Plasticity in the human nervous system Investigations with transcranial magnetic stimulation It is now well known that the functional organization of the cerebral cortex is plastic, and that changes in organization occur throughout life in response to normal and abnormal experience. Transcranial magnetic stimulation (TMS) is a non-invasive and painless technique that has opened up completely new and fascinating avenues to study neural plasticity. First, TMS can be used to detect changes in excitability or connectivity of the stimulated cortex which may have occurred through processes suchas learning or recovery from a lesion. Second, repeated TMS by itself can induce changes in excitability and connectivity of the stimulated cortex which may be used therapeutically in neurological and psychiatric disease. Third, TMS can induce short-lasting virtual lesions which may directly test the functional relevance of brain plasticity. Current knowledge of all these exciting possibilities is brought together in this book, written by the world s leading experts in the field. The book is an essential compendium on plasticity of the human brain in health and disease, for clinical neurophysiologists, neurologists, psychiatrists and neuroscientists. Simon Boniface is Consultant Neurophysiologist and Director of Neurophysiology, Addenbrooke s Hospital and Wolfson Brain Imaging Centre, Cambridge, UK. Ulf Ziemann is Assistant Professor of Neurology, Clinic of Neurology, Johann Wolfgang Goethe-University of Frankfurt, Germany.
Plasticity in the Human Nervous System Investigations with Transcranial Magnetic Edited by Simon Boniface Department of Clinical Neurophysiology Addenbrooke s Hospital Wolfson Brain Imaging Centre University of Cambridge UK and Ulf Ziemann Clinic of Neurology Johann Wolfgang Goethe-University of Frankfurt Germany
published by the press syndicate of the university of cambridge The Pitt Building, Trumpington Street, Cambridge, United Kingdom cambridge university press The Edinburgh Building, Cambridge CB2 2RU, UK 40 West 20th Street, New York, NY 10011-4211, USA 477 Williamstown Road, Port Melbourne, VIC 3207, Australia Ruiz de Alarcón 13, 28014 Madrid, Spain Dock House, The Waterfront, Cape Town 8001, South Africa http://www.cambridge.org C Cambridge University Press 2003 This book is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2003 Printed in the United Kingdom at the University Press, Cambridge Typefaces Minion 11/14.5 pt and Formata System L A TEX2ε [tb] A catalogue record for this book is available from the British Library Library of Congress Cataloguing in Publication data Motor plasticity and TMS : basic science and clinical applications / edited by Simon J. Boniface and Ulf Ziemann. p. cm. Includes bibliographical references and index. ISBN 0 521 80727 1 1. Neuroplasticity. 2. Magnetic brain stimulation. I. Boniface, Simon J., 1964 II. Ziemann, Ulf. QP363.3.M685 2003 612.8 dc21 2002031559 ISBN 0 521 80727 1 hardback Every effort has been made in preparing this book to provide accurate and up-to-date information that is in accord with accepted standards and practice at the time of publication. Nevertheless, the authors, editors and publisher can make no warranties that the information contained herein is totally free from error, not least because clinical standards are constantly changing through research and regulation. The authors, editors and publisher therefore disclaim all liability for direct or consequential damages resulting from the use of material contained in this book. Readers are strongly advised to pay careful attention to information provided by the manufacturer of any drugs or equipment that they plan to use.
Contents List of contributors Preface vii xi 1 The nature and mechanisms of plasticity 01 Mengia-S. Rioult-Pedotti and John P. Donoghue 2 Techniques of transcranial magnetic stimulation 26 John C. Rothwell 3 Developmental plasticity of the corticospinal system 62 Janet Eyre 4 Practice-induced plasticity in the human motor cortex 90 Joseph Classen and Leonardo G. Cohen 5 Skill learning 107 Edwin M. Robertson, Hugo Theoret and Alvaro Pascual-Leone 6 -induced plasticity in the human motor cortex 135 Joseph Classen and Ulf Ziemann 7 Lesions of cortex and post-stroke plastic reorganization 166 Paolo M. Rossini and Joachim Liepert 8 Lesions of the periphery and spinal cord 204 Michael J. Angel, Nick Davey, Peter Ellaway and Robert Chen 9 Functional relevance of cortical plasticity 231 Pablo Celnik and Leonardo G. Cohen 10 Therapeutic uses of rtms 246 Chip Epstein and John C. Rothwell v
vi Contents 11 Rehabilitation 264 David Gow, Chris Fraser and Shaheen Hamdy 12 New questions 288 Mark Hallett, Eric M. Wassermann and Leonardo G. Cohen Index 301 Colour plates between pp.116 and 117
Contributors Editors Simon Boniface Department of Clinical Neurophysiology Addenbrooke s Hospital and the Wolfson Brain Imaging Centre Cambridge CB2 2QQ, UK Ulf Ziemann Neurologische Klinik Johann Wolfgang Goethe-Universität Frankfurt Theodor-Stern-Kai 7 60590 Frankfurt am Main Germany Contributors Michael J. Angel Toronto Western Hospital 5W 445, 399 Bathurst Street Toronto, Ontario, M5T 2S8, Canada Pablo A. Celnik Department of Physical Medicine and Rehabilitation Johns Hopkins University 136 West Lanvale Street Baltimore MD 21217, USA Robert Chen Toronto Western Hospital 5W 445, 399 Bathurst Street Toronto, Ontario, M5T 2S8, Canada Joseph Classen Department of Neurology University of Würzburg Josef-Schneider-Str 11 D-97080 Würzburg, Germany Leonardo G. Cohen Human Cortical Physiology Section NINDS National Institutes of Health Building 10, Room 5N 234 10 Center Drive, MSC 1428 Bethesda MD 20892-1428, USA vii
viii List of contributors Nicholas J. Davey Department of Sensorimotor Systems (Room 10L09) Division of Neuroscience and Psychological Medicine Imperial College School of Medicine, Charing Cross Hospital Fulham Palace Road London W6 8RF, UK John P. Donoghue Department of Neuroscience Brown University Box 1953 Providence RI 02912, USA PeterH.Ellaway Department of Sensorimotor Systems (Room 10L09) Division of Neuroscience and Psychological Medicine Imperial College School of Medicine, Charing Cross Hospital Fulham Palace Road London W6 8RF, UK Chip M. Epstein Department of Neurology Emory Clinic 1365 Clifton Road NE Atlanta GA 30322, USA JanetA.Eyre Department of Child Health The Royal Victoria Infirmary Queen Victoria Road Newcastle upon Tyne NE1 4LP, UK Chris Fraser Department of Medicine Royal Bolton Hospital Farnworth Bolton BL4 0JR, UK David Gow Department of G.I. Sciences and Medicine University of Manchester Hope Hospital Eccles Old Road Salford M6 8HD, UK Mark Hallett Human Motor Control Section NINDS National Institutes of Health Building 10, Room 5N 226 10 Center Drive, MSC 1428 Bethesda MD 20892-1428, USA Shaheen Hamdy Department of Gastroenterology University of Manchester Hope Hospital Eccles Old Road Salford M6 8HD, UK Joachim Liepert Clinic of Neurology University of Hamburg Hamburg 52 20246, Germany Alvaro Pascual-Leone Laboratory for Magnetic Brain Behavioral Neurology Unit
ix List of contributors Beth Israel Deaconess Medical Center 330 Brookline Avenue, Kirstein Building KS 452 Boston MA 02215, USA Mengia-S. Rioult-Pedotti Department of Neuroscience Brown University Box 193 Providence RI 02912, USA EdwinM.Robertson Laboratory for Magnetic Brain Behavioral Neurology Unit Beth Israel Deaconess Medical Center 330 Brookline Avenue, Kirstein Building KS 452 Boston MA 02215, USA Paolo M. Rossini Department of Neuroscience Ospedale Fatebenefratelli Isola Tiberina 39 00186 Rome, Italy John C. Rothwell Sobell Department Institute of Neurology (Box 146) Queen Square London WC1N 3BG, UK Hugo Theoret Laboratory for Magnetic Brain Behavioral Neurology Unit Beth Israel Deaconess Medical Center 330 Brookline Avenue, Kirstein Building KS 452 Boston MA 02215, USA Eric M. Wassermann NINDS National Institutes of Health Building 10, Room 5N 226 10 Center Drive, MSC 1428 Bethesda MD 20892-1428, USA Ulf Ziemann Neurologische Klinik Johann Wolfgang Goethe-Universität Frankfurt Theodor-Stern-Kai 7 60590 Frankfurt am Main Germany
Preface xi Plasticity of the brain is an increasingly important topic in many areas of neuroscience including development, learning and repair. It is still a challenge to study plasticity directly in the human nervous system. Transcranial magnetic stimulation (TMS), however, has become a suitable non-invasive and painless technique, which can be applied to detect changes in cortical excitability or connectivity as indicators of plasticity. Further, TMS can be used to induce short-lasting virtual lesions in order to test the functional relevance of brain plasticity. Finally, TMS can induce plasticity itself. In this book, we utilize TMS in these ways to investigate and manipulate plasticity in the human nervous system. In so doing, we have been fortunate to gather many of the world s leading contributors in this field. The basic nature and mechanisms of plasticity are tackled in the introductory chapter, with particular reference to the animal primary motor cortex. This is followed in the next chapter by an introduction to the technique and physiological effects of human TMS. In the next section we then apply this background to TMS studies of plasticity in healthy subjects. Chapter 3 is about developmental plasticity of the human corticospinal tract. The next two chapters demonstrate the maintained capability of the adult human brain for plastic change by looking into TMS studies of use-dependent plasticity and learning of motor skills. Finally, the induction of plasticity by TMS itself is the focus of Chapter 6. The next section is more clinically orientated and examines functional deficits and the principles of recovery of function after cortical lesions, stroke in particular, and lesions of the periphery and spinal cord. This is followed by a demonstration of the functional relevance of cortical plasticity. The concluding two chapters of this section provide a survey of TMS as a potential therapeutic tool for promoting beneficial plasticity in various neurological
xii Preface and psychiatric disorders, and the applications of TMS in the process of neurological rehabilitation. The book closes with a look towards the future, speculating on novel and farther reaching avenues for the study and influence of human brain plasticity with TMS. We would like to thank the contributors for all their time and effort, and chiefly we would like to thank our families for their support, past and future. Simon Boniface and Ulf Ziemann Cambridge and Frankfurt, September 2002