EVOLUTIONARY DEVELOPMENTAL BIOLOGY OF THE CEREBRAL CORTEX The Novartis Foundation is an international scientific and educational charity (UK Registered Charity No. 313574). Known until September 1997 as the Ciba Foundation, it was established in 1947 by the CIBA company of Basle, which merged with Sandoz in 1996, to form Novartis. The Foundation operates independently in London under English trust law. It was formally opened on 22 June 1949. The Foundation promotes the study and general knowledge of science and in particular encourages international co-operation in scientific research. To this end, it organizes internationally acclaimed meetings (typically eight symposia and allied open meetings and 15—20 discussion meetings) and publishes eight books per year featuring the presented papers and discussions from the symposia. 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Other Wiley Editorial Offices John Wiley & Sons, Inc., 605 Third Avenue, New York, NY 10158-0012, USA WILEY-VCH Verlag GmbH, Pappelallee 3, D-69469 Weinheim, Germany Jacaranda Wiley Ltd, 33 Park Road, Milton, Queensland 4064, Australia John Wiley & Sons (Asia) Pte Ltd, 2 Clementi Loop #02-01, Jin Xing Distripark, Singapore 129809 John Wiley & Sons (Canada) Ltd, 22 Worcester Road, Rexdale, Ontario M9W 1L1, Canada Novartis Foundation Symposium 228 ix+271 pages, 48 figures, 1 table Library of Congress Cataloging-in-Publication Data Evolutionary developmental biology of the cerebral cortex/ [editors, Gregory R. Bock and Gail Cardew]. p. cm. — (Novartis Foundation symposium ; 228) Symposium on Evolutionary Developmental Biology of the Cerebral Cortex, held at the Novartis Foundation, London, 20-22 April 1999. Includes bibliographical references and index. ISBN 0-471-97978-3 (hbk : alk. paper) 1. Cerebral cortex—Congresses. 2. Brain- Evolution-Congresses. 3. Developmental neurobiology—Congresses. I. Bock, Gregory. II. Cardew, Gail. III. Novartis Foundation. IV Symposium on Evolutionary Developmental Biology of the Cerebral Cortex (1999 : London, England). V Series. QP383.E95 2000 573.8'6-dc21 00-027101 British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN 0 471 97978 3 Typeset in l01/2 on 12/1/2 pt Garamond by DobbieTypesetting Limited, Tavistock, Devon. Printed and bound in Great Britain by Biddies Ltd, Guildford and King's Lynn. This book is printed on acid-free paper responsibly manufactured from sustainable forestry, in which at least two trees are planted for each one used for paper production. Contents Symposium on Evolutionary developmental biology of the cerebral cortex, held at the Novartis Foundation, London, 20-22 April 1999 This symposium is based on a proposal made by Zoltan Molnar Editors: Gregory R. Bock (organizer) and Gail Cardew L.Wolpert What is evolutionary developmental biology? 1 Discussion 9 K. Herrup Thoughts on the cerebellum as a model for cerebral cortical development and evolution 15 Discussion 24 P. Rakic Radial unit hypothesis of neocortical expansion 30 Discussion 42 General discussion I 46 E. Boncinelli, A. Mallamaci and L. Muzio Genetic control of regional identity in the developing vertebrate forebrain 53 Discussion 61 J. L. R. Rubenstein Intrinsic and extrinsic control of cortical development 67 Discussion 75 A. J. Reiner A hypothesis as to the organization of cerebral cortex in the common amniote ancestor of modern reptiles and mammals 83 Discussion 102 General discussion II 109 I. Bar and A. M. Goffinet Evolution of cortical lamination: the reelin/Dabl pathway 114 Discussion 125 vi CONTENTS J. G. Parnavelas, S. A. Anderson, A. A. Lavdas, M. Grigoriou,V. Panchis and J. L. R. Rubenstein The contribution of the ganglionic eminence to the neuronal cell types of the cerebral cortex 129 Discussion 139 Z. Molnar Conserved developmental algorithms during thalamocortical circuit formation in mammals and reptiles 148 Discussion 166 P. Levitt and K. L. Eagleson Regionalization of the cerebral cortex: developmental mechanisms and models 173 Discussion 181 J. H. Kaas Organizing principles of sensory representations 188 Discussion 198 L. A. Krubitzer How does evolution build a complex brain? 206 Discussion 220 E.Welker Developmental plasticity: to preserve the individual or to create a new species? 227 Discussion 235 D. Purves, S. M.Williams and R. B. Lotto The relevance of visual perception to cortical evolution and development 240 Discussion 254 Final discussion 259 Index of contributors 264 Subject index 266 Participants E. Boncinelli DIBIT, Scientific Institute San Raffaele, Via Olgettina 58, Milan, Italy F. Bonhoeffer MPI fur Entwicklungsbiologie, Abt. Physikal. Biologie, Spemannstr. 35/1, 72076 Tubingen, Germany V. Broccoli (Bursar) TIGEM Institute Dibit HS Raffaele, Via Olgettina 58, I-20132 Milan, Italy A. B. Butler Krasnow Institute for Advanced Study and Department of Psychology, George Mason University, MSN 2A1, Fairfax, VA 22030, USA S. E. Evans Department of Anatomy and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK A. M. Goffinet Neurobiology Unit, University of Namur Medical School, 61 rue de Bruxelles, B5000 Namur, Belgium K. Herrup Department of Neuroscience and University Alzheimer Research Center of Cleveland, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH 44120, USA W. Hodos Department of Psychology, University of Maryland, College Park, MD 20742-4411, USA S. Hunt Department of Anatomy and Developmental Biology, Medawar Building, University College London, Gower Street, London WC1E 6BT, UK J. H. Kaas Department of Psychology, Vanderbilt University, 301 Wilson Hall, Nashville, TN 37240, USA H. J. Karten (Chair) Department of Neurosciences, University of California at San Diego, La Jolla, CA 92093-0608, USA viii PARTICIPANTS L. A. Krubitzer Center for Neuroscience and Department of Psychology, 1544 Newton Court, University of California, Davis, CA 95616, USA P. R. Levitt Department of Neurobiology, University of Pittsburgh School of Medicine, E1440 Biomed Science Tower, Pittsburgh, PA 15261, USA A. Lumsden Department of Developmental Neurobiology, King's College London, Hodgkin House, Guy's Campus, Guy's Hospital, London SE1 9RT, UK Z. Molnar* Institut de Biologie Cellulaire et de Morphologie, Universite de Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland D. D. M. O'Leary Laboratory of Molecular Neurobiology, The Salk Institute, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA N. Papalopulu Wellcome/CRC Institute, Tennis Court Road, Cambridge CB2 1QR, UK J. G. Parnavelas Department of Anatomy and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK J. Pettigrew Vision Touch and Hearing Research Centre, University of Queensland, Brisbane, QLD 4072, Australia L. Puelles Dpto. Ciencias Morfologicas, Facultad de Medicina, Universidad de Murcia, Campus de Espinardo, 30100 Espinardo, Murcia, Espana D. Purves Department of Neurobiology, Box 3209, Duke University Medical Center, 101-I Bryan Research Building, Durham, NC 27710, USA P. Rakic Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510, USA A. J. Reiner Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee, 855 Monroe Avenue, Memphis, TN 38163, USA *Current address: Department of Human Anatomy and Genetics, University of Oxford, South Parks Road, Oxford OX1 3QX, UK PARTICIPANTS ix J. L. R. Rubenstein Nina Ireland Laboratory of Developmental Neurobiology, Center for Neurobiology and Psychiatry, Department of Psychiatry and Programs in Neuroscience, Developmental Biology and Biomedical Sciences, University of California at San Francisco, 401 Parnassus Avenue, San Francisco, CA 94143, USA E.Welker Institut de Biologie Cellulaire et de Morphologie, Universite de Lausanne, Rue du Bugnon 9, 1005 Lausanne, Switzerland L.Wolpert Department of Anatomy and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK