawling infants and recently walking infants on their locomotion on two different surfaces; a rigid and a pliable surface. Although crawling infants did not differentiate between these two surfaces, recently walking infants changed their mode of locomotion depending on the surface. They crawled on the pliable surface and walked on the rigid one (Gibson et al., 1987). More recently, it was shown that recently walking infants adopt a more stable posture (sitting) as they negotiate a surface with a downward incline, whereas crawling infants did not adapt their posture (Adolph, Eppler, & Gibson, 1993). These studies show that perception (e.g., perceived stability of surface)

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influences action and action in turn influences perception (e.g., newly walking infants differentiating among surfaces). Contrary to the proposals of early models of perceptual-motor development (Piaget, 1952), goaldirected behavior is observed very early in development. Infants as young as 3 weeks old have been observed to reach out and grasp stationary and moving objects (von Hofsten, 1982). Neonates actively control their gaze and look at faces that engage them in a mutual gaze (Farroni et al., 2002), and visually track moving objects within their first month (Bloch & Carchon, 1992). Von Hofsten (1993) argues that behaviors that are explored in the womb (e.g., hand-tomouth behavior) may demonstrate an advantage after birth. The evidence described in this section highlights that infants are capable of goal-directed movements based on visual information available in the environment (e.g., from a moving object). Although this behavior is highly variable from trial to trial, and fragile (it is not observed consistently), the existence of such control provides evidence that our perceptual systems are tuned to act on visual and haptic information from a very early age. According to Thelen (Thelen, 1995; Thelen & Corbetta, 1994), behavior is highly variable when first expressed and is gradually adapted as a result of a dynamic process of selection of the most appropriate coordinative structures that are specific to the contextual demands of the task. The contextual nature of perceptual-motor behavior, in part, is dependent on the fact that motor skills are not simply influenced by perceptual processes but also by biomechanical and physiologic factors. For example, although infants are able to reach for moving targets at the age of 3 weeks, such behavior is contingent on the stability of their head (von Hofsten, 1982). When the head is not stabilized, goal-directed reaching is not observed. In a now classic example of the contextual nature of perceptual-motor behavior, Thelen and colleagues described the case of the “disappearing reflex” (Thelen, 1995; Thelen, Fisher, & Ridley-Johnson, 1984). Infants are known to demonstrate a stepping reflex when held upright with their feet on a supporting surface. Within a few months, this “reflex” pattern of movements is not seen. The traditional explanation for the disappearance of this reflex was that the maturing nervous system inhibited the reflex, a primitive behavior. However, at the same time that the reflex disappears, infants also demonstrate an increase in their body mass. When such infants were held upright partially submerged in water with their feet in contact with a surface, the stepping reflex re-emerged, indicating that the reflex “disappeared” primarily because of increased weight and a biomechanically demanding posture (Thelen et al., 1982; Thelen & Fisher, 1982)

rather than simply because of neuromaturational factors.

CONCEPT FORMATION (KNOWLEDGE) Concept formation refers to a higher-order mental process that acts on information that has been perceived through our sensory organs and encoded and stored in memory. This process includes organization of the information into conceptual categories and the use of such knowledge in reasoning, problem solving, goal selection, and planning. Through the process of categorization, infants and young children begin to form concepts about objects, people, and actions. For instance, early in development, infants learn to categorize faces as familiar and unfamiliar. As discussed in an earlier section, infants are seen to spend more time attending to faces that are familiar, such as the mother (Bushnell et al., 1989). This indicates that infants have already begun to categorize faces according to their perceived familiarity. Concepts (e.g., faces and objects) are units of mental representation that assign certain perceptual features to specific conceptual categories. Early in development, we learn to differentiate between living and nonliving objects, based on our ability to generate selfmotion. This process becomes more complex as we learn to differentiate subcategories within these categories of living and nonliving objects. Knowledge organized into such categories is encoded and stored in long-term memory and retrieved during action. Key elements of concept formation are the processes of grouping and differentiation. Grouping involves the clustering of information into larger units, a process known as “chunking” (Gentile, 2000). Chunking helps the system function more efficiently because the performer has to attend to groups of information rather than each piece of information separately. The benefits of chunking perhaps can be seen best through an example: Consider a child walking through his classroom to his teacher. In performing this task, he encounters numerous toys strewn across the floor, furniture placed all over the room and a few peers running around in the classroom. The process of chunking allows the grouping of all stimuli into stationary and moving objects; this way the child can perceive the movement of his peers as a unit rather than attend to the movement of each child individually. Grouping reduces the attention demands of the task and allows the child to allocate his attention to additional stimuli (furniture) that are important. Differentiation, on the other hand, refers to the process through which performers perceive more detail in an array of stimuli as they become more familiar with it. To use the example cited in the preceding paragraph,

Cognition and Motor Skills • 107 as the child begins to learn to walk, he will likely not perceive the subtle differences in the speed of movement of the moving objects in the environment. With experience, he will learn to distinguish between stimuli related to other children either walking or running. Development of concepts and knowledge is extremely useful for understanding the demands of the task and goal completion. Early in the learning of a task, performers should learn the relationship between movement and the goal of the movement. Failure to understand the goal of the task can lead to goal confusion, which is commonly seen in elderly individuals with memory disorders (Gentile, 2000). Specification of the goal of the task has been shown to be critical in improving the quality of movement (determined by kinematic analysis) in unimpaired adults (Lin, Wu, & Trombly, 1998; Wu et al., 1998) and individuals recovering from a cerebrovascular accident (Wu et al., 1998). Changing the goal of the task influences the movement pattern selected. In a classic study (Marteniuk et al., 1987) demonstrated that unimpaired subjects reached for and grasped a disc differently depending on whether the goal of the task was to place the disc accurately in a container or to throw the disc. Attention to the goal and knowledge of the relationship between movement and its outcome (action) are key components of concept formation pertaining to hand skills. In summary, concept formation is a conscious and active process that categorizes sensory information by associating it with conceptual categories. These categories are stored in long-term memory and retrieved in response to the demands of the task. As stated earlier in the chapter, such information is thought to be processed through ventral neural pathways projecting from the visual cortex to the temporal cortex (Goodale, 1992).

M EMORY Memory is the process by which knowledge is encoded, stored, and retrieved (Milner, Squire, & Kandel, 1998). The neurobiological pathways responsible for memory are dependent on our sensory perceptual and attention processes (discussed in the preceding sections) that allow task-related information to be stored. Most models of memory propose the existence of multiple systems of memory, each devoted to a specific function (Willingham, 1997). Memory can be classified in many different ways: One is to classify it according to the time scale of the operation. Thus we distinguish between short-term (working) and long-term memory systems. Working memory is proposed to be a dedicated system that holds information for short periods of time

so that it can be manipulated during functional tasks. According to Baddeley (2003), working memory is a limited capacity system that supports thought processes by providing an interface among perception, long-term memory, and action. Working memory is proposed to consist of at least three components: a central executive, and two storage loops; the phonological loop and the visuospatial sketch pad. The central executive is proposed to be the attention control system, which regulates the function of the other two subsidiary rehearsal systems. The central executive also serves as a buffer that holds information temporarily. The phonological loop contains a phonological store “which can hold memory traces for a few seconds before they fade, and an articulatory rehearsal process that is analogous to sub-vocal speech” (Baddeley, 2003). The phonological loop has a limited capacity that limits the amount of information that can be held and manipulated at any given time. Finally, the visuospatial sketch pad is also a limited capacity rehearsal loop and mainly deals with spatial information perceived through the visual system (Baddeley, 1998). The function of the visuospatial loop is to hold and manipulate visual spatial representations, as seen in tasks that require mental rotation of images. Most of the evidence supporting the model of working memory comes from studies in unimpaired adults and adults with focal cortical lesions. From a developmental perspective, it seems likely that the visuospatial sketch pad develops before the phonological loop because the phonological loop is dependent on language-based processes. Studies on the development of working memory report age-related differences in the speed with which words can be articulated and differences in attention span (Hitch & Towse, 1995). These age-related differences appear to result from maturational factors (Cowan et al., 1999). The other major classification that pertains to longterm memory is based on how the information is stored and recalled. According to this classification, memory can be either explicit (or declarative) or implicit (procedural). Explicit memory is associated with conscious awareness and the intention to recall information. This form of memory typically is tested with recall or recognition and underlies the memory for objects, people, and events. Studies with infants have revealed that they can retain memory for objects (as tested by retention) across intervals of 1 to 3 months (Bahrick & Pickens, 1995). Based on additional studies, Bahrick and colleagues proposed that recent memories are expressed as a visual preference for novelty, whereas remote memories are expressed as a preference for familiarity (Bahrick, Hernandez-Reif, & Pickens, 1997). However, younger children need greater numbers of prompts to recall memories compared with older children.

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Explicit memories are further divided into memories for facts (semantic memory) and events (episodic memory). Semantic memory is built up by associating a stimulus with specific concepts. Thus a visual image of an elephant associates features of the elephant (e.g., its large size, large ears, tusks, and small tail) with the conceptual category of “elephant.” This information is then further associated with additional knowledge about elephants that allows children to close their eyes and recall an internal representation of an elephant. Semantic memory is thought to be stored in a distributed fashion in the neocortex, including the medial temporal areas that process verbal information and occipital areas that process visual information. Episodic memory, on the other hand, is concerned with the temporal ordering of events. In children, this type of memory is built up by associating events with what happened during such events (Schneider, 2000). Explicit memory is processed in four distinct phases. The first phase is called the encoding phase, during which new information is attended to and processed at first encounter. All pertinent information in the stimulus must be attended to for memory to be stored in long-term memory. A second phase is consolidation, in which the new information is altered from a labile state to a stable state for long-term storage. Consolidation is a time-dependent process, and any event that interferes with this process prevents new and labile information from being converted to long-term memory. The third phase is storage, which refers to the mechanism by which memories are retained over time. Finally, the fourth phase is retrieval, which refers to the process of recall of memories (Kandel, 2000). Implicit memory, in contrast with explicit memory, is concerned with storage and recall of information without conscious awareness (Milner et al., 1998). This kind of memory is also called procedural memory, because it refers to knowledge about “how” a task is performed, rather than “what” a task is. Implicit memory does not depend on conscious processing of information, builds slowly over time through repetition, and is primarily expressed through performance rather than through language (Kandel, 2000). Most of the early evidence of the distinction between implicit and explicit memories came from the study of individuals with focal lesions of the medial temporal lobe. In one patient (HM) most of the medial temporal lobes were removed secondary to seizures. The surgical lesion left HM with a memory deficit of explicit long-term memory, particularly for facts and events that occurred after the surgery and also a deficit of events that occurred immediately before the surgery (retrograde amnesia). Although he had a relatively intact short-term memory, HM was unable to transfer information from short-

term to long-term memory (Milner et al., 1998). Despite his devastating deficit in explicit (declarative) memory, HM could learn new motor skills such as mirror drawing (Milner, Corkin, & Teuber, 1968) or novel patterns of arm movements (Shadmehr, Brandt, & Corkin, 1998) comparable to age-matched unimpaired subjects. Thus patients with temporal lobe lesions are able to learn tasks that do not require conscious awareness and tasks that are procedural. These studies have helped us understand that explicit and implicit memories are independent systems, controlled by different areas in the cortex (Milner et al., 1998). For the developing child, it has been shown that older children demonstrate an advantage for explicit memories, whereas there is no specific age-related difference in the formation of implicit memories. This difference in the development of the two memory systems may result from the fact that sensory and perceptual systems are developed early in life (as discussed in the preceding section), whereas concept formation (which is necessary for development of explicit memories) continues to develop until the school years (Bertenthal, 1996; Schneider, 2000).

SKILL ACQUISITION (LEARNING) Learning is the process by which we acquire knowledge about the world and ourselves. Skill can be defined as consistently attaining an action goal with some economy of effort (Gentile, 2000). Learning of motor skills concerns a set of processes associated with practice or experience, which leads to a relatively permanent change in the ability of the performer to produce movements (Shumway-Cook & Woollacott, 2001). Box 6-1 highlights a few important concepts. Learning is thought to progress in stages. Although different models of learning have been proposed, most models agree that different processes operate during the early and late stages of learning. For the purpose of this chapter, we discuss the two-stage model proposed by Gentile (1992, 1998, 2000). According to this model, in the early stages of learning, the performer acquires the general concept of the demands of the task and the movements that are necessary to successfully achieve the goal. Part of this process is to understand and attend to important features of the action goal: This enables the performer to focus on the regulatory features in the environment and ignore the nonregulatory features. According to Gentile (2000) the action goal concerns the function of the task (whether the task requires manipulation or requires body orientation or both) and the nature of

Cognition and Motor Skills • 109 BOX 6-1

Descriptions of Learning

1. Learning is a process whereby a child acquires the capability for skilled action. 2. Learning results from practice or experience, rather than being simply a function of neuromaturation. Perhaps this concept is best highlighted by the fact that infants practice tasks such as reaching (von Hofsten & Fazel-Zandy, 1984) and locomotion (Adolph, 1997) several hundred times in a day over a period of months before they become skilled. This extended practice is the basis for improvement of skill. 3. Learning is a process that cannot be observed directly and typically is inferred from changes in behavior. As discussed in the preceding sections, much of the evidence on motor development has come from detailed longitudinal observational studies in infants and young children (Adolph, 1997; Thelen, 1995; von Hofsten & Fazel-Zandy, 1984). 4. Learning produces changes that are relatively

the environment in which the action is taking place (whether the environment is stationary or in motion). Focus on the regulatory features necessitates selective attention to pertinent stimuli. During this process, the performer’s system learns to differentiate the environment (perceive greater detail in the sensory array) and grouping of similar stimuli into chunks, a process described earlier. During this phase, the child pays attention to the overall structure (shape or configuration) of the movement. Thus in reaching for an object, a child is aware of the orientation of her hand as it attempts to approximate the orientation of the object for successful grasp. Gentile (1992) terms this the topology or shape structure of the movement. Although the performer is aware of the topology, she or he is not aware of the internal processes of parameter specification that specify the timing of the movement components, the forces to be imparted to the limbs, and so on. During this early stage, based on the results of the movement, the child receives feedback on the outcome of the movement. This knowledge is then encoded and stored in memory and helps the child learn the association between movement patterns and their outcome. This process enables children to repeat successful movements and leads to the formation and refinement of internal models (or representations) of the task. Studies of infants learning to perform goal directed reaching have demonstrated evidence for this notion. Recording of the movement patterns of infants have shown that early in learning, arm reaching movements are extremely variable and the goal of reaching for and grasping an object is not achieved consistently. How-

permanent. This indicates that information acquired through learning is stored in long-term memory, which typically is retained over long periods of time. 5. Learning is task specific. A pattern of movement that produces successful goal-directed interactions may not be sufficient if there are changes in the environment or in the morphology of the performer, as happens continuously through development. Thus skill attained under certain conditions can be generalized only to other skills that share features with the original skill learned. For instance, once a child learns to reach for one stationary object, she or he can adapt this skill and generalize it to successfully reach for stationary objects of different shapes and sizes; however, this skill of reaching for stationary objects does not necessarily generalize to reaching for moving objects because such a task poses different challenges to the system and requires novel solutions.

ever, within a relatively short period of time, movements converge to a consistent topology enabling the child to achieve the goal more consistently (Konczak et al., 1995; von Hofsten et al., 1984). With refinement of the internal model, the abstract representation of the movement and outcome becomes independent of the actual environmental and biomechanical constraints. For instance, in learning the task of writing, a child acquires an internal model of the task. In this case the movements of the hand (and the forces applied) that produce the form (or topology) of a letter. Once this model is learned, the child can perform this task not only with the dominant hand, but with the nondominant hand as well (although not as efficiently because the nondominant hand is not as skilled). The fact that we can produce the same action using different effectors highlights the importance of an internal model (abstraction) of the task that is independent of the effectors. Skill is refined during the later stages of learning. Performance improves but at a much slower rate than in the early stages of learning. In this phase improvements occur in the efficiency of the movement: The child is better able to predict the consequences of her movement and better able to produce consistent movements from one trial to the next. According to Gentile (1998) this phase is characterized by changes that the performer is not aware of. The changes pertain to the parameter specification, and include improvements in the timing of force generation of the segments involved in the movement and the timing and amplitude of muscle contractions that ultimately produce the

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movements. In addition, movement sequences are more efficiently blended together temporally so that each sequence is not discernible from other sequences of movement. The evidence from recording of intersegmental forces and patterns of muscle activation demonstrates that improvements at this level of the system continues over a much longer period of time (Konczak, Borutta, & Dichgans, 1997). Although the topology of reaching movement improves within the first few months, improvements in the coordination of forces continue until at least the third year. This underscores the fact that consistency in the external features of movements (e.g., topology) are contingent on internal features (e.g., coordination of forces and muscle patterns) that remain variable over a much longer period of time (Manoel Ede & Connolly, 1995). It can be argued that the variability in the coordination of forces allows the system flexibility and generalizability. In summary, learning is thought to progress through two interdependent and parallel processes. The early phase is characterized by establishment of a mapping between the performer and the environment that, with practice, quickly improves the overall shape structure of the movement. The processing of information during this phase is explicit in nature and leads to the formation of an internal model of the task (Gentile, 1998). Later in learning, movements are refined at a micro level that is not observable in the behavior. The processing of this information progresses without conscious awareness on the part of the performer (i.e., implicitly). Because the improvements at this stage concern coordination of the details of intersegmental forces, the later stage of learning is extended over a longer period of time (Gentile, 2000).

EPILOGUE: RELATIONSHIP BETWEEN COGNITIVE AND MOTOR DEVELOPMENT Historically, motor development and cognitive development have been studied separately and viewed as somewhat independent of each other. It was also a widely held belief that cognitive development occurred over a longer period of time compared with motor development. It is now apparent that motor skills, particularly complex skills such as bimanual control and some visuomotor skills, continue to develop until adolescence. A recent development in the understanding of the relationship between cognitive and motor development proposes that they are in fact highly interrelated. This relationship is primarily

ascribed to the relationship between the prefrontal cortex (which was thought to control cognitive skills) and the cerebellum (which was thought to be involved in movement), both of which are proposed to be involved in cognitive and motor skills (Diamond, 2000). Evidence for this proposal comes from imaging studies during performance of motor or cognitive skills and studies with patients with cortical and cerebellar lesions. In terms of learning of motor skills, it has been shown that both the prefrontal cortex and cerebellum are activated: The activation shifts from the prefrontal cortex to the cerebellum as the task is learned (Shadmehr & Holcomb, 1997). Coactivation of the prefrontal cortex and cerebellum also has been seen in working memory tasks (Desmond, Gabrieli, & Glover, 1998; Smith & Jonides, 1997). According to Diamond (2000), both the cerebellum and prefrontal cortex are active under certain conditions; when the task is more difficult, novel as opposed to familiar, unpredictable as opposed to stable, and requires a quick response (p. 45). Patients with lesions to the cerebellum demonstrate deficits in a variety of cognitive tasks such as working memory tasks administered through bedside neuropsychological tests, set shifting tasks, and visuospatial memory tasks (Schmahmann & Sherman 1998). These deficits are presumably seen because of the interconnections between the prefrontal cortex and the neocerebellum (Ghez & Thach, 2000). Developmental evidence in support of this theory has come from studies that have examined motor problems in children with cognitive problems. Attention deficit hyperactive disorder (ADHD) is a syndrome in which children demonstrate cognitive deficits, including a short attention span. It is interesting to note that along with deficits in cognition, many children with ADHD demonstrate motor deficits as well (Kadesjo & Gillberg, 1998). This may be related to a decreased size of the cerebellum in children with ADHD compared with unimpaired children (Castellanos, 1997). Similar motor deficits are also reported in children with dyslexia. In one study, it was reported that children with dyslexia have problems with motor tasks that require control of the timing of movements, such as tapping a rhythm (Geuze & Kalverboer, 1994). Because timing of movements is a function attributed to the cerebellum (Ghez & Thach, 2000; Keele & Ivry, 1990), and given the connections between the cerebellum and prefrontal cortex, it is not surprising that children with dyslexia demonstrate motor deficits. Children with autism also show deficits in motor tasks, particularly in the execution of goal-directed movements (Hughes, 1996). Although the motor deficit in all these disorders is not the most significant, the existence of these motor disorders highlights the close relationship between cognitive and motor skills.

Cognition and Motor Skills • 111

SUMMARY In this chapter we have described motor skills as goal oriented and made up of movements that are organized to solve the spatial and temporal challenges presented by specific tasks. In addition to the control processes underlying motor control, we have described many components of cognitive skills that are important for the development and execution of motor skills. Cognitive development and motor development are closely related and have a reciprocal relationship. Hand function is critical in supporting cognitive development because hand movements allow for interactions with objects that in turn support the development of knowledge about objects. Tool use with the hands almost always requires cognitive skill to comprehend the means–end relationship of movement to goal or outcome. In contrast with hand skills, gross motor skills seem to require little cognitive development for their emergence. This chapter has covered a number of topics related to the literature on the relationship between motor skills and cognition. The past few years have seen a fundamental shift in the way in which we understand the relationship of cognitive and motor skills and our understanding of development in general. The emerging paradigm proposes that movement skills are developed not only as a function of neuromaturation, but also through the interaction of emergent movement and cognitive skills with the environment. This new paradigm “emphasizes the multicausal, fluid, contextual and selforganizing nature of developmental change, the unity of perception, action and cognition, and the role of exploration and selection in the emergence of new behavior” (Thelen, 1995).

For therapists interested in learning better ways to teach children to learn or relearn cognitive and motor skills, the new paradigm offers novel ways to assess and plan interventions. For instance, different interventions may be necessary to facilitate implicit versus explicit learning. Although therapists can use conscious processes to facilitate explicit learning, the only way to enhance implicit learning is to carefully structure the environment and select tasks for optimal practice, and provide timely feedback and structure ample opportunities for prolonged practice (Gentile, 1998). Thus therapists not only have to keep the child in mind during the assessment and intervention, but the environment in which the skills are performed as well. As we develop greater knowledge of the differential impact of cognitive disability (e.g., attention, perceptual, memory, conceptual) on the acquisition of motor skills,

the challenge ahead will be to develop creative therapeutic solutions that enhance skill acquisition.

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Chapter

7

HAND SKILL DEVELOPMENT IN THE CONTEXT OF INFANTS’ PLAY: BIRTH TO 2 YEARS Jane Case-Smith

CHAPTER OUTLINE DEVELOPMENTAL THEORIES AND CONCEPTS A Neuromaturation Model Individual Patterns in Hand Skill Development Hand Skills Emerge Through the Interaction of Systems Perception as a Primary Influence on Hand Skill Development Development of Hand Skills for Functional Outcomes CONTEXTS FOR HAND SKILL DEVELOPMENT SYSTEMS THAT CONTRIBUTE TO THE DEVELOPMENT OF HAND SKILLS

The development of prehension and bimanual coordination is essential to an infant’s ability to play and explore. As hand skills mature, the infant becomes increasingly competent in exploring and playing with objects. The young infant’s rudimentary grasp and release patterns become precise patterns during the first years of life. The purpose of this chapter is to describe the infant’s development of grasp, release, and bimanual skills in the context of exploratory and functional play. The first section describes developmental theories and concepts helpful to understanding the development of hand skills. The second and third sections describe how contexts, posture, and sensory function influence hand skill development The fourth section describes the play activities and specific hand skills that characterize the sequential stages of infant development, birth to 2 years.

Posture Sensory Systems DEVELOPMENT OF HAND SKILLS IN THE CONTEXT OF INFANT PLAY ACTIVITIES

DEVELOPMENTAL THEORIES AND CONCEPTS

Play Activities: Birth to 12 Months Prehension: Birth to 12 Months Object Release: Birth to 12 Months Bimanual Skills: Birth to 12 Months Play Activities: 12 to 24 Months Prehension: 12 to 24 Months Object Release: 12 to 24 Months Bimanual Skills: 12 to 24 Months SUMMARY

A N EUROMATURATION MODEL Early theories of motor development (Gesell, 1928; Halverson, 1931, 1937; Shirley, 1931) emphasized the importance of central nervous system control over motor performance. Gesell documented an orderly sequence of motor development, stage by stage, that could be observed in every typically developing child. The theory that maturation of skill and behavior resulted from the maturation of the central nervous system dominated understanding of motor development in the

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1930s and 1940s. Based on neuronal maturation, grasp and manipulation patterns develop in an orderly and relatively invariant sequence. The sequence of reaching and grasping patterns identified in the 1930s by Gesell and Halverson continues to be referenced in developmental motor tests in use today (Bayley Scales of Infant Development) (Bayley, 1993). The neuromaturation theory—that motor development reflects central nervous system maturation— emphasizes that early movements are involuntary reflexes under the influence of subcortical brainstem structures (Andre-Thomas, 1964; Gilfoyle, Grady, & Moore, 1990; McGraw, 1943). Neonates’ reflexive behaviors are automatic reactions to sensory stimulation that result in neonates experiencing arm and hand movements over which they later gain control. Reflexes provide young infants with survival capabilities (e.g., sucking and rooting) and protective responses (e.g., avoiding response). Reflexes allow infants to experience a complete range of movement and tactile proprioceptive input. Reflexes and reactions are modified through interactions with the environment as infants assimilate the sensory feedback from reflexive movements (Gilfoyle et al., 1990). In the first 6 months they become integrated into acquired or voluntary behaviors. McGraw (1943) describes a typical progression of maturation: (a) dominant reflexive responses, (b) inhibition of reflexes, (c) transitional behaviors, and (d) voluntary motor pattern and skill. This typical sequence varies in the timing of onset and completion of each phase but appears to be remarkably invariant in the ordering of developmental motor patterns. When cortical control begins to dominate over subcortical control of hand movement, voluntary grasp emerges. Transitional behaviors mark the period when reflexes are inhibited and voluntary controlled movements begin to develop (Twitchell, 1970). By 4 months the infant grasps a visually located object. A series of studies were completed from 1925 to 1940 to examine the neuromaturation model. These descriptive studies documented the unfolding of grasping patterns in the first year of life (Castner, 1932; Halverson, 1931, 1932, 1937; Jones, 1926). Each researcher investigated specific aspects of prehension development. Jones (1926) was interested in when infants begin to use their thumbs, recognizing the importance of thumb movement to effective prehension. He found thumb opposition to be present in all infants by 9 months. Halverson examined visual control of prehension, approach or reach, and grasping patterns. He documented the emergence of visual attention and visually guided grasp. Halverson reported active thumb movement by 7 months and the beginning of fingertip grasp by 9 months. Castner (1932) was primarily interested in precision grasp of small objects (i.e., a

pellet). His study documented whole hand closure at 5 months, palmar grasp at 8 months, scissors grasp at 9 months, and pincer grasp at 12 months.

I NDIVIDUAL PATTERNS OF HAND SKILL DEVELOPMENT The design of these early studies of hand skill development was cross-sectional; and therefore identified what patterns infants demonstrate at specific ages, but not how infants develop these skills. The purpose of the first developmental studies was to document typical development, without realizing that infants’ individual differences might be more interesting and of equal importance to examine. To learn how infants develop and how developmental patterns differ among individual infants requires longitudinal designs in which performance patterns are observed over time. In assuming a hierarchy of central nervous maturation, the results in an invariant sequence of motor skills development and neuromaturational theory limited the thinking about how a child learns to act on the environment. Current research models (Gibson & Walker, 1984; Smith & Thelen, 2003; Thelen et al., 1993) reveal that infants follow a general sequence of motor milestones, but how they achieve skills is quite individual and infants’ developmental trajectories follow individual pathways. Beginning with Piaget (1952), researchers have demonstrated that children acquire skills through an interaction of their experience and their innate abilities. The influence of the environment on learning and development has become an emphasis of child development research. Behavior patterns are assumed to emerge from an organism– environment coaction (Gottlieb, 1992). This line of reasoning brought new understanding as to how coordinated movements develop, emphasizing the importance of sensory experience and feedback through the hand’s surfaces (Bushnell & Boudreau, 1993; Newell & MacDonald, 1997; Rochat, 1987; Ruff, 1984). For example, the first grasping patterns of neonates are driven by sensory input to the palmar surface. Throughout the first year infants’ actions directly relate to sensory experiences, and movements are adapted based on sensory feedback. Grasp and hold patterns, which are first associated with proprioceptivetactile input, become grasp and manipulate patterns guided by tactile, proprioceptive, and visual input (Bushnell, 1985; McCall, 1974).

HAND SKILLS E MERGE THROUGH THE I NTERACTION OF SYSTEMS Recent research of hand skill development (e.g., Bushnell & Boudreau, 1991; Newell & MacDonald,

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 119 1997; Thelen et al., 1993) has explored how infants’ actions and performance emerge from the interaction of many systems, both internal and external to the child. Factors that influence hand skills include the infant’s size, growth, biomechanical attributes, neurological maturation, perceptual abilities, sensation, and cognition (Gordon & Forssberg, 1997; Manoel & Connolly, 1998; Thelen, 1995; Thelen, Kelso, & Fogel, 1987). Within individual infants, these factors vary with time, activity, and environmental conditions. An infant’s actions during the performance of a task, then, are the results of the subsystems (e.g., motor, sensory, perceptual, skeletal, psychologic) interacting with each other and the environment. These individual systems are interdependent and work together, such that strengths in one system (e.g., visual) can support limitations in another (e.g., kinesthetic). Which systems are recruited for the tasks varies according to the novelty of the activity and the degree to which the task has become automatic. For example, reaching to pick up a cup initially is guided by the visual system, but after it is practiced and learned, reaching is guided primarily by the kinesthetic system, with some direction by the visual system. In contrast, grasping appears to initially involve primarily somatosensory input, but later also is guided by vision. Early grasping and manipulation patterns that are guided by visual and somatosensory input (e.g., play with a rattle) are later guided by cognition and memory (e.g., handwriting). The infant’s sensory–motor–biomechanical systems self organize in a coordinated way to achieve the infant’s goal. For example, when an infant reaches for the toy, grasps it, brings it to midline in hand-to-hand play, and then to the mouth, his attention is not on planning each of these actions. Instead, the infant is focused on assimilating the toy’s actions and perceptual features, organizing his or her movement around that goal. Therefore developmental outcomes reflect both an infant’s self organization and the opportunities in the environment.

Gibson (1988) defines early action as both exploratory (seeking information) and consequential (causing a consequence). The infant’s actions are based on affordances of the environment. Affordance defines the fit between the child and her environment (Gibson, 1979, Gibson, 1988). The environment and objects in it offer infants opportunities to explore and act. The infant’s performance is based on not only what the environment affords, but also her perceptual capability to recognize those affordances. For example, most infant toys provide opportunities for manipulation because they have movable parts, rounded surfaces, and easily fit into an infant’s hand. Individual finger movements, thumb opposition, hand-to-hand transfer, and eye–hand coordination are facilitated by the infant’s perception of the physical characteristics of the toy and his desire to explore those perceptual qualities. CaseSmith, Bigsby, and Clutter (1998) found that toys with movable parts afford higher-level skills than a cube or pellet. The movable parts provide a variety of surfaces for the infant to explore. The toy’s reciprocal action gives feedback to finger movements and sustains the infant’s attention. The perceptual-motor experience of a toy with movable parts is much more interesting than that of a cube (Figure 7-1). The first actions of the infant directly relate to his interest in acquiring perceptual and sensory information (infants first explore objects with their eyes and then hands). Through object manipulation, infants develop haptic perception (i.e., an understanding of objects’ shape, texture, and mass). Specific motor skills are necessary to develop haptic perception. Researchers (e.g., Bushnell & Boudreau, 1993; Lederman &

PERCEPTION AS A PRIMARY I NFLUENCE ON HAND SKILL DEVELOPMENT A first influence on the young infant’s action and movement is sensation. Through vision and touch the infant is motivated to explore his environment and objects within the environment. The infant’s perception of his environment informs action and then his action provides feedback about performance. Initially the infant’s goal is to explore the sensory attributes of objects (e.g., learn their shape, texture, and consistency) (Bushnell & Boudreau, 1993). Soon the infant also learns that his actions cause environmental consequences (e.g., shaking a toy makes a noise).

Figure 7-1 Movements are guided by object affordances. Toys with movable parts elicit a variety of grasping patterns.

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Klatzky, 1987) have demonstrated that young infants develop the hand skills that are necessary to explore an object’s sensory qualities. For example, infants’ first hand skills enable them to squeeze soft objects, run their fingers back and forth over textured objects, rotate, turn, and transfer objects with interesting shapes. Bushnell and Boudreau (1993) noted that infants learn to identify an object’s sensory qualities (e.g., texture, consistency, contour) only when they develop the motor skills to explore each different sensory quality. Therefore an infant does not accurately discriminate texture until she can explore texture by moving her fingers back and forth. She also cannot discriminate hardness until 6 months when she can tighten and lessen her grip while holding an object (Bushnell & Boudreau, 1991). Because configurable shape requires that two hands are involved in exploring the object’s surfaces, infants typically cannot accurately perceive shape until 12 months.

DEVELOPMENT OF HAND SKILLS FOR FUNCTIONAL OUTCOMES Once infants learn to discern the perceptual qualities of objects, they become interested in mastering objects for functional purposes. Through their exploration of objects and the environment, infants realize that they have an effect on the environment and their actions can produce functional outcomes. The outcomes that motivate an infant may be social (e.g., mother’s smile) or physical (e.g., a toy moves, makes a sound, falls over). Functional tasks and outcomes begin to organize the infant’s action (Gibson, 1988). Their actions are intentional and goal driven (Manoel & Connolly, 1998). With this interest in functional outcomes, the infant first attempts to use tools and relate objects to each other (Lockman, 2000). By the end of the first year, infants handle and manipulate objects according to their functional purpose, and the goal of accomplishing a task guides the interaction (Connolly & Dalgleish, 1989). One-year-old infants begin to use a spoon and a cup to self feed. Infants at 14 months can relate one object to another and use simple tools to achieve a goal. By 2 years they learn to hold a comb, a brush, and a marker and crudely apply them in appropriate tasks (Lockman, 2000; McCarty, Clifton, & Collard, 2001).

How Are Functional Hand Skills Learned? Infants generally go through three stages of learning to acquire a new skill (Box 7-1) (Gibson, 1988; Manoel & Connolly, 1998). The first stage involves exploratory activity. As noted in the previous section, the first year of life is primarily a period of sensory motor exploration. Through exploration, an infant learns about

BOX 7-1

Three Stages of Learning to Acquire a New Skill

1. Exploratory activity Learn about objects and tasks A variety of patterns and approaches tried Lower levels of skills used Focus on perceptual learning about the tasks to gain information 2. Perceptual learning and feedback acquired from previous tasks performed Actions initially tried and ineffective are discarded Continue to gain perceptual knowledge about the task Performance is variable, demonstrating higher and lower levels of skill 3. Discovery of the “optimal solution” by selecting the action pattern that will best achieve the goal Pattern selected is comfortable, efficient, and indicates increased self-organization Demonstrates flexible consistency in performance Tends to use a stable pattern for a task (e.g., stack blocks), but can easily adapt the pattern according to task’s requirement (e.g., with larger blocks, heavier blocks) High adaptability characterizes well-learned tasks Mature movement patterns are characterized by adaptable stability Synergist movements (muscles and joints working together) are softly assembled around the goal of the task Specific movement patterns are observed (e.g., a tripod grasp) Generalizes movement patterns to other tasks when well learned for one task

objects and tasks. Most skill acquisition begins with exploration, when a variety of patterns and approaches are tried. New challenges tend to elicit lower levels of skills because these more basic skills can be accessed easily and require less energy and effort than higherlevel skills (Gilfoyle et al., 1990). By using lower-level skills to explore a new task, the child can focus on perceptual learning about the tasks to gain information that will allow mastery with experience. In the second phase of learning a task, the infant uses the perceptual learning and feedback he acquired from attempting to perform the task. Actions that were initially tried and were ineffective are discarded. During this phase, the infant continues to gain perceptual knowledge about the task. Learning potential is high when the task is perceptually interesting and the skill demands are within the capability of the infant. At this transitional phase, the infant’s performance is variable in that he demonstrates higher and lower levels of skill. For example, Connolly and Dalgleish (1989) found considerable variability when infants first attempted to

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 121 use a spoon. McCarty, Clifton and Collard (1999) noted that the transitional stage for spoon feeding is between 14 and 19 months with an “optimal solution” emerging by 19 months. In the third phase of learning, an infant discovers the “optimal solution” by selecting the action pattern that will best achieve the goal. The pattern selected is comfortable and efficient and indicates increased selforganization. During this last stage of learning, the child demonstrates flexible consistency in performance. The infant tends to use a stable pattern for a task (e.g., stack blocks), but can easily adapt the pattern according to the task’s requirement (e.g., with larger blocks, heavier blocks). High adaptability characterizes a welllearned task and mature movement patterns are characterized by adaptable stability (Gordon & Forssberg, 1997; Thelen, 1995; Thelen et al., 1987). Synergistic movements (muscles and joints working together) are softly assembled around the goal of the task, allowing the infant to adapt the pattern he has learned when task variables change. Specific movement patterns are observed in most children, such as a tripod grasp; once a tripod grasp is well learned, it is easily adapted to pens and pencils of different sizes and weights. When movement patterns are well learned for one task and are performed with flexible adaptability, the infant also generalizes them to other tasks. McCarty and coworkers (2001) demonstrated that infants who learned to hold a spoon with a radial grasp consistently generalized this pattern to other tools and tasks with self-directed goals. By 14 months, the infants consistently used a radial grasp on tools that were selfdirected (e.g., a hairbrush), recognizing it as the most efficient grasp for using the tool. A century of research on infant motor development has provided a detailed description of the sequence of hand skills development and a conceptual understanding of how infants develop hand skills. Knowledge about the sequence allows therapists to identify infants who may benefit from intervention and to establish goals that reflect the next skill expected to emerge. The theories that explain how infants develop hand skills form the basis for intervention and educational approaches. One recurring theme in human development research, the relationship between skill development and environmental context, is discussed in the following section.

CONTEXTS FOR HAND SKILL DEVELOPMENT A child’s development is nested in his culture, family, and community; these contexts determine his genetic

makeup and after birth provide his learning environment. Children develop skills through participation in their family’s and community’s cultural practices. Cultural practices are the routine activities common to a community or people and reflect how they play, recreate, and interact in social occasions. The infant’s cultural, social, and physical contexts expand greatly through the first 2 years of life. The widening context affords the infant an increasing variety of experiences, challenges, and opportunities. In most cultures, the first 6 months of life are characterized by closeness to the caregiver. Often children are held and when they are positioned for play, they are immobile for all practical purposes. The infant is quite dependent at this point in life, not only to have his basic needs met, but to bring play objects within reach. In cultures with high interdependence and strong appreciation of extended family, the infant may be continually held by a variety of family caregivers beyond the parents. Hand skills may be practiced on the caregiver’s lap by reaching for and grasping hair, jewelry, or clothing items. First reach and grasp may be practiced on the mother’s breast. A family’s culture background influences the objects made available to the infant. In some cultures, toys are not valued or not available; as a result, young infants do not experience these learning objects. The contexts for play expand for infants after they gain mobility (e.g., around 8 months). Because the infant now can move to play objects, her sense of autonomy increases and she has increasing choice about play with objects. Once the infant is mobile, she is unlikely to spend play time on her parents’ lap and is more likely to play on the floor or in a seating device with the caregiver nearby. Being able to move to a location or object affords the infant greater variety of play objects, enables the infant to develop selfdeterminism, and expands the infant’s perception of form, space, direction, and depth. Cultural traditions influence how much the infant is held, the space afforded to him or her for exploration, and the complexity of the environment available. Infants of families with low economic status may not have appropriate spaces to explore and may be restricted for safety reasons. Families of cultures that value infants’ exploration and play may have more toys and activities available. The effect of poverty on motor skills development is equivocal. Peterson and Albers (2001) found that poverty had a small negative effect on motor development in girls. In contrast, boys whose families had lower income demonstrated higher motor skills than boys from more affluent families. Using a large sample of different ethnic and economic groups, Bradley and co-workers (2001) found that poverty per se did not have a negative effect on infants’ motor develop-

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ment; however, variables sometimes related to ethnicity and economic status (i.e., availability of learning materials and degree of parental responsiveness) did relate to motor development. A number of studies have found differences in hand skill development when children from different cultures are compared. In a study that examined motor performance in Chinese and American children, American children demonstrated higher scores in most gross motor skills and Chinese children were higher in fine motor skills (Chow, Henderson, & Barnett, 2001). The authors suggest that Chinese children may not have the same amount of space available for play and exploration and Chinese parents also may not value gross motor skill development as much as fine motor skill because early proficiency with chopsticks and writing implements is expected. Yim, Cho, and Lee (2003) found that hand strength of children in Korea was lower than in children from America and other Western countries. Although these studies of Chinese and Korean children examined older children (preschool and elementary ages), the results have implications for infants because hand skill and strength develop incrementally from infancy. Differences in caregiving practices across cultures appear to affect infant skill development. When evaluated using the Bayley Scales of Infant Development, 3- to 5-month old Brazilian infants were less skilled in grasping and sitting than American infants (Santos, Gabbard, & Goncalves, 2001). Santos and co-workers attributed these differences to the tradition that Brazilian mothers hold their infants almost constantly for the first 6 months. Because the infants are totally supported for an extended period, their delay in hand skill development may relate to delay in postural stability development. These studies illustrate differences that have been observed in different ethnic groups; however, these differences have not been systematically studied in ethnic groups that live in America, limiting generalizability to children of different cultures who live in the United States.

SYSTEMS THAT CONTRIBUTE TO THE DEVELOPMENT OF HAND SKILLS Extensive research has demonstrated the importance of posture and sensory function (i.e., visual, tactual, proprioceptive) to the development of hand skills (Bertenthal & von Hofsten, 1998; Thelen & Spencer, 1998; von Hofsten, 1986). The reciprocal influence of sensory function was discussed in a previous section.

This section presents a developmental perspective of the influence of posture and sensory functions.

POSTURE The first stable posture of the infant is lying on his back. Laying supine offers optimal stability; the infant must reach against gravity, which constrains reach with grasp. Because posture is unstable in the first months after birth, the 2-month-old infant primarily demonstrates asymmetric posturing, reinforced by the influence of the asymmetric tonic neck reflex (Gesell et al., 1940). This asymmetric posture limits his or her visual field and reinforces visual inspection of the hands (Bower, 1974). To reach and grasp objects, infants must maintain stable vision of the target as they lift their arms. Thelen and Spencer (1998) found that head control is critical to successful reaching. In their study reaching did not emerge in any of the infant participants until several weeks after good head control emerged. By 3 months, the infant has an emerging sense of midline, and when supine brings the head to midline and the hands toward midline. Symmetric weight bearing in prone and increasing head control contribute to establishing a sense of midline. Neck and shoulder stability develops as a prerequisite for control of reach and hand movements in space. Symmetry is the predominant characteristic of the infant’s posture between 4 and 6 months. Head and hands come to midline, enabling a hands-together posture and visual inspection of both hands. As a result, the infant spends much of the time in hand-to-hand play, first on the chest and then in space at the midline. Head and trunk control and postural stability change dramatically during this quartile. Thus the infant gains important axial support for reach and use of hands in space. Stability through the neck and shoulders helps the infant gain control of the arms; therefore in supported positions he or she can hold her hands in space while grasping an object. The movements of neck, trunk, and arms appear to be coordinated early in life. Van der Fits and Hadders-Algra (1998) found that complex postural adjustments accompany the infant’s reach by 4 months, when successful reaching emerges. Therefore as reach and grasp emerge and later mature, postural stability provides a base for these movements. By 6 months, the infant demonstrates increased postural control in the prone position, pushing onto extended hands and shifting weight side to side. When on elbows, the infant is able to lift one arm entirely from the weight-bearing surface for reach to an object. This complete lateral weight shift provides proprioceptive input through the hands across the palmar surface. It also results in asymmetric sensory experiences. Prone

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Figure 7-2

Prone position strengthens arms and hands.

Figure 7-4

Figure 7-3

Most 7-month-old infants sit independently.

positions help the infant strengthen arm and hand musculature and provide tactile proprioceptive information that appears important to the hand’s perceptual development (Boehme, 1988) (Figure 7-2). Although the increased postural control of the 6-month-old child supports symmetric movements of the hands in space, it does not appear adequate for skilled asymmetric or unilateral movements. In the following months, when trunk stability is sufficient for independent sitting, the infant develops an increased repertoire of arm and hand movements that includes both symmetric and asymmetric patterns. Gains in postural control allow the 7-month-old child to sit independently (Figure 7-3). In the next several months sitting becomes a favorite play position because the hands are free to hold objects, and the infant can control weight shift forward or to the sides to obtain objects (Figure 7-4).

Hands are freed to hold objects.

Increased axial control seems to support the use of one-hand reach and bimanual fingering (exploration) of an object held at midline. Trunk rotation has developed in fully supported positions (i.e., rolling from supine to prone and prone to supine) and begins to develop in sitting positions. Related to these skills, the infant demonstrates crossing the midline and begins to use the hand in crossed lateral space. In a review of the research literature, Bertenthal and von Hofsten (1998) reported that reaching skills significantly improve between 6 and 7 months of age. At this age, infants become highly accurate in reaching for a moving target, a task that requires rapid adjustments of arm movement and the postural stability to allow for those adjustments. Infants at 7 and 8 months also assume the quadruped position and begin to creep. The on-handsand-knees position results in frequent weight bearing on the hands. This position tends to be dynamic and mobile, thereby providing tactile and proprioceptive input across the hand (Figure 7-5). The frequency of play in prone position (in and out of quadruped) strengthens the arms and hands. The infant shifts weight across the hands in a diagonal direction while moving from quadruped to side sitting (Boehme, 1988). Strengthening of the arms also occurs through pulling to stand and through supporting himself while erect (Figure 7-6). Postural stability increases such that the 12-monthold infant has greater control of arms in space while sitting independently. The internal stability of the arm allows the infant to prehend a small object using a superior pincer grasp (i.e., use a pincer grasp without

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Figure 7-5 Creeping on hands and knees provides tactile and proprioceptive input to hands.

Weight-bearing experiences continue to provide heavy work for the upper extremities. Creeping usually is the primary form of mobility. The infant may rise into the hands-and-feet position (bear crawling), resulting in heavy work for the arms. Fast creeping over a variety of surfaces provides important tactual and proprioceptive input to the hands. By 13 months the child’s balance and postural stability are sufficient for upright ambulation. Trunk rotation and pelvic stability are noted in smooth transitions from floor sitting to standing and from standing to sitting. Postural control can now support hand manipulation with arms in space, as observed in stacking blocks, placing objects in a container, and toy exploration. Now that upright ambulation is the child’s consistent form of mobility, upper extremity weightbearing experiences become limited and the hands no longer are critical for support, resulting in increased emphasis on their role in manipulation. Postural control is excellent by 2 years as the child begins to concentrate on speed, strength, balance, and endurance. Postural stability of the child at 24 months enables use of hands with control in all positions and planes around the body. Although dexterity diminishes when the child is in a less stable position (e.g., half kneel), postural stability in typical sitting and standing positions is sufficient for control of a great range of manipulative skills.

SENSORY SYSTEMS

Figure 7-6 arms.

Practice of pull-to-stand helps to strengthen

stabilizing the arm on the surface). Postural stability is an important factor in the development of an accurate and well-directed reach (Corbetta & Thelen, 1996). With increasing trunk stability and rotation the infant is able to reach to the body’s contralateral side. Postural stability also enables the child to reach overhead and behind when sitting.

The sensory systems that most influence hand skill development are visual, tactile, and proprioceptive. By the third month the head is held at midline, which frees the range of vision. During this same period the infant learns to control eye movements, and visual inspection becomes a key strategy for learning about the environment. Visual attention to specific events and objects indicates the infant’s ability to focus and assimilate important information from the environment (Bower, 1974; White, Castle, & Held, 1964). Although visual attention becomes more discriminating (von Hofsten & Rosander, 1996), hand skills remain primitive in that the hand does not adapt to the specific sensory qualities of the object it grasps, and control of release has not been established (Figure 7-7). The infant from birth through 3 months is often prone lying and has frequent opportunities for tactile or proprioceptive input to the hands and forearms. He presses into a prone propped position with the head erect, resulting in deep proprioceptive input to the arms. Hand opening while weight bearing, prone-onelbows, provides specific tactile input to the palms. Mouthing of the hand allows tactile exploration of the hand and provides tactile or proprioceptive input to the

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Figure 7-7

Hands conform to the object’s shape

Figure 7-9 Infant at 4 months explores a toy with hands and eyes.

Figure 7-8 Hands grasp at midline on his chest in 3month-old infant.

hand. When the infant is supine, the hands find each other on the chest, clasping and engaging in mutual fingering (Figure 7-8). These tactile or proprioceptive experiences contribute to the development of grasp and release patterns, as do the visual experiences that contribute to the development of visually guided hand movements. Sensory experiences continue to be a primary basis for movement in the 3- to 6-month-old infant. The infant delights in the sensory world and begins to integrate the information from more than one sensory system. Rochat (1987) reported that infants this age perceive hardness when compared with soft consistencies. Bushnell and Boudreau (1993) concluded that infants as young as 3 months can perceive hardness,

size, and temperature. Mouthing and fingering behaviors increase significantly from 3 to 6 months, increasing an infant’s perceptual learning (Ruff, 1984) (Figure 7-9). Fingering behaviors are associated with visual inspection. At 4 and 5 months of age infants increasingly make successive oral and visual contacts with the object, thereby integrating information from two different sensory systems. Beginning at 5 and 6 months, infants use both hands to explore objects. They explore textures, rotate and transfer objects, and alternate looking with mouthing (Rochat, 1989). Ruff and Kohler (1978) demonstrated that after 6-monthold infants tactually explore objects, they tend to visually prefer those objects. Their results provide evidence that an infant visually recognizes an object that was previously held and tactually experienced but not visualized. Sensory play at this time consists of mouthing, hand-to-hand fingering, and intense visual inspection. The role of vision in guiding manipulation has an increasingly important role after 6 months and then throughout development (Bushnell & Boudreau, 1991). Whereas tactile input had primary influence on grasp and manipulation, vision becomes a primary sense for guiding the infant’s manipulation. McCall (1974) reported an increase in manipulation with visual regard at 81⁄2 months. Castner (1932) observed that the duration of regard increased at 8 and 9 months, as did the infant’s accuracy in reach and grasp of a pellet.

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Figure 7-10 Infant at 8 months integrates visual and tactile information from toy with movable parts.

Active mouthing decreases as manipulation with visual regard increases in the second half of the first year (McCall, 1974). This active mouthing appears to be replaced with fingering. The increasing importance of vision in manipulation complements rather than diminishes the importance of the tactile system. The infant is now able to integrate visual and tactile information, using both senses simultaneously to learn about the object’s properties (Corbetta & Mounoud, 1990; Ruff, 1984) (Figure 7-10). lntermodal transfer of tactile and visual information (visual recognition of an object after handling it without vision) becomes possible at this age (Ruff & Kohler, 1978; Steele & Pederson, 1977). Changes in discrimination of the object’s weight and shape enable the 9- to 10-monthold child to hold a cracker without crushing it and lift an object with the appropriate amount of force. At 12 months the infant continues to use vision as a primary guide to object manipulation. The infant can visually recognize the physical properties of the object and act on it appropriately. For example, a 12-monthold infant bangs and hits a rigid object and squeezes or presses a spongy object (Bushnell & Boudreau, 1993; Gibson & Walker, 1984). Fingering and hand-to-hand manipulation become the primary modes for exploring the sensory qualities of an object (Ruff, 1984) (Figure 7-11). Integration of senses continues and the infant becomes increasingly able to recognize objects visually that had been explored only through the tactile sense. Infants learn anticipatory control; that is, they plan their

Figure 7-11 object.

Infant at 12 months visually explores

movements after visualizing the object. Anticipatory control means that the infant opens his hand according to the object’s size and shape before prehension. Through their prehension experiences infants also begin to anticipate the force necessary to grasp and lift an object (Gordon & Forssberg, 1997; Johansson & Westling, 1988). In the second year of life, the infant becomes interested in the functional use of objects and functional goals become the prime motive for manipulation (Gibson, 1988). The child continues to integrate visual, tactile, and proprioceptive sensations by practicing perceptual motor skills, demonstrating increased abilities to use information from these sensory systems to correct and refine movements. Thus increased precision of movement results from increased perceptual ability, as well as improved motor skill. The child can now recognize the tactile and auditory properties of the object through visual inspection and therefore approaches an object with an appropriate response (i.e., shaking a rattle, squeezing a sponge, crumpling paper, or using more force to lift a large object). By 2 years of age, improved sensory discrimination and integration enable the child to demonstrate increased variety and control of perceptual-motor skills. The 24-month-old child is able to assimilate multimodal sensory information and make appropriate adaptive responses. Success in perceptual-motor skills such as stringing beads and simple dressing tasks illustrates the child’s ability to integrate and use sensory information.

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DEVELOPMENT OF HAND SKILLS IN THE CONTEXT OF INFANT PLAY ACTIVITIES PLAY ACTIVITIES: BIRTH TO 12 MONTHS In the first months of life, infants delight in sensory experiences of touch and movement. Infants exhibit frequent generalized movements through which they gather multisensory input that increases arousal and attention. Play behaviors of young infants include swiping movements to cause a mobile to move and make sounds, or mouthing objects in perceptual exploration. When general swiping movements cause a mobile to move and make sounds, this sensory experience reinforces that action and the infant swipes at the mobile again. As noted in the previous section, visual exploration, mouthing, and tactile reflexes appear to be the infant’s primary methods for learning about the environment (Bower, 1974; Gesell et al., 1940) (Figure 7-12). The 4- to 6-month-old infant continues to delight in the sensory experiences of vision, touch, and movement. One goal of generalized movements and reactions appears to be creating sensory experiences. As the infant scratches the weight-bearing surface of the parent’s shoulder, this behavior seems to be automatically reinforced by the tactile and proprioceptive

input to the hand. He or she begins to actively explore objects using specific movements to create sounds and visual effects. By 6 months the infant can purposely roll and initiate rolling to experience movement. Toys that react to simple movements are favorites in play. Rattles are good examples, in that almost any movement produces a sound, reinforcing the infant’s play and exploration (Piaget, 1952). Toys that are activated by generalized responses continue to be preferred to those that require specific, more localized responses; for example, a rattle is preferred to a busy box requiring differentiated push, pull, and press of fingers (McCall, 1974). From 6 to 12 months, infants spend most of their playtime in object exploration. Interest in and awareness of the environment increases (as described in the previous section). Visual and tactile exploration of objects predominates. These exploratory behaviors are characterized by a rich variety of manipulative skills. Cause and effect are well established, and rather than repeating the same actions on a toy, the infant tries new strategies to create different reactions (Piaget, 1952). Play involves imitation of actions observed, including toy manipulation. The physical properties of the object guide responses, because the infant does not yet understand the specific functional uses of objects. The infant begins to bang objects together and place one object in proximity to another. These behaviors signal the advent of tool usage and specific actions of one object in relation to another (Bruner, 1970; Lockman, 2000). In the first year, infants also engage in social play that is focused on attachment, or bonding, to the primary caregivers. Infants play social games with parents and others to elicit responses. These may involve pat-acake, squeezes, and kisses. Although infants at this age engage readily with individuals other than family, they require their parents’ presence as an emotional base and return to them for occasional emotional refueling before returning to play. Therefore an infant remains near to caregivers, who assist in opening containers, turning knobs, and providing physical assistance as the infant investigates his environment (Pierce, 1997).

PREHENSION: BIRTH TO 12 MONTHS The prehension skills that infants develop in their first year of life serve their play goals and enable them to explore and learn about the environment. As infants’ play transitions from sensory-driven to functional, hand skills refine from generalized to precise patterns.

Primitive and Transitional Grasps Figure 7-12 Mouthing at 4 months is a primary method of object exploration.

Newborns tightly flex their fingers around a flexed thumb, only occasionally opening the hand in association with active extension of the trunk or arms. The neonate’s fisted hand is consistent with the overall

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predominance of physiologic flexor tone that dominates upper- and lower-extremity movements. He or she frequently brings the fisted hand to the mouth when prone, pulling the hands toward midline while assuming an overall flexed position. The first reflexive response of the arm and hand, termed the traction response, is demonstrated by the neonate when proprioceptive input or traction is applied to the arm. When the arm is pulled away from the body, synergistic flexion of the fingers, wrist, elbow, and shoulder results. As described by Twitchell (1970), stretch to the flexor and adductor muscles of shoulder is a sufficient stimulus for eliciting this response. In the first couple of weeks of life, the grasp reflex has not yet emerged. The neonate may posture with fisted hands, but responses to touch on the hands result in opening or partial opening. It is not until the second to fourth week of life that the infant automatically closes the fingers around an object (or adult’s finger) placed in his palm. This first grasp reflex requires that pressure (proprioception), as well as tactile input be applied to the palm and is accompanied by the traction response. A grasping reflex is not elicited in response to a visual stimulus. By 4 weeks the grasp reflex can be elicited with a contact stimulus to the palm or fingers. A moving stimulus is most effective in producing this local grasp reaction, which is immediately followed by the traction response. By 8 weeks two distinct phases of the grasp reflex are observed. The first is the catching phase, which is an immediate flexion of the fingers and thumb. In the second or holding phase the finger flexion is sustained. This holding is intensified if the object is lightly pulled. The traction response declines at this time but can be elicited when the arm is pulled from the body (Twitchell, 1970). By 3 to 4 months of age a true grasp reflex has developed and the traction response no longer automatically accompanies this response, although dorsiflexion of the wrist continues to accompany the finger flexion. When an object is placed in the hand and is moved medially, the fingers flex in a sustaining grasp. A palmar grasp is observed with the fingers flexing tightly and pressing the object into the palm. Although in past research an ulnar palmar grasp was documented to emerge first, more recent research shows that the index finger is active first and has a leading role in the first grasping patterns (Lantz, Melen, & Forssberg, 1996). The grasp reflex becomes diminished at 4 to 5 months of age and fractionation of the grasp reflex begins (Twitchell, 1970). One or two fingers flex in isolation from the others, given specific stimulation of their volar surfaces. At 5 to 6 months an instinctive grasp emerges, which combines the fractionated grasp and the orienting response (Twitchell, 1970). At this time the

infant not only orients to the stimulus by adjusting his forearm but actually gropes for a tactile stimulus. Groping for the moving object that is touching the hand occurs without visual input and can be observed in the child who has visual impairment (Corbetta & Mounoud, 1990). Therefore instinctive grasp includes following a moving stimulus to secure it and then adjusting the hand’s grasp to accomplish sustained holding of the object. Flexion of a single digit can be induced given isolated tactile contact. The instinctive grasp is a transitional behavior between primitive (reflexive) and mature patterns of movement, as the fractionated movements of the fingers and hand come under the infant’s voluntary control (Gilfoyle et al., 1990).

Purposeful Grasp The transitional behaviors described previously lead to the emergence of voluntary prehension (Gilfoyle et al., 1990). Between 4 and 6 months the infant develops control of grasp (Figure 7-13). Using both tactile and visual information, she becomes skillful in adjusting the hand to the object. The infant begins to use visual input to prepare the hand for grasp by opening and shaping the hand before grasp according to the object’s size and shape (Corbetta & Mounoud, 1990; Forssberg, 1998). These beginning abilities to grasp, orient, and adjust the hand to objects based on tactile and visual information signify the beginning of purposeful grasp. The infant becomes capable of using a variety of grasping patterns that are selected based on the affordances of

Figure 7-13

Palmar grasp at 6 months.

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 129 the objects and his or her playful intentions. Initially the infant uses only a few grasping patterns and uses them indiscriminately. As the infant gains experience and matures, a variety of patterns can be observed. At 20 weeks most infants touch, but do not grasp, a cube placed before them. The infant who successfully secures the cube does so by pulling it to the other hand or the body and squeezing it against another surface. Squeeze grasp develops by 20 to 24 weeks. The infant presses the cube using total finger flexion against the palm. Because his or her proprioceptive system and motor control remain crudely developed, the cube is squeezed tightly. Success in retaining the object is limited by his or her ability to adjust the object within the hand or differentiate finger movement. The thumb does not actively participate in this grasp and tends to lie in the palmar plane. Finger and hand movements without object grasp contribute to the development of grasp (Castner, 1932; Halverson, 1931). The 4- to 5-month-old infant often is observed scratching the supporting surface when prone on elbows. The infant uses alternating finger flexion and extension of the digits together. Scratching also may occur on the caregiver’s clothing when holding the infant upright against the shoulder. The scratching motion allows the infant to practice the full range of reciprocal finger flexion and extension. Scratching also provides the infant with rich tactile information about different textural surfaces. Halverson (1931) observed rubbing of the hand on the surface as an additional method for obtaining tactile input in the infant at 16 to 28 weeks. As the infant continues to use scratching, finger movements become differentiated such that one or two fingers move in isolation of the others. Halverson documented pianoing or “raising and lowering of each finger alternately” on the table in infants 16 to 24 weeks of age. Pianoing appears to be an automatic movement rather than a purposeful isolated motion of each digit. As with other hand skills, isolated movements of the fingers occur first in these automatic behaviors elicited by the sensory stimulation of the hand resting on a flat surface. A palmar grasp is most frequently used by the 24-week-old infant. The palmar grasp is characterized by a pronated hand and flexion of all fingers around the object. The thumb may slide around the object passively rather than actively holding it (see Figure 7-13). Halverson suggested that when thumb opposition first appears at 28 weeks, it is used only in association with a palmar grasp. By 28 weeks the infant holds the object in a radial palmar grasp (Gesell & Amatruda, 1947) or what Halverson (1931) termed a superior palmar grasp. The radial fingers and thumb press the cube against the palm (Figure 7-14). Therefore when held in a

Figure 7-14

Radial palmar grasp.

supinated hand, the object can be brought to and put into the mouth. The object can be banged against another surface, and the object becomes accessible for object transfer from hand to hand. The radial palmar grasp is a hallmark in grasp maturation because the infant now differentiates the sides of the hand, using the ulnar side to provide stability for the grasping movement and the radial side to prehend and hold the object. This early pattern signifies the initial development of radial fingers as the skill side of the hand. Knobloch and Pasamanick (1974) emphasized the versatility observed in manipulation patterns at 7 months: “He grasps it, brings it to his mouth, withdraws it again for inspection, restores it again for mouthing, transfers it to the other hand, bangs it, contacts it with the free hand, retransfers it, mouths it again, drops it, rescues it, mouths it again” (p. 60). Between 32 and 36 weeks the infant demonstrates grasp of the object in the fingers rather than the palm, and by 36 weeks the infant exhibits a radial digital grasp (Gesell & Amatruda, 1947) or inferior forefinger grasp (Halverson, 1931) (Figure 7-15). At this time the infant can prehend a small object between the radial fingers and thumb. With the object held distally in the fingers (proximal to the finger pads), the infant can adjust the object within the hand and as a result can use the object for various purposes while holding it. The adjustments allow for greater success in relating two objects or in bringing the object to the mouth for finger feeding. The movement of the object distally and to the radial fingers gives the infant greater control of the object and enables release control. When the 36-week-old infant grasps a very small object (pellet size), a scissors grasp is used. Gesell and

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Part II • Development of Hand Skills surfaces, in and on other objects. He also can use the index finger to turn or move the object before prehension to increase success in grasp. Along with increased accuracy in grasp at this time, by 1 year the infant requires less time to prehend an object, displaces the object less before grasp, and makes fewer adjustments to secure the object firmly in the hand.

OBJECT RELEASE: BIRTH TO 12 MONTHS

Figure 7-15

Radial digital grasp at 8 months.

Object release matures after early grasping patterns are achieved. Release is an integral part of prehension and manipulation, but involves extensor movement patterns that follow a slightly different developmental trajectory.

Automatic Release

Figure 7-16

Scissors grasp at 9 months.

Amatruda, as edited by Knobloch and Pasamanick (1974), defined a scissors grasp as prehension of a small object between the thumb and lateral border of the index finger after a raking movement of the fingers. The hand is stabilized on a surface during this grasp, and the ulnar fingers are flexed to provide stability of the thumb and radial finger movement (Figure 7-16). Forefinger grasp (Halverson, 1931) or inferior pincer grasp (Gesell & Amatruda, 1947) is observed at 40 weeks. This is a fingertip grasp in which the infant stabilizes the forearm on the table as a base while grasping the cube. The fingers that prehend the small object are more extended than flexed. By 52 to 56 weeks the infant prehends and holds the object between the thumb and forefinger tip. Successful prehension using a superior pincer grasp (Halverson, 1931; Illingworth, 1991) is achieved without the forearm stabilizing on the surface. At this time the fingers adjust to the size and weight of the object. The object is now in a position that it can be used readily in a play activity or as a tool. Because the infant no longer needs to stabilize to grasp, he can easily prehend objects from a variety of

As with grasp, the first object release observed is a reflexive behavior. Finger extension is observed as the neonate withdraws and abducts the fingers in response to touch of the hand (Twitchell, 1970). This response, termed the avoiding reaction, is usually only a slight withdrawal of the neonate’s hand. By 3 weeks and continuing to about 8 weeks, the avoiding response is elicited easily. When the dorsum of the hand is touched, the fingers abduct and extend. The hand also may pronate to withdraw from a contact stimulus. This response is elicited when the contact stimulus is lighter and more quickly applied than the firm palmar stimulation that elicits the grasp reflex. Twitchell (1970) described an instinctive avoiding response that is similar in nature to the instinctive grasp response, in that it represents a transitional behavior between reflexive and voluntary responses. The instinctive avoiding response emerges between 12 and 20 weeks of age. It is characterized by pronation and adduction away from a stimulus on the hand’s ulnar border and supination with abduction to stimulation of the hand’s radial side. The instinctive avoiding reaction generally is fully developed by 24 to 40 weeks of age (Twitchell, 1965, 1970). At this time the infant withdraws from light contact stimulation, using a variety of hand movements, including flexion, extension, abduction, adduction, and rotation. Avoiding reactions are seen more frequently when the infant is irritable or when generalized tactile defensiveness is present. The avoiding response serves as an automatic mechanism to reinforce hand opening and facilitate finger extension to balance the effects of the grasp reflex. According to Gesell and Amatruda (1947), release requires inhibition of the flexor muscles with contraction of the extensors, which is a more mature, later-developing neuromotor pattern. More recent theories (Thelen et al., 1987, Thelen & Smith, 1994) that recognize the interaction of systems in development attribute initial hand opening to per-

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 131 ceptual and biomechanical influences. The hand may first open with wrist flexion, which produces tension of the finger extensors. The hand also may open to rub or pat objects to perceive their sensory qualities (Bushnell & Boudreau, 1993).

Purposeful Release From 5 to 6 months the infant begins a transition from reflexive to purposeful release. The infant demonstrates release accidentally or involuntarily in association with movements, tactile stimulation to the hand, or contact with another surface. At 6 months release is observed during mouthing and bimanual play. The infant brings an object or finger food to the mouth with both hands and may release one or both once the object is stabilized in the mouth. When the infant holds an object with two hands, one hand may fall from the object. Meanwhile, the infant practices finger extension in other activities. For example, extended fingers may be observed in patting the bottle or toy (Figure 7-17). Additional facilitation of finger extension in the 6- and 7-month-old child (see Figure 7-2) also occurs in the prone-on-hands position. At 28 weeks, the child releases an object when transferring it from one hand to the other. Initially object transfer is achieved by holding the object at midline with both hands and pulling it out of one hand into the other. Therefore the release is actually a forced withdrawal accomplished by the opposite hand. During this same developmental period the infant releases an object on a table surface or another resisting (Gesell & Amatruda, 1947) or assisting (Ammon & Etzel, 1977) surface. Release with the assistance of another surface enables the child to roll the object from the fingers or remove it from the hand by inhibiting finger flexion (i.e., without active extension). Between 40 and 44 weeks the infant demonstrates purposeful release in the context of play (Illingworth, 1991; Knobloch & Pasamanick, 1974). This first active

Figure 7-17

Fingers extend as infant pats toy.

release is often accomplished by flinging the object— combining elbow, wrist, and finger extension in a synergistic, ballistic movement. The infant now purposefully drops food and toys from his or her highchair and takes great pleasure in practicing this newfound skill. The object is released with the hand above the table surface, using full finger and thumb extension. Object-releasing activity is reinforced by the auditory and visual consequence of dropping the object. This new skill is also reinforced by the development of object permanence and the infant’s interest in observing objects disappear and reappear. By 52 weeks the infant demonstrates greater proficiency in releasing the object. With increasing control of finger extension, the infant begins to demonstrate graded hand opening when releasing. At this time she is practicing precision release for stacking one block on another or placing a form in its form space. Graded hand opening with controlled finger extension is first observed with the proximal hand base and forearm stabilized on a surface.

BIMANUAL SKILLS: BIRTH TO 12 MONTHS Humans are essentially bimanual beings from birth and most movement patterns of the arms and hands involve combined movements of both. Fagard and Jacquet (1996) indicated that bilateral arm movements are the predominant pattern of upper extremity movement throughout the first year of life. Two hand actions generally follow prehension and although varied, follow a developmental sequence. The sequence of bimanual skills observed during infancy relates to the infant’s postural, sensory, perceptual, and cognitive development, as well as hand skill development.

Early Development of Bilateral Arm Movements The neonate exhibits both asymmetric and symmetric limb movements. Some of these are associated with the asymmetric tonic neck reflex; many appear to be random. Smooth, alternating arm and leg movements are most characteristic, with specific reflexive behaviors elicited by specific tactile input. The first bimanual reach toward an object may be observed at 2 months (White et al., 1964), although swiping at objects tends to be unilateral. By 3 months swiping increases and hand-to-hand interplay, without an object, is observed with hands clasped on the chest (see Fig 7-8). The infant may involuntarily hold an object on the chest at midline, resulting from the clasping of the hands together. Most spontaneous arm and hand movements appear to be simultaneous and symmetric. At 16 weeks this symmetry continues to predominate, although one hand tends to lead the other. Usually the hands join together at midline, and the

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Figure 7-18

Symmetric arm movements at 4 months. Figure 7-19

object is held between them (Figure 7-18). Almost universally, once the object is prehended, the infant brings it to the mouth or chest. The object may drop when transported to the mouth or may be captured against a body part. These behaviors are reinforced by the infant’s drive toward symmetric midline movements at this age and the desire to experience oral sensation. Lack of internal trunk stability at 4 months also results in bringing both hands together around the object for distal stability. The 20-week-old infant tends to use the simultaneous approach described earlier, in which both hands move toward the object at the same time. The infant attempts to prehend the object using both hands (Castner, 1932). Although the 5-month-old infant reaches for the object with two hands, he uses only one to grasp the object (Fagard & Peze, 1997). The second hand may support the first after grasp is achieved, and often both hands bring the object to the mouth or hold it in space for visual inspection. Intermanual transfer has significantly increased (Rochat, 1989), although active purposeful release has not yet developed. Compared with 2- and 3-month-olds, 4- and 5-month-old infants demonstrate significantly better organized bimanual action with more holding and fingering of objects, The bilateral fingering behavior observed at this age has been described as grasping the object with one hand and touching it or scanning the object’s surface with the other (Ruff, 1984).

Transitional Bilateral Skills Between 24 and 28 weeks the infant approaches the cube most frequently with both hands, corralling it. During this developmental period first a simultaneous, then a successive bilateral approach is used. The infant

Unilateral approach to grasp object.

initiates movement in the second hand as the first hand ends its approach (Castner, 1932). Bilaterality versus unilaterality in approach seems to be determined by the object’s size and the way it is presented. The 7-month-old infant uses a bilateral approach for large objects and a unilateral approach for small objects (Fagard, 1998) (Figure 7-19). Other authors suggest that approach is determined by the external support provided for the infant’s proximal stability during reach (Bushnell, 1985; Halverson, 1931). After grasping the object, the infant visually inspects it or brings it to the mouth. She may transfer it using the mouth as a stabilizer. The 7-month-old infant uses primarily bilateral movements for object manipulation (Goldfield & Michel, 1986; Flament, as cited in Corbetta & Mounoud, 1990). At this time the infant demonstrates associated, rather than independent, bimanual movements. Although the two hands act in concert, an increasing variety of exploratory and manipulative behaviors are observed (Figure 7-20). For example, the infant uses an extended index finger to poke or probe an object held in the other hand. This probing with one hand while holding with the other is a primary method of object exploration. As mentioned, by 7 months the infant holds the object in the radial digits and actively transfers it from hand to hand, while visually and tactilely exploring it. Active supination and isolated wrist movements enable the infant to partially rotate or turn the object for visual inspection. These isolated movements often are mimicked by the other hand. Manipulation of the object at this time is limited to transfers from hand to

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 133

Figure 7-20 movements.

Two hands explore in associated bimanual

Figure 7-21 toys.

A 7-month-old infant continues to mouth

A

B

hand or hand to mouth rather than within hand manipulation. Mouthing remains an important part of the infant’s exploration (Figure 7-21). After 7 months of age, infants begin to play with two toys at a time (Figure 7-22). The infant bangs two objects together as the first indication of her capacity to associate objects (Corbetta & Mounoud, 1990). In the following weeks the infant adds to the repertoire of bilateral movements. In addition to visual inspection and hand-to-hand exchange, the infant waves toys in the air and bangs them on the table surface. By 9 months the striking change in manipula-

Figure 7-22 A, B. Infants can hold two objects simultaneously by 7 months.

tion is not related to the development of any specific skill, but to the expanded range of behaviors observed. Now one hand holds the object and the second hand manipulates the object. In “complementary bimanual activities,” one hand positions the object and the other manipulates parts of it (Bruner, 1970). Halverson (1931) noted that 9-month-olds “exhibited all of the following behaviors: transfer, visual inspection, release and regain, bang it on the table, and hold it with both hands.” By 9 months object rotation, primarily achieved by transferring from hand to hand, allows the infant to perceive the shapes of objects (Lederman &

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Klatzky, 1987). This type of rotation is possible because of increasing control of the radial digits and ability to grade supination and pronation as the object moves from hand to hand. This two-hand cooperation in turning an object is evidence of beginning dissociation of symmetric arm movements. Near the end of the first year a change is observed in the linkage between two-hand movement (Goldfield & Michel, 1986). Whereas 7-month-old infants move their hands in the same direction, 11-month-olds move them in complementary directions. This change marks the initiation of mature bimanual skills.

Coordinated Bimanual Skills At 12 months the infant demonstrates significant increases in both dexterity with one hand and cooperative use of two hands together. Ruff (1984) observed an increase in fingering by 12 months, which she associated with an increase in the infant’s ability to simultaneously assimilate tactile and visual information. The two hands begin to demonstrate coordinated asymmetric roles (Figure 7-23). These complementary movements are observed as the infant simultaneously holds two objects or an object and a container. A typical bilateral pattern at this time is for one hand to be active (generally the preferred hand) and one hand to be passive or to support and stabilize the object (e.g., one hand holds the container while the other removes a block inside). Bruner (1970) studied the success of infants in removing a toy from a toy box. He found that before 12 months infants are rarely successful in removing the object. Beginning at 12 months the hands work in cooperation; for example, one hand holds the bottle and the other unscrews the lid. These complementary functions are flexile and adaptable, enabling the hands to work together for functional

Figure 7-23 Play includes distinct yet complementary movement of each hand.

purposes. Flexible bimanual skills that can combine in numerous patterns, switching roles in a sequence of movements, develop in the second and third year as the child’s play repertoire expands.

PLAY ACTIVITIES: 12 TO 24 MONTHS The 1-year-old infant has developed an understanding of an object’s functional purpose, thereby attempting to use objects for the function for which they are intended. For the first time the infant’s repertoire of manipulative skills increases, in accordance with functional capabilities of the object more than its sensory qualities. The infant pushes a truck, pulls a toy dog on a string, lifts a telephone receiver to the ear, rolls a ball, and lifts a brush to the hair. All of these movements are based on emerging cognitive understandings, as functional play begins to predominate over sensory play. The child’s interest in relating two objects also results in more advanced unilateral and bilateral skills. Endless repetitions of putting objects in a container and placing one object next to another create interesting results for the infant and at the same time refine releasing skills. New skills in imitation are a basis for developing additional manipulation skills as the infant attempts new movements that he observes others perform. The child’s play between 18 and 24 months continues to focus on concrete, functional activities with toys. Play sequences increase in length and complexity. Symbolic play begins about the same time that language develops, between 16 and 20 months. At first the infant demonstrates self-play that is centered around or directed toward the self (Belsky & Most, 1981). The child’s play might consist of simulating eating, drinking, or sleeping. These self-directed actions signal the beginning of pretend play (Piaget, 1952). The child knows cause and effect and repeatedly makes the toy telephone ring or the battery-powered doll squeal to enjoy the effect of the initial action. By 2 years, the child’s symbolic play becomes directed to objects. This decentered play involves acting on dolls or teddy bears, feeding them, putting them to bed, combing their hair. The hand skills to perform such actions are complex and require that a series of related movements be linked together. These play activities are thus an integrated combination of bimanual skills, most of which require that one hand holds and the other acts on the object. By the end of the second year, play has expanded in two important ways. First, the child begins to combine actions into play sequences (e.g., he or she relates objects to each other by stacking one on the other or lining up toys beside each other). These combined actions show a play purpose that matches the various

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 135

Figure 7-24

Functional play with a toy car.

functions of the toy. Second, 2-year-old children now direct actions away from themselves. The objects used in play generally resemble real-life objects (Linder, 1993). The child places the doll in a toy bed and then covers it. The child pretends to feed a stuffed animal or drives toy cars through a toy garage. At 2 years of age, play remains a central occupation of the child, who now has an increased attention span and the ability to combine multiple actions in play. The emergence of symbolic or imaginary play with toys and objects offers the first opportunities for the child to practice the skills of daily living (Parham & Primeau, 1997; Reilly, 1974). As the infant learns more about the capabilities and affordances of objects, his play become more elaborate. His manipulation skills match his need to open and combine objects in novel ways, sometimes imitating parents and peers and sometimes experimenting with object properties. In general, the functional purpose of toys determines the toddler’s response: dialing the phone, turning the music box, unzipping a zipper, scribbling with a crayon, or pushing a car (Figure 7-24). With an increased interest in relating multiple objects, the child fills a container with small objects, places one object on or next to another, and scoops food with a spoon. These relational play activities often require stabilizing the toy or object with one hand while manipulating with the other. The child’s understanding of cause and effect and object permanence results in increased interest in switches, hinges, push buttons, and pop-up toys. Switches require elaboration of the prehensile patterns developed and new combinations of arm and hand movements. Most play activities now require bimanual skills, and the child is able to use hands together simultaneously or reciprocally (Corbetta & Mounoud, 1990) (Figure 7-25). The child engages in longer and more complex play sequences that

Figure 7-25 Blended mobility and stability and use of isolated finger movements.

Figure 7-26 Cup drinking as an example of coordinated hand movements for a functional goal.

require new combinations of hand skills. Pushing, pulling, probing, rotating, and turning are combined into a new repertoire of play behaviors (Nicholich, 1977). With new understanding of tool use, the child engages in play activities that require mobility of the proximal arm and stability of the hand for grasping the object (Exner, 2005). The functional use of some objects, such as a cup, requires a series of combined mobility and stability of the arm and hand (Figure 7-26). The functional play that characterizes the child at this age correlates with an increasing purposefulness

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Figure 7-27

Spoon feeding at 18 months.

in manipulation. Although the child continues to explore objects to learn their sensory properties, she also often “uses” objects for their specific function as part of a purposeful play activity. The 2-year-old child uses utensils with competency. He now has sufficient control of crayon or pencil grasp to make a vertical stroke. Most children insist on selffeeding at this stage. Although early attempts to spoon feed generally fail, the intent is clear. Self-feeding becomes more successful because the child does not turn the spoon as it enters the mouth (Figure 7-27). Spoon feeding and early drawing skills are made possible by integration of sensory and perceptual information into blended patterns of mobility and stability. With improved perceptual-motor integration, the child imitates a circular stroke, matches a form to a form space, holds an object with appropriate pressure, places and releases an object with accuracy, and demonstrates beginning eye–hand coordination in ball play. All of these skills indicate an increased ability to integrate sensory experience and make accurate motor responses or adaptations to those sensory inputs (Connolly & Dalgleish, 1989).

PREHENSION: 12 TO 24 MONTHS By 60 weeks prehension is deft and precise. The child plans and uses grasping patterns that enable him or her to act on the object after prehension (Gesell & Amatruda, 1947). Fingertip grasp is used unless the object is large and heavy or the situation is stressful for the child (e.g., being off balance or hurried). The hand is sufficiently differentiated to hold two cubes in one hand (Knobloch & Pasamanick, 1974). The child can

move different parts of the hand (i.e., the radial and ulnar sides) independently and can control the action of isolated fingers. Gesell described the grasp of an 18-month-old child as enveloping rather than manipulative. At this age thumb opposition is good; however, the hand remains primarily a prehender rather than a manipulator. Exploration of the object requires both hands and involves transferring and turning the object from one hand to the other. At this time the infant is able to adjust grasp to accommodate the weight and shape of the object (Gordon & Forssberg, 1997). This enables holding a cracker without crushing it. The infant has increasing ability to differentiate the pressure used in finger flexion, indicating increased tactile and proprioceptive discrimination in addition to greater motor control. The 24-month-old child demonstrates increasing dissociation of the fingers, strength and control of the hand’s arches, and sensitivity to the tactual properties of the object. These underlying hand skills enable the child to perform a great variety of functional skills (e.g., self-feeding, using a spoon, scribbling with a crayon, building a tower of three cubes, and turning pages of a book). Practice of these skills leads to emergence of the pretend play sequences that dominate by 3 and 4 years.

OBJECT RELEASE: 12 TO 24 MONTHS The need to stabilize a proximal hand or arm part on a surface to accomplish controlled release (e.g., release cubes in a cup) continues through 18 months. In particular, more precise release (e.g., of a small object) requires the support of a stabilizing surface (Knobloch & Pasamanick, 1974). Release of a cube in building a three-cube tower is practiced, and, although generally successful, alignment of the cubes is imprecise. Typically, when stacking cubes or small blocks, the infant extends the fingers all at one time, using more extension than is necessary to actually release the object. The infant’s release is graded rather than abrupt, and small wrist, forearm, and finger movements are used to adjust the positions of the cubes one on the other. Visual inspection during release increases, such that the hand can accurately place a cube or puzzle piece. Perhaps the most important contribution to the infant’s ability to place one object on another is internal stability of the arm while it is held in space, which allows the hands to act independently. By the end of the second year the child has welldeveloped internal proximal stability and smooth graded or incremental release patterns. He can open the hand partially while carefully monitoring whether the object is correctly placed. Therefore the infant is

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 137 now able to adapt and adjust the hand opening according to the size, shape, and weight of the object. Controlled release in the 2-year-old child enables him to fit puzzle pieces into their form space, place small objects in a container, turn pages of a book, stack blocks, and manage a cup and feeding utensils. He can construct a six-cube tower by precisely centering each cube and slowly releasing it, using gradual extension of his fingers. Object release continues to develop over the next 3 years with significant increases in steadiness, precision, dexterity, and speed.

BIMANUAL SKILLS: 12 TO 24 MONTHS From 12 to 24 months the infant develops greater control of bimanual skills with increasing complexity and integration of motor patterns. Speed, accuracy, and dexterity increase. Proximal arm movements become dissociated from distal arm movements such that the infant can hold the hands in space to manipulate objects. He or she also can demonstrate controlled arm movement while maintaining grasp of an object (Exner, 2005). Many of the child’s activities involve one hand manipulating and the other stabilizing the object. For example, the child begins to spoon feed while holding the bowl, scribble with a marker while holding the paper, bang with a toy hammer while stabilizing the target toy. Between 18 months and 2 years the child learns a variety of bimanual skills that require control of simultaneous hand movements involving blended combinations of alternating stability and mobility (Gilfoyle et al., 1990). Stringing beads, pulling off shoes, and unwrapping a piece of candy are examples of skills in the repertoire of the 2-year-old that involve a sequence of bimanual movements in which the child simultaneously controls arm and hand stabilization and movement (Knobloch & Pasamanick, 1974). These bimanual movements can be asymmetric and dissociated when the activity requires that two hands act together in different movements. Two-handed simultaneous movement also represents a developmental step from the earlier pattern of one hand manipulating and the other stabilizing. Cooperative and complementary bimanual movements continue to be added to the child’s repertoire of fine motor skills throughout the

first decade of life. The complexity, speed, accuracy, and precision of the skills increase with experience, cognitive development, and neuromotor maturation. Table 7-1 presents the developmental sequence of grasp, release, and bimanual skills. Although the developmental ages for the listed skills vary, the sequence of development tends to remain consistent across children; therefore the months listed are estimated ages when the described skills are achieved.

SUMMARY The child’s play and the hand skills that enable that play undergo tremendous developmental changes in the first 2 years of life. Exploratory play skills evolve from generalized movements that gather comprehensive sensory input to specific exploration of the sensory qualities of objects. After the first year of life, infants exhibit functional play skills in which objects are used as means toward a functional goal. Infants learn to use tools as evidence of their expanding knowledge about how objects relate and how tools can serve functional goals. As play skills mature, the infant’s crude prehension patterns become precise grasping patterns that enable skillful manipulation of objects. The child holds objects first in the palm, then in the fingers, and finally in the fingertips. As she holds objects more distally, coordination of two hands together evolves, enabling the child to achieve greater competence and skill in play and interaction within the environment. This chapter described how hand skills evolve from reflexive, stereotypical patterns into precise, well-controlled prehension and manipulation patterns. Current research has investigated how the infant develops hand skills. Posture, sensory functions, and perception appear to have essential roles in hand skill development. The activities and environments that surround the infant afford a multitude of manipulation opportunities. Current explanatory models explain how hand skills develop and elucidate what variables influence an infant’s developmental trajectory. These models emphasize the influence of contextual elements in addition to biological foundations and have application in early childhood intervention and education.

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Table 7-1

Development of grasp, release, and bimanual skills: birth through 24 months

Approximate Age

Grasp

Release

Bimanual Skill

Neonate

Traction response

Avoiding reaction: hand opens with tactile stimulus to hand’s dorsum

Smooth, alternating arm movements; reflexive arm responses to proprioceptive and tactile input

1 months

Grasp reflex: local grasp reaction, followed by traction response

Avoiding reactions continue

Asymmetry of arm reaction; reflexive arm responses to proprioceptive and tactile input

2 months

Grasp reflex: catch and holding phases Instinctive avoiding response; pronation and adduction from stimulus on ulnar side, supination, abduction from stimulus on radial side

Hands held together on chest, usually without object; symmetric, simultaneous arm movement

3 months

4 months

True grasp reflex; primitive squeeze of fingers; diminished traction response; orienting response

Instinctive avoiding reactions continue; variety of hand movements used to avoid touch contact

Objects held with both hands at midline; symmetric, midline movements

5 months

Instinctive grasp; squeeze grasp, gropes for tactile stimulus; adjusts hand to object

Release involuntary or accidental

Two-hand reach, with unilateral prehension; object transfer, hand to hand; bilateral holding and fingering

6 months

Palmar grasp; pronated hand and flexion of all fingers; adjusts hand using visual and tactile information

Object accidentally released in mouthing or bimanual play

Simultaneous, symmetric, bilateral approach with bimanual or unilateral prehension

7 months

Radial palmar grasp; superior palmar grasp; differentiation of ulnar and radial sides stable; radial fingers hold object

Purposeful release; transfer of object from one hand to the other; release against a resisting surface

Successive bilateral approach with unilateral prehension; bilateral object manipulation; associated bimanual movements

8 months

Radial digital grasp; inferior forefinger grasp; object held proximal to finger pads; ulnar side stable and radial fingers hold object

Purposeful release with assistance or resistance against a surface

Continued

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 139

Table 7-1

Cont’d

Approximate Age

Grasp

9 months

Scissors grasp; able to hold small objects

10 months

Forefinger grasp; tip of thumb and forefinger used in grasp; grasping accuracy without stabilization

Release

Bimanual Skill Object rotation by transferring it hand to hand; plays with two toys, one in each hand, banging together; dissociation of symmetric arm movement

Active release; flinging of object by combining elbow, wrist, and finger extension; object release above surface

11 months

Complementary and cooperative bimanual movement

12 months

Superior pincer grasp; tip of thumb and forefinger used in grasp; grasping accuracy without stabilization

Beginning of controlled release; remains imprecise

Coordinated, asymmetric movements; one hand stabilizes and one hand manipulates

15 months

Deft and precise grasp; a variety of grasps used

Controlled release; increasing control when releasing

Beginning of two-hand tool use; continues pattern of one hand stabilizing and one manipulating

18 months

Increasing dissociation, strength, and perception enable child to use tools and manipulate objects

Controlled release, increasing accuracy with limited precision of placement; tends to extend fingers all at one time

Asymmetric, dissociated bimanual skills; blended stability and mobility; alternating sequences of two-hand movements

Greater precision and control of release; adjustment of hand opening according to object’s size and shape

Increasing competence in two-hand tool use; increasing complexity in movement patterns; cooperation of two hands

24 months

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Exner C (2005). The development of hand skills. In J CaseSmith (editor): Occupational therapy for children, 5th ed. (pp. 304–355). St Louis, Mosby. Fagard J (1998). Changes in grasping skills and the emergence of bimanual coordination during the first year of life. In DJ Connolly (editor): The psychobiology of the hand (pp. 123–143). Cambridge, UK, Cambridge University Press. Fagard J, Jacquet AY (1996). Changes in reaching and grasping objects of different size between 7 and 13 months of age. British Journal of Developmental Psychology, 14:65–78 Fagard J, Peze A (1997). Age changes in interlimb coupling and the development of bimanual coordination. Journal of Motor Behavior, 29:199–208. Forssberg H (1998). The neurophysiology of manual skills development. In KJ Connolly (editor): The psychobiology of the hand (pp. 123–141). Cambridge, UK, Cambridge University Press. Gesell A (1928). Infancy and human growth. New York, Macmillan. Gesell A, Amatruda CS (1947). Developmental diagnosis. New York, Harper & Row. Gesell A, Halverson HM, Thompson H, Ilg PL, Castner BM, Ames LB, Amatruda CS (1940). The first five years of life. New York, Harper & Brothers. Gibson EJ (1988). Exploratory behavior in the development of perceiving, acting, and the acquiring of knowledge. Annual Review of Psychology, 39:1–41. Gibson EJ, Walker AS (1984). Development of knowledge of visual-tactual affordance of substance. Child Development, 55:453–460. Gibson JJ (1979). The ecological approach to visual perception. Boston, Houghton-Mifflin. Gilfoyle E, Grady A, Moore J (1990). Children adapt, 2nd ed. Thorofare, NJ, Slack. Goldfield EC, Michel GP (1986). The ontogeny of infant bimanual reaching during the first year. Infant Behavior and Development, 9:81–89. Gordon AM, Forssberg H (1997). Development of neural mechanisms underlying grasping in children. In KJ Connolly, H Forssberg (editors): Neurophysiology and neuropsychology of motor development (pp. 214–231). London, MacKeith Press. Gottlieb G (1992). Individual development and evolution: The genesis of novel behavior. New York, Oxford University Press. Halverson HM (1931). An experimental study of prehension in infants by means of systematic cinema records. Genetic Psychology Monographs, 10:107–286. Halverson HM (1932). A further study of grasping. Journal of General Psychology, 7:34–63. Halverson HM (1937). Studies of the grasping responses of early infancy. Journal of Genetic Psychology, 51:371–449. Illingworth RS (1991). The normal child: Some problems of the early years and their treatment, 10th ed. Edinburgh, Churchill Livingstone. Johansson RS, Westling G (1988). Coordinate isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Experimental Brain Research, 71:59–71. Jones MC (1926). The development of early patterns in young children. Pedagogical Seminar, 33:537-585.

Hand Skill Development in the Context of Infants’ Play: Birth to 2 Years • 141 Knobloch H, Pasamanick B (1974). Gesell and Amatruda’s developmental diagnosis: The evaluation and management of normal and abnormal neuropsychologic development in infancy and early childhood. Hagerstown, MD, Harper & Row. Lantz C, Melen K, Forssberg H (1996). Early infant grasping involves radial finger. Developmental Medicine and Child Neurology, 38:668–674. Lederman SJ, Klatzky RL (1987). Hand movements: A window into haptic object recognition. Cognitive Psychology, 19:342–368. Linder T (1993). Transdisciplinary play-based assessment. Baltimore, Brooks. Lockman JJ (2000). A perception-action perspective on tool use development. Child Development, 71:137–144. Manoel EJ, Connolly KJ (1998). The development of manual dexterity in young children. In KJ Connolly (editor): The psychobiology of the hand (pp. 177–198). Cambridge, UK, Cambridge University Press. London, MacKeith Press McCall RB (1974). Exploratory manipulation and play in the human infant. Monographs of the Society for Research in Child Development, 39:155. McCarty ME, Clifton RK, Collard RR (1999). Problem solving in infancy: The emergence of an action plan. Developmental Psychology, 35:1091–1101. McCarty ME, Clifton RK, Collard RR (2001). The beginnings of tool use by infants and toddlers. Infancy, 2(2):233–256. McGraw MB (1943). The neuromuscular maturation of the human infant. New York, Columbia University Press. Newell KM, MacDonald PV (1997). The development of grip patterns in infancy. In KJ Connolly, H Forssberg (editors): Neurophysiology and neuropsychology of motor development (pp. 232–256). Cambridge, UK, Cambridge University Press. Nicholich L (1977). Beyond sensorimotor intelligence: Assessment of symbolic maturity through analysis of pretend play. Merrill-Palmer Quarterly, 23:89–102. Parham D, Primeau L (1997). Play and occupational therapy. In D Parham, L Fazio (editors): Play in occupational therapy for children (pp. 2–22). St Louis, Mosby. Peterson SM, Albers AB (2001). Effects of poverty and maternal depression on early child development. Child Development, 72:1794–1813. Piaget J (1952). The origins of intelligence in children. New York, Norton. Pierce D (1997). The power of object play for infants and toddlers at risk for developmental delays. In D Parham, L Fazio (editors): Play in occupational therapy for children (pp. 86–111). St Louis, Mosby. Reilly M (1974). Play as exploratory learning. Beverly Hills, Sage. Rochat P (1987). Mouthing and grasping in neonates: Evidence for the early detection of what hard or soft substances afford for action. Infant Behavior and Development, 10:435–449. Rochat P (1989). Object manipulation and exploration in 2- to 5-month-old infants. Developmental Psychology, 25(6):871–884.

Ruff HA (1984). Infants’ manipulative exploration of objects: Effects of age and object characteristics. Developmental Psychology, 20:9–20. Ruff HA (1989). The infant’s use of visual and haptic information in the perception and recognition of objects. Canadian Journal of Psychology, 43:302–319. Ruff HA, Kohler CJ (1978). Tactual-visual transfer in sixmonth-old infants. Infant Behavior and Development, 1:259–264. Santos DC, Gabbard C, Goncalves VM (2001). Motor development during the first year: A comparative study. Journal of Genetic Psychology, 162(2):143–153. Shirley MM (1931). The first two years: A study of twenty five babies, vol. 1. Locomotor development. Minneapolis, University of Minnesota Press. Smith LB, Thelen E (2003). Development as a dynamic system. Trends in Cognitive Science, 7:343–348. Steele D, Pederson DR (1977). Stimulus variables which affect the concordance of visual and manipulative exploration in six-month-old infants. Child Development, 48:104–111. Thelen E (1995). Motor development: A new synthesis. American Psychologist, 50(2):79–95. Thelen E, Corbetta D, Kamm K, Spencer JP, Schneider K, Zernicke RF (1993). The transition to reaching: mapping intention and intrinsic dynamics. Child Development, 64:1058–1098. Thelen E, Kelso JAS, Fogel A (1987). Self organizing systems and infant motor development. Developmental Review, 7:39–65. Thelen E, Smith LB (1994). A dynamic systems approach to the development of cognition and action. Cambridge, MA, MIT Press. Thelen E, Spencer JP (1998). Postural control during reaching in young infants: a dynamic systems approach. Neuroscience and Biobehavioral Reviews, 22:507–514. Twitchell TE (1965). Normal motor development. Journal of the American Physical Therapy Association, 45:419–423. Twitchell TE (1970). Reflex mechanisms and the development of prehension. In K Connolly (editor): Mechanisms of motor skill development. London, Academic Press. Van der Fits IBM, Hadders-Algra M (1998). The development of postural response patterns during reaching in healthy infants. Neuroscience and Biobehavioral Reviews, 22:75–85. von Hofsten C (1986). The emergence of manual skills. In MG Wade, HTA Whiting (editors): Motor development in children: Aspects of coordination and control (pp. 167–185). Boston, Martinus Nijhoff. von Hofsten C, Rosander K (1996). The development of gaze control and predictive tracking in young infants. Vision Research, 36:81–96. White BL, Castle P, Held R (1964). Observations on the development of visually directed reaching. Child Development, 35:349–364. Yim SY, Cho JR, Lee IY (2003). Normative data and development characteristics of hand function for elementary school children in Suwon Area of Korea: Grip, pinch and dexterity study. Journal of Korean Medical Science, 18:552–558.

Chapter

8

OBJECT MANIPULATION IN INFANTS AND CHILDREN Charlane Pehoski

CHAPTER OUTLINE OBJECT MANIPULATION DURING INFANCY Movements Used in Object Exploration by Infants Exploratory Nature of Infant Object Manipulation Object Exploration by the Mouth and Hand Role of Vision in Infant Object Manipulation Handling Multiple Objects Summary and Therapeutic Implications OBJECT MANIPULATION DURING THE TODDLER YEARS Beginning of In-Hand Manipulation Control over Object Release Complementary Two-Hand Use Summary and Therapeutic Implications OBJECT MANIPULATION IN THE PRESCHOOL AND EARLY CHILDHOOD YEARS Studies of In-Hand Manipulation Role of Variability in Motor Skill Development Factors Contributing to the Improvement of In-Hand Manipulation Skills Summary and Therapeutic Implications OBJECT MANIPULATION IN OLDER CHILDREN SUMMARY

The hand is a wonderful tool that has the exploration and manipulation of objects as its primary purpose. The development of the hand in the service of object manipulation follows a long course. It is one of the ways

children experience success and the perception of competence. Bruner (1973) pointed out that competence includes not only social interaction but also mastery over objects. The theme of this chapter is how the child gradually gains control over the hand to manipulate objects. Infancy appears to be a time when reach is perfected and the basic grasp patterns are developed. At first the infant can manipulate objects only by grasping the object, waving the arm, and moving the wrist because the object is held in a power grip that fixes it in the hand (Napier, 1956). Gaining the ability to transfer an object hand to hand greatly expands the actions the infant can produce with the object, but it is the appearance of a precision grip (pad of radial fingers to pad of thumb) that marks a major change in the eventual skills of the hand. Landsmeer (1962) indicated that the purpose of a precision grip is to “operate the object with precision by means of the fingers.” The perfection of this skill covers a long developmental period. Voluntary release (e.g., releasing an object in a predetermined place) also develops in late infancy and is an important component to skilled object interaction. Like object release, many of the basic components for skilled hand use are seen during infancy, but their perfection takes many years. As an example, the child must learn to control the release of an object so he or she can place it with skill and accuracy. In-hand manipulation skills, or the movement of an object in the hand after grasp, are yet to be acquired, and although the infant has the rudiments of two-hand use, the ability to plan the movements of both hands at the same time is not yet present. This chapter discusses what is known about the development of these components. There are many gaps in our understanding of these changes and how they might impact on the child’s gradual mastery of the

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physical world. Given the importance of object manipulation to human behavior, it is interesting that so little study has been done on this motor skill. In looking at what has been written, we divided the children into four age groups: infancy (neonate to 12 months old), toddler (1 to 2 years old), preschool/ early childhood (3 to 6 years old), and the older child. In addition, themes that might help us understand the direction skilled hand use is taking at each of these stages are explored. One last note: The hand is the tool of the mind. It is the mind that directs and guides the hand in the context of the child’s environment and culture. Object exploration or manipulation is the result of our desire to master the physical world. In infancy the basic drive to explore the world is present and, although the infant’s physical skills are limited, these skills are used to gain information about object properties. It is probable that this drive sets the stage for all future object exploration and the continued drive toward mastery.

OBJECT MANIPULATION DURING INFANCY Manipulation implies that the movement of the object is done to achieve some purpose or goal; that is, that the individual is consciously engaged in the activity and directing the action. By this definition, there was a time when researchers would not have considered studying object “manipulation” in the very young infant. Neonates and young infants were considered to be primitive beings dominated by reflexes that would gradually be integrated so the infant could engage the world. More recent research has been guided by the belief that infants are born curious and with a drive to explore their universe (although admittedly within the limitations of their physical capabilities). As an example, if properly supported and alert, neonates reach toward a visually captured object (Bower, Broughton, & Moore, 1970; von Hofsten, 1982). Although this behavior has been termed prereaching (Trevarthen, 1974) or prefunctional (von Hofsten, 1982), it is voluntary and has purposefulness not seen in more reflexive behaviors.

MOVEMENTS USED IN OBJECT EXPLORATION BY I NFANTS Humans are born with the drive to reach out and explore the physical world. Even as a neonate, the infant uses primitive motor skills to begin this process. Based on the observation of infants from 1 month to about 10 to 12 months of age, Karniol (1989) proposed 10 stages in the early object exploration of the infant

BOX 8-1

Ten Stages in the Development of Object Manipulation in Infancy

ONE TO THREE MONTHS Stage 1: Rotation: An object is moved by twists of the wrist. Stage 2: Translation: There are movements of the arm that change the location of an object by increasing or decreasing the distance from self. Stage 3: Vibration: There are repeated, rapid bending motions of the arm as the object is held. THREE TO FOUR MONTHS Stage 4: Bilateral Hold: The object is held passively in one hand as the other hand holds or does something else to another object. Stage 5: Two-handed Hold: A single object is held with both hands. Stage 6: Hand-to-Hand Transfer: An object held in one hand is transferred to the other. FIVE MONTHS Stage 7: There is coordinated action with single object: One hand holds the object stationary and the other hand does something to it (e.g., strokes a doll or pulls at the hair). SIX TO NINE MONTHS Stage 8: There is coordinated action with two objects: Manipulation of two objects, each held in a separate hand, such as hitting two blocks together. Stage 9: Deformations: The object is made to change shape, such as tearing paper or pressing a toy to make a sound. Stage 10: Instrumental Sequential Actions: There is the sequential use of two hands in obtaining a goal, as demonstrated when the infant lifts a cup to obtain a cube. Data from Kamiol R (1989). The role of manual manipulative stages in the infant’s acquisition of perceived control over objects. Developmental Review, 9:222–225.

(Box 8-1). Three of these stages—rotation, translation, and vibration—were related to the young infant less than 4 months old. If an object was placed in the hand of a 2- to 3-month-old infant, the earliest engagement Karniol noted was that the infant would rotate or twist the wrist, but only if the object happened to be visible to the infant. If the hand was not visible, the object was dropped. The next actions seen were translation movements, or a deliberate effort to change the location of an object by moving the arm toward or away from the body. Often this involved bringing an object to the mouth or was combined with rotation. Karniol believes that these movements assist the infant in combining changes in the retinal image of the object with proprioceptive feedback from the arm. The third method of engagement that Karniol observed in the very young

Object Manipulation in Infants and Children • 145 infant was a movement she called vibration. She defined this as rapid, periodic movements of an object by repeated bending of the arm. If the object produced noise, the motion might be maintained or be more vigorous. If the object did not make noise, it might be translated, rotated, and visually examined before being dropped. Consequently it appears that the very young infant will manipulate objects if they are placed in the hand, but this manipulation is limited to movements of the arm and wrist. As we will discuss later, grasp itself can also provide information about object properties to even very young infants. Young infants also may use their feet for exploration. Galloway and Thelen (2003) found that when infants about 3 to 4 months old were given an opportunity to contact a suspended toy with either their feet or their hands, the infants were able to make contact with their feet at about 12 weeks of age and with their hands at about 16 weeks of age. Reach is becoming functional at 4 months of age; the 4-month-old infant can also bring both hands together to engage the object at midline. This ability expands the action that can be taken on objects and is a necessary first stage of “complementary two-hand use” (Bruner, 1970). Midline behavior is facilitated by changes in the general control of the arm and the body itself. There is better balance in the trunk, as well as neck flexors and extensors, so the head is held in midline and the child can tuck the chin to better observe the hands. By 4 months the child can also lie on his or her back and bring the hands together up into the space above the body (Bly, 1994). This ability to bring the two hands together is used by the infant in exploring objects. At 3 to 4 months, Karniol (1989) adds bilateral hold and two-handed hold to the list of options available to the infant; that is, the infant can hold an object while the other hand does something else or hold the object using two hands. In a study of the object manipulation and exploration of 2-, 3-, 4-, and 5-month-old infants, Rochat (1989) saw an increase in mouthing in the 4to 5-month-old infants over the 2- to 3-month-old infants, a behavior he found significantly associated with two-handed grasp. Therefore two-hand support for an object may assist the infant’s attempts to mouth objects, increasing the likelihood that this form of exploration will occur (Figure 8-1). Once midline engagement of the hands is developed, manipulation also is assisted by allowing one hand to hold and the other to explore the surface of the object with the fingers. Rochat (1989) also saw an increase in this fingering behavior in his 4-month-old subjects. Further object exploration is possible around 5 to 6 months of age, when the infant is able to transfer an object hand to hand. This is an important comple-

Figure 8-1 Mouthing of objects is assisted once an infant is able to use two hands to support the object (4-month-old infant).

mentary two-hand use stage. Karniol (1989) indicated that, when this action is first seen, the infant often rotates the wrist and bends the arm with the object in one hand and then transfers it to the other hand and repeats the action. In recording the infant’s exploratory actions during a 90-second segment with a toy, Rochat (1989) found that the 5-month-old infants in his study transferred the toy a mean of three times, whereas the 2-, 3-, and 4-month-old infants transferred the toy a mean of less than once per trial. Therefore like Karniol’s infants, Rochat’s infants began to incorporate hand-tohand transfer into their exploratory play at about 5 months of age. By 6 months of age infants have a variety of actions at their disposal by which they can explore and manipulate objects. They can mouth, look, rotate, wave, bang, finger (run the fingers over the surface of an object), and transfer the object hand to hand. Nevertheless grasp at this stage is still dominated by a power grip. The thumb may be opposed to the fingers when picking up an object such as a block (Halverson, 1931), but when a smaller object is grasped, the fingers and thumb work together so the object is raked into the hand. By 9 to 10 months of age a major change occurs. Infants can now isolate the movements of the index finger and thumb from other movements of the hand and fingers. They can poke with the index finger and pick up a small object in a precision grip between the radial fingers and thumb (Folio & Fewell, 2000). When studying 6-, 9-, and 12-month-old infants, Ruff (1984) found an increase in fingering behavior in the older infants (running the fingers over the surface of an object), a function she felt was facilitated by the increased independence of the fingers and increased

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Figure 8-2 Older infants can hold a cube with the fingers acting independent of the palm. The object no longer needs to be pressed into the palm but can be held out on the finger surface (10-month-old infant).

coordination of the two hands. Grasp of an object, such as a cube, has also changed; the cube can now be held with the fingers acting independent of the palm, so the object no longer needs to be pressed against the palm but can be held out on the finger surface (Halverson, 1931) (Figure 8-2). The ability to move the object out onto the finger surface, the development of a precision grip, and the beginning of the differentiation of individual fingers are critical to the further development of skilled manipulation by the hand. Another important development during this period is the beginning of controlled release. As an example, it is also at about 9 to 10 months that infants can release a cube into a cup (Folio & Fewell, 2000). Therefore because infants’ exploratory actions become more refined as they gain better control over their motor abilities, the variety of actions that can be taken on an object increases. Infants use these motor skills to explore the properties of the objects they grasp. That is, infants’ actions with objects are not purely random but have the characteristics of true exploration.

EXPLORATORY NATURE OF I NFANT OBJECT MANIPULATION Although the neonate may be able to accomplish a primitive form of reach, he or she does not yet have voluntary control over the grasp of an object but will hold an object placed in the hand. For the young infant the mouth is also an instrument of grasp or exploration.

Rochat (1987) looked at the neonate’s use of the hand and mouth to explore or differentiate object properties. He addressed this question by looking at the reaction of neonates to a soft or rigid object placed in either the mouth or the hand. Newborn infants (49 to 96 hours of age) were presented with either a soft foam or rigid plastic tube, which was placed in their hand for grasp or in their mouth for sucking. The tubes were attached to a transducer, which was able to monitor the amount of pressure the infants applied to the two different objects. When grasped with the hand, the hard object was associated with significantly more squeezes than the soft object. When it was placed in the mouth, the reverse was seen. Obviously the infants were responding to differences in the flexibility of the object. The author suggests that the hand appears to be more concerned with the graspability of an object and the mouth with suckability. He also states that this “supports the idea of an early detection of what objects afford for functional action”; that is, the hand and mouth are tuned from the very beginning to actively explore an object’s functional properties. More recent studies also have found that the grasp of the neonate is not just a rigid reflex but rather a movement that allows the infant to gather information about object properties. Streri, Lhote, and Dutilleul (2000) placed either a cylinder or an elongated prism in the hands of neonates. After they had habituated to the object (defined as holding time that decreased to one third of the time on the first two trials or after nine trials), the infant was either given the same or the opposite object to hold. Holding time increased when the infant was presented with the novel object. It appeared that the infants were differentiating between the two shapes and demonstrating at least a primitive form of tactile discrimination. Neonates 3 days old can also differentiate between objects that are smooth or have a granular surface (Molina & Jouen, 1998, 2004). The infants in these studies tended to use more pressure when holding a smooth object and less pressure when holding a granular object. Molina and Jouen (2004) believe that neonates’ grip is an exploratory tool that can be used to process object properties. The object manipulation of the infant less than 4 months of age is necessarily limited because reach and grasp are still quite primitive. Yet if an object is placed in the infant’s hand or the infant happens to grasp an object once in contact with it, some attempts to explore the object’s characteristics appear to be present. Older infants have more physical skills at their disposal that are used to explore object properties. Steele and Pederson (1977) looked at the difference in manipulation with changes in object properties in 6-monthold infants. They measured the amount of visual fixation on the object, as well as the amount of manipulation.

Object Manipulation in Infants and Children • 147 Manipulation in this study was defined as any contact between the infant’s hand and the object. No attempt was made to further define the type of manipulation. Familiar objects the infant had previously manipulated and novel objects were used. The authors found an increase in looking and manipulating with novel more than familiar objects and also an increase in manipulation to changes in shape and texture but not to color. Of these two variables, texture elicited more manipulative behavior from the infants than changes in shape. The authors concluded, “the results indicate that an object that presents different tactile sensations is necesary to produce different manipulative behaviors.” Ruff (1984) also looked at how infants responded to different object characteristics. In this study, infants of 6, 9, and 12 months of age were presented with two sets of blocks that varied in color and pattern; more importantly, they also varied in surface texture and shape. Of interest was the observation that the infants tended to adjust their manipulative behavior to the different physical characteristics of the objects; that is, they mouthed and transferred the object more in the shape series and did more fingering in the texture series (e.g., blocks with bumps and depressions). In addition, with increasing familiarity with an object, these exploratory actions on the object decreased. This included looking, handling, rotating, transferring, and fingering. One behavior, banging the object, did not decrease over time. The author suggests that this activity may represent a play behavior unrelated to object exploration. This was also found by Ruff and co-workers (1992), who further suggested that certain types of mouthing might not be related to true object exploration.

OBJECT EXPLORATION BY THE MOUTH AND HAND In early infancy object exploration by both the mouth and hand is a major component in the infant’s interaction with objects, particularly the infant 7 months of age and younger. Ruff and co-workers (1992) indicated that, in their study, mouthing behavior peaked at about 7 months of age and comprised 27% of the time the infant was engaged with an object. This fell to 17% for 11-month-old infants. Ruff (1984) suggested that the decrease in mouthing might result from a better haptic system becoming available in the hand. Ruff and co-workers (1992) looked at the exploratory behavior of both the hands and the mouth in 5- to 11-month-old infants. They described what they called active mouthing and distinguished this from more general actions of objects in the mouth. Active mouthing was defined as movements of the object in the mouth by the hand (e.g., being turned in the

mouth) or when the mouth moved over the object. The authors found a significant association between active mouthing and then immediately looking at the object, but not other forms of object–mouth interaction (e.g., just holding the object in the mouth). After a bout of active mouthing the infant immediately paused to look at the object. They hypothesized that mouthing with looking might serve an exploratory or information-gathering function. To study this further, they presented infants with familiar and novel objects and noted the forms of exploration used in the two situations. They found that mouthing with looking and manual actions such as turning the object, transferring hand to hand, and fingering all declined as the infant became familiar with the object but returned when the infant was presented with a novel toy. Therefore they suggest that these actions are truly exploratory and a means of gathering information about objects. Other actions, such as mouthing without looking, banging, and waving, did not significantly decline in frequency as the infants became familiar with the object, and they indicate that these actions may serve some other function.

ROLE OF VISION IN I NFANT OBJECT MANIPULATION Up to this point we have discussed changes in the motor system that provide the infant with mechanisms by which object manipulation and exploration can happen. We have also indicated that even neonates appear to use the motor skills available to them to explore object characteristics. Also important to the object exploration of infants is consideration of the role vision plays in driving and supporting this behavior. Blind infants are significantly delayed in their object exploration when compared with sighted peers. Fraiberg (1968) indicated that totally blind infants do not spontaneously bring their hands to midline for mutual fingering, as seen in the 4-month-old sighted child. She argued “that there is good reason to believe that the mutual fingering games and the organization of the hands at midline are largely facilitated by vision and that the tactile engagement of the fingers requires simultaneous visual experience to insure its pleasurable repetition.” She also indicated that the hands of the totally blind infant do not explore objects, but serve primarily to bring the object to the mouth. Consequently it appears that, for the normally sighted infant, vision is an important motivator that leads the hand into space and serves to facilitate grasp and manipulation. Even in neonates manual activity appears to be directed by visual information. Molina and Jouen (2001) presented 3- to 5-day-old neonates with one of two objects. One object was smooth and

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the other granular (same objects used in the studies mentioned previously). In a pretest period one of the objects was placed in the infant’s hand without the infant being able to see the object. The time until the object was dropped and the amount of pressure exerted on the object were measured. After this pretest period the object was placed back in the infant’s hand at the same time a smooth or granular visual object was presented on the table in front of the infant. Therefore the child was holding one object and looking at another object that was either the same or a different texture than the one being held. The holding time and pressure on the held object were measured again. The visual object was then removed and the holding time and pressure on the object that remained in the hand were measured. The authors found that the holding time when the texture of the held object and the visual object matched increased but holding time remained the same when the visual and tactile objects were mismatched. Molina and Jouen (2001) feel the results indicate that the infant is comparing the held object with the visual object. If the infant finds differences between the tactile and visual object, the process of comparison is stopped. That is, holding time decreases because the “problem” the child was given is solved. Alternately, as long as no differences are observed between the tactile and visual object, the process of comparison is ongoing and exploration time is increased. Therefore the authors feel that vision and touch are interconnected even at birth and that neonates can make some comparisons across these two modalities. The role of vision also can be seen in older infants. As indicated, Karniol (1989) found that when a 2month-old infant grasped an object, he or she would rotate it but only if the hand could be seen. If the hand was out of visual regard, the object would be dropped. In his study of 2- to 5-month-old infants, Rochat (1989) looked at what infants did first with an object. Did they immediately bring it to the mouth or did they first bring it to the eyes to look at it? (The infants were all seated in slightly reclining infant seats.) He found that at 2 to 3 months more than two thirds of the infants first brought the object to the mouth. At 4 to 5 months the majority of the infants first brought the object into the field of vision for inspection. This was particularly true of the 5-month-old infants, in whom visual exploration was used first in 90% of the sample. Rochat (1989) also indicated that fingering of an object by infants might be linked to vision. In one study using 2-, 3-, 4-, and 5-month-old infants, the author found a significant interaction between fingering and looking. To test this interaction further, he studied a different set of 3-, 4-, and 5-month-old infants as they manipulated objects in dark and light situations. The dark situation was accomplished using an infrared light

and a video camera sensitive to this light. He found that fingering was dramatically decreased in the dark situation, whereas the incidence of mouthing and handto-hand transfer remained the same in the two experimental conditions. The author indicated that early fingering appears to be linked to vision and depends on this modality. Alternately, mouthing appears to be independent of vision, and in this study early hand-tohand transfer also did not seem to depend on vision. Therefore it appears that, at least in younger infants, vision is an integral part of the process of grasp and manipulation, and in fact may be the early motivator for object exploration and drive some of the more refined manipulative actions, such as fingering of an object.

HANDLING M ULTIPLE OBJECTS Effective object manipulation also requires that the infant solve the problems of how to deal with more than one object at a time. Bruner (1970) attempted to look at what he called “taking possession of objects” by presenting infants with a small toy and then presenting a second toy to the same hand. If the infant did not make an attempt to secure the second toy, it was then held at midline. After two toys were grasped, the infant was handed a third and fourth toy and the child’s solution to this multiple object problem was observed. Bruner found that 4- to 5-month-old infants had difficulty managing two objects. Often, as the infant’s attention was attracted to the second toy, the held toy was dropped. The 6- to 8-month-old infants were able to solve the two-toy problem by transferring the initial toy to the other hand and then grasping the second toy. Solving the problem of three objects required a different strategy that was not seen until 9 to 11 months; that is, when offered the third object, the older infants “stored” one of the objects he or she had been holding on the table or lap. But half the infants of this age then retrieved the stored object immediately. They did not appear to be able to inhibit the drive to pick up what they saw or could not delay this process. By 12 months the infants had the solution of this problem well “in hand.” They not only transferred the first object to the other hand in anticipation of receiving the second object, but also anticipated the third and fourth by storing the toys in hand in the lap or the arm of the chair. By 15 to 17 months the infants also stored by handing objects to the parent or examiner. Therefore by 12 months and older, infants have learned to deal with several items at one time.

SUMMARY AND THERAPEUTIC I MPLICATIONS As infants gain control over the movements of their arms and hands, they also increase the options available

Object Manipulation in Infants and Children • 149 to them for object exploration. In the very young infant objects are fixed in the hand, and exploration is limited to a power grip and movements of the arm and wrist. An important expansion of the actions available to infants comes when they can bring both hands together and eventually transfer an object from one hand to the other. The infant can now wave, bang, mouth, transfer, rotate, and run fingers over an object’s surface. The ability to manage more than one object at a time is also an important aspect of object interaction, and infants appear to gradually accomplish this skill over the first 12 months of life. During this period infants also develop two other extremely important skills: Control over voluntary release or placement of an object, and the ability to use a precision or refined pincer grip. This latter skill is critical to the further development of object manipulation by the hand. From a therapeutic point of view, one should note that changes in object properties seem to elicit different manipulative behaviors from infants. As an example, changes in shape appear to generate more transferring and rotation activities, and changes in texture more fingering and possibly an increase in the duration of manipulation (Figure 8-3). Often parents and others who interact with infants see the infant’s mouthing, turning, and handling of objects as random motions. As indicated, however, at least some of these movements appear to be meaningful attempts to explore object properties. This is important information to consider when evaluating and planning programs for a child. Pointing out to parents or caregivers how the infant changes manipulative strategies with changes in object properties can help them appreciate the infant’s competencies and the importance of these actions to the infant’s learning. Providing the infant with a variety of objects that differ in shape and texture may well facilitate this process. In observing infants, it is also important to note when they do not show the variety of exploratory behaviors appropriate for their age. As indicated, waving, banging, and some forms of mouthing may not serve the same exploratory functions as activities such as transferring hand to hand, fingering, rotating, and active mouthing. Ruff and co-workers (1984) state that “The infant who does not finger, rotate, and transfer objects very much has less opportunity to learn about object properties. We can speculate that the less infants learn about object properties the less they will engage in categorization of objects. Any deficit in categorization should affect early language development. In this way it is possible for manipulative exploration of objects to contribute directly to an infant’s cognitive development” (p. 1173).

Several studies (Church et al., 1993; Goyen & Lui, 2002; Ross, 1985; Ross, Lipper, & Auld, 1986; ThunHohenstein et al., 1991) have found preterm infants to

A

B Figure 8-3 Changes in an object’s texture and surface characteristics may increase higher-level manipulation such as fingering. This figure shows two infants who are approximately 9 months old using finger movements to explore (A) a yarn ball, or (B) bells attached to a toy.

score lower than term infants on eye–hand and fine motor items of developmental tests. Kopp (1976) found preterm infants to differ significantly from fullterm infants on the duration of exploratory activity. In another study this same author (1974) found a greater percentage of preterm infants (age corrected for prematurity) to be clumsy in object manipulation when compared with term infants (70% of the preterm infants and 19% of the term infants). The clumsy infants also were noted to spend less time manually exploring objects and more time in visual exploration. Ruff and co-workers (1984) also studied the manipulative abilities of preterm and term infants. They divided the preterm infants into high- and low-risk groups depending on the infants’ early medical history. They then compared these two groups to a group of full-

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term infants (preterm infants’ age corrected for prematurity). They found a significant decrease in the incidence and amount of fingering, transfer, and rotation of objects in the high-risk group compared with the two other infant groups. Apparently for some infants, the delay in fine motor skills is long lasting. Goyen and Lui (2002) followed 54 high-risk infants (