MOTOR CONTROL AND LEARNING

MOTOR CONTROL AND LEARNING

MOTOR CONTROL AND LEARNING

Edited by

Mark L. Latash

THE PENNSYLVANIA STATE UNIVERSITY

and

Francis Lestienne

UNIVERSIT ´E DE CAEN BASSE-NORMANDIE, FRANCE

Library of Congress Cataloging-in-Publication Data

Motor control and learning / edited by Mark L. Latash and Francis Lestienne.

p. ; cm.

Includes bibliographical references and index.

ISBN-13: 978-0-387-25390-9 (alk. paper) ISBN-10: 0-387-25390-4 (alk. paper)

1. Motor learning. 2. Cognition. 3. Movement, Psychology of. I. Latash, Mark L., 1953- II. Lestienne, Francis.

[DNLM: 1. Movement—physiology. 2. Learning—physiology. 3. Psychomotor Performance—physiology. WE 103 M9167 2006]

QP301.M6855 2006 612.8

11—dc22

2005051575

C

2006 Springer Science+Business Media, Inc.

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CONTENTS

Preface vii

I. CONTROL OF MOVEMENT AND POSTURE 1

1. The Nature of Voluntary Control of Motor Actions 3

Anatol G. Feldman

2. Plans for Grasping Objects 9

David A. Rosenbaum, Rajal G. Cohen, Ruud G. J. Meulenbroek and Jonathan Vaughan

3. Adherence and Postural Control: A Biomechanical Analysis of Transient Push Efforts 27

Simon Bouisset, Serge Le Bozec and Christian Ribreau

II. CONTROL OF RHYTHMIC ACTION 45 4. Trajectory Formation in Timed Repetitive

Movements 47

Ramesh Balasubramaniam

5. Stability and Variability in Skilled Rhythmic Action—A Dynamical Analysis of Rhythmic Ball Bouncing 55

Dagmar Sternad

6. The Distinctions Between State, Parameter and Graph Dynamics in Sensorimotor Control and Coordination 63

Elliot Saltzman, Hosung Nam, Louis Goldstein, and Dani Byrd

III. MOTOR LEARNING AND NEURAL PLASTICITY 75

7. Stabilization of Old and New Postural Patterns in Standing Humans 77

Benoˆıt G. Bardy, Elise Faugloire, Paul Fourcade and Thomas A. Stoffregen

8. The Role of the Motor Cortex in Motor Learning 89

Mark Hallett

9. Feedback Remapping and the Cortical Control of Movement 97

Michael S. A. Graziano

10. How Cerebral and Cerebellar Plasticities may Cooperate During Arm Reaching Movement Learning: A Neural Network Model 105

Alexander A. Frolov and Michel Dufoss´e

11. Motor Performance and Regional Brain Metabolism of Four Spontaneous Murine Mutations with Degeneration of the Cerebellar Cortex 115

Robert Lalonde and Catherine Strazielle

IV. DEVELOPMENT AND AGING 125 12. Development and Motor Control: From the

First Step on 127

Guy Cheron, Anita Cebolla, Franc¸oise Leurs, Ana Bengoetxea and Bernard Dan

13. Changes in Finger Coordination and Hand Function with Advanced Age 141

Mark L. Latash, Jae Kun Shim, Minoru Shinohara, and Vladimir M. Zatsiorsky

Author Index 161 Subject Index 167

v

PREFACE

The purpose of the current volume is two-fold. First, it presents a series of review papers reflecting the re- cent progress in the area of neural control of posture and movement (Parts I and II). Second, it focuses on issues of changes in motor patterns and neurological structures involved in their production with learning, development, and aging (Parts III and IV).

The chapters in this volume were written by speak- ers at the Fourth meeting “Progress in Motor Con- trol” that took place in Caen (France) in 2003. As such, it continues the tradition of a series “Progress in Motor Control” with the first three volumes published in 1999, 2002, and 2003. The authors of the chapters were explicitly encouraged to present state-of-the-art review of particular aspects of motor control and to use their own studies as illustrations of the most im- portant developments in the area.

As in all previous volumes, we hope that the spirit of Nikolai Bernstein can be perceived in all the chapters. Nikolai Bernstein, viewed by many as the father of contemporary motor control, was deeply in- volved in studies of the effects of learning on mo- tor coordination. These activities resulted in a clas- sical book “Dexterity and Its Development” written in the mid-nineteen-forties and published in English in 1996. Bernstein also contributed to several seminal studies in the area of motor development. He used a unique method of measuring movement kinematics, cyclogrammetry, which he had himself developed, and quantified changes in locomotor patterns happening during the first years of age.

The opening chapter of the volume written by Ana- tol Feldman addresses very basic issues of motor con- trol, those related to the nature of variables that are manipulated by the central nervous system to pro- duce natural movements. The chapter makes a strong argument in favor of parametric control of the neu- romotor apparatus contrasting it with attempts to de- velop control schemes that try to prescribe patterns of state variables such as forces, displacements, or mus- cle activation patterns. Feldman briefly reviews the equilibrium-point hypothesis of motor control, which he suggested about 40 years ago, and illustrates its power in dealing with a spectrum of motor problems including such evergreen problems as the relation be- tween posture and movement and the problem of mo- tor redundancy.

The second chapter is co-authored by Rosenbaum, Cohen, Meulenbroek, and Vaughan. The authors ad- dress in this chapter another central issue of motor control, that of creating motor plans. In line with the- orizing by David Rosenbaum and his colleagues, this chapter develops the idea of end-state comfort as an organizing criterion for the formation motor plans.

The chapter also highlights the role of mental repre- sentation in motor control.

Chapter 3 focuses on issues of postural control.

Bouisset, Le Bozec, and Ribreau consider an aspect of the control of vertical posture that has been typi- cally overlooked in many earlier studies. Their chapter deals with the question of the interface between the body and its physical environment, namely adherence and friction. The authors used a particular experimen- tal method involving the application of self-imposed postural perturbations to study a quantitative index of adherence. They also develop a biomechanical model that allows analyzing the mechanical behavior of the postural chain.

The second part of the volume unites three chapters written by leaders in the area of studies of cyclic actions. Ramesh Balasubramaniam in Chapter 4 reviews recent studies that link the ideas from the tra- jectory formation area to timing accuracy in repetitive movements. This chapter also offers a controversial paradigm that tries to bring together two approaches to motor control that have traditionally been viewed as incompatible, the dynamic systems approach and the information processing approach.

The fifth chapter by Dagmar Sternad focuses on a particular motor task, bouncing a ball on the tennis racket to address several basic aspects of the produc- tion of rhythmic actions such as their stability in the presence of external perturbations and spontaneous variability of the motor pattern. Sternad describes a discrete non-linear model reflecting the kinematics of the ball and the racket and their interactions during impact. The model is used to predict stable regimes of ball bouncing, which are then compared to ac- tual performance of humans. Based on her studies, Sternad concludes that human actors sense and make use of stability properties of this task.

The last chapter in the second part of the book by Saltzman, Nam, Goldstein, and Byrd addresses issues that are in some aspects similar to those

vii

viii PREFACE

reviewed by Feldman in Chapter 1. In particular, these authors analyze skilled motor behavior in terms of state-, parameter-, and graph-dynamics. After a review of these concepts, Saltzman and his colleagues focus on the manner in which variation in dynamical graph structure can be used to explicate the temporal pat- terning of speech. They present simulations of speech gestural sequences using the task-dynamic model of speech production.

The five chapters of Part III review very different aspects of changes in motor patterns and neurophys- iological structures associated with motor learning.

Bardy, Faugloire, Fourcade and Stoffregen suggest a model of vertical posture and then describe changes that happen when human subjects are asked to learn a novel coordination among major postural joints. This chapter addresses central issues of stabilization and destabilization that accompany the process of motor skill acquisition. It also reviews similarities and dif- ferences between the processes of learning a postural coordination and a bimanual coordination.

The motor cortex and the cerebellum have tradi- tionally been in the center of attention of motor con- trol researchers. Recently, a number of studies have suggested that the motor cortex is not simply an ex- ecutor of motor commands and that it is involved in different aspects of motor learning. Chapter 8 by Mark Hallett address the role of the motor cortex in motor learning. Mark Hallett reviews studies us- ing brain stimulation techniques such as transcranial magnetic stimulation (TMS), traditional electroen- cephalographic methods (EEG), and brain imaging techniques (positron emission tomography, PET) to demonstrate plastic changes in the motor cortex dur- ing different phases of motor learning. These studies have shown, in particular, the important role of motor cortex during implicit motor learning and during the stage of consolidation.

In Chapter 9, Michael Graziano reviews his recent exciting studies of the effects of relatively long-lasting electrical stimulation of the motor cortex of primates that has been shown to induce multi-joint movements resembling common gestures in the monkey’s behav- ior. Experiments by Graziano and his colleagues sug- gest that the mapping between cortex and muscles may continuously change depending on propriocep- tive feedback from the limb. This “feedback remap- ping” may play a fundamental role in motor control, allowing motor cortex to flexibly control different as- pects of movement.

The interaction between the cerebal cortex and the cerebellum is addressed in Chapter 10 by Frolov and Dufosse. These authors offer a neural network model developed based on the column organization of the

cerebral cortex and the Marr-Albus-Ito theory of cere- bellar learning. The model assumes synaptic plasticity in the cerebral cortex, in the cerebellar cortex, and in the cerebellar-thalamo-cortical pathway. The model demonstrates that adaptive processes that take place in different sites of the cerebral cortex and the cere- bellum do not interfere but complement each other during learning of arm reaching movement, and that any linear combination of the cerebral motor com- mands may generate signals able to drive the cerebellar learning processes.

Issues of the role of the cerebellum in motor con- trol and learning are also addressed in Chapter 11 by Lalonde and Strazielle. These researchers used a unique animal model of mutant mice with cerebellar atrophy. Motor performance of the mutant mice in a set of motor tasks was shown to correlate with changes in the activity of a mitochondrial enzyme, cytochrome oxidase, in the cerebellar cortex and deep nuclei. These results suggest that changes in the cerebellum are re- sponsible for behavioral differences in the used motor tasks. They also showed that staining of this particular enzyme may be useful as a predictor of motor capacity.

Two large chapters form the last part of the volume.

Cheron, Cebolla, Leurs, Bengoetxea, and Dan discuss in detail the issue of changes in intersegmental co- ordination during development of locomotion. The general pattern of intersegmental coordination and the stabilization of the trunk with respect to vertical are immature at the onset of unsupported walking in toddlers, but they develop in parallel very rapidly in the first few weeks of walking experience. The authors describe a dynamic recurrent neural network, which is able to reproduce lower limb kinematics in toddler locomotion by using multiple raw EMG data. In the context of motor learning such a network may be con- sidered as a model of biological learning mechanisms underlying motor adaptation.

The final chapter deals with changes in motor

coordination that accompany natural aging. Latash,

Shim, Shinohara, and Zatsiorsky consider age-related

changes in the hand neuromuscular apparatus and ac-

companying changes in both finger strength and fin-

ger coordination. They use analysis of performance in

maximal and submaximal effort tasks with different

degree of involvement of intrinsic and extrinsic mus-

cle groups. These studies have suggested a dispropor-

tionate loss of force by intrinsic hand muscles, which

may have important implications for multi-digit syn-

ergies. They have also shown a deficit in the ability

to stabilize the total force and the total moment pro-

duced by a set of digits in both pressing and grasping

tasks. The chapter discusses a possibility that some of

the age-related changes may be viewed as adaptive,

PREFACE ix

while other changes are more likely to interfere with the everyday hand function making it suboptimal.

This volume may be recommended to a broad range of researchers working in the areas of aging, biome- chanics, development, kinesiology, motor control, neurophysiology, neuroscience, psychology, robotics and related areas. It may also be used as a supplemen- tary reading for graduate students in these areas.

Acknowledgments

The organization of the “Progress in Motor Control IV” conference would not have been possible without the generous support of:

– Universit´e de Caen Basse-Normandie – Conseil R´egional de Basse-Normandie

– Conseil G´en´eral du Calvados – Mairie de Caen

– Centre National de la Recherche Scientifique (CNRS)

– UFR STAPS & Centre de Recherche en Activit´e Physique et Sportive (EA 2131) Universit´e de Caen – Maison de la Recherche en Sciences Humaines (UMS CNRS 843) et PPF ModeScos (Plan Pluri Formation  Mod´elisation en Sciences Cognitives

& Sociales ) Universit´e de Caen

We are very grateful to Prof. Francine Thullier, Prof.

Pierre Denise & Christophe Bertrand who shared the load of organizing and running the meeting.

Mark L. Latash and Francis G. Lestienne