RESEARCH AND PERSPECTIVES IN NEUROSCIENCES Fondation Ipsen Editor Yves Christen, Fondation Ipsen, paris (France). Editorial Board Albert Aguayo, McGill University, Montreal (Canada). Philippe Ascher, Ecole Normale Superieure, Paris (France). Alain Berthoz, College de France, CNRS UPR 2, Paris (France). Jean-Marie Besson, INSERM U 161, Paris (France). Emilio Bizzi, Massachusetts Institute of Technology, Boston (USA). Anders BjOrklund, University of Lund, Lund (Sweden). Ira Black, University of Medicine & Dentistry of New Jersey, Piscataway, (USA). Floyd Bloom, Scripps Clinic and Research Foundation, La Jolla (USA). Joel Bockaert, Centre CNRS-INSERM de Pharmacologie Endocrinologie, Montpellier (France). Pierre Buser, Institut des Neurosciences, Paris (France). Jean-Pierre Changeux, College de France, Institut Pasteur, Paris (France). Carl Cotman, University of California, Irvine (USA). S. Dunnett, University of Cambridge, Cambridge (UK). George Fink, Medical Research Council, Edinburgh (UK). Fred Gage, University of California, La Jolla (USA). Jacques Glowinski, College de France, Paris (France). Claude Kordon, INSERM U 159, Paris (France). Michel Lacour, CNRS URA 372, Marseille (France). Michel Le Moal, INSERM U 259, Bordeaux (France). Gary Lynch, University of California, Irvine (USA). Brenda Milner, McGill University, Montreal (Canada). John Olney, Washington University Medical School, Saint Louis (USA). Alain Privat, INSERM U 336, Montpellier (France). Allen Roses, Duke University MedIcal Center, Durham (USA). Constantino Sotelo, INSERM U 106, Paris (France). Jean-Didier Vincent, Institut Alfred Fessard, CNRS, Gif-sur-Yvette (France). Bruno Will, Centre de Neurochimie du CNRS/INSERM U 44 (Strasbourg). G. Buzsaki . R. Llinas . W Singer A. Berthoz . Y. Christen (Eds.) Temporal Coding in the Brain With 97 Figures and 4 Tables Springer-Verlag Berlin Heidelberg New York London Paris Tokyo Hong Kong Barcelona Budapest Buzsaki, G., Ph. D. Center for Molecular and Behavioral Neuroscience Rutgers University, 197 University Avenue Newark, NJ 07102 USA Llinas, R., Ph. D. Department of Physiology and Biophysics New York University Medical Center 550 First Avenue, New York, NY 10016 USA Singer, W., Ph. D. Max Planck Institute for Brain Research Deutschordenstr. 46, D-60528 Frankfurt/Main Germany Berthoz, A., Ph. D. Laboratoire de Physiologie de la Perception et de l'Action College de France-CNRS, 15, rue de l'Ecole de Medecine F-75270 Paris Cedex 06 Christen, Y., Ph. D. Fondation IPSEN, 24, rue Erlanger F-75016 Paris ISBN-13: 978-3-642-85150-6 e-ISBN-13: 978-3-642-85148-3 DOl: 10.1007/978-3-642-85148-3 Library of Congress CataIoging-in-Publication Data Temporal coding in the brain / G. Buzsaki ... let al.] eds. p. cm. -- (Research and perspectives in nuerosciences) Includes bibliographical references and index. (acid-free paper: New York). - (acid-free paper: Berlin) 1. Cerebral cortex. 2. Hippocampus. 3. Time perception. 1. Buzsaki, G. II. Series. QP383.T46 1994 599'.0188--dc20 94-12945 CIP This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. © Springer-Verlag Berlin Heidelberg 1994. Softcover reprint of the hardcover I st edition 1994 The use of general descriptive names, registered names, trademarks, etc, in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Product Liability: The publishers cannot guarantee the accuracy of any information about dosage and application contained in this book. In every individual case the user must check such information by consulting the relevant literature. Typesetting: Fotosatz-Service Kohler OHG, 97084 Wiirzburg 27/3130 - 5 4 3 2 1 0 - Printed on acid-free paper Preface To understand how neuronal activity gives rise to mental life is a central issue in modern neuroscience. This "mind-brain" issue has traditionally been a concern for epistemologically-oriented philosophers and theoretical neurobio logists. However, it appears that the time has arrived to shift the theoretical debate to testable hypotheses and laboratory experiments. Whereas it has been accepted by most neuroscientists that the "special" qualities of the brain lie in its unique cooperativity among its parts, it is only now that the technology for revealing these "emergent" or "cooperative" properties is becoming a routine laboratory tool. Importantly, such a "top down" approach coincided with "bottom-up" inquiries about the role of "noisy" brain states such as occuring during sleep. Temporal coding in the brain addresses the pivotal issue of how ensemble oscillations and transient cooperative states of neurons bind together the complex representations of our outer and inner worlds. Some answers to these questions are now emerging and discussed by leading authorities represented in this book. The volume is a result of a memorable symposium held in the fall of 1993, as part of Colloque Medicine et Recherche series by Fondation Ipsen. The hot and controversial dialogue continues and the range of scien tifically attackable topics widens. Such a highly complex issue is therefore the topic of the next Fondation Ipsen symposium: Neurobiology of decision making, Paris, October 24, 1994. GYORGY BUZSAKI, Newark YVES CHRISTEN, Paris Contents The Coding and Processing of Temporal Information in the Electrosensory System of Fish W. Heiligenberg . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Chaotic Oscillations and the Genesis of Meaning in Cerebral Cortex W. J. Freeman and J. M. Barrie ... . . . . . . . . . . . . . . . . . . 13 Synchronization in Neuronal Transmission and Its Importance for Information Processing M. Abeles, Y. Prut, H. Bergman, and E. Vaadia . . . . . . . . . . . 39 Time as Coding Space in Neocortical Processing: A Hypothesis W. Singer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51 Oscillatory Neuronal Activity in Visual Cortex: A Critical Re-Evaluation Y. Fregnac, V. Bringuier, and A. Baranyi ..... 81 Electrocortical Rhythms in the 40 Hz Band in Cat: In Search of Their Behavioral Correlates A. Rougeul-Buser ...................... . 103 Coherent Activities in Corticothalamic Networks During Resting Sleep and Their Development Into Paroxysmal Events M. Steriade . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 115 From Cellular to Network Mechanisms of a Thalamic Synchronized Oscillation T Bal, M. von Krosigk, and D. A. McCormick ........ 129 Oscillatory and Intermittent Synchrony in the Hippocampus: Relevance to Memory Trace Formation G. Buzsilki, A. Bragin, J. J. Chrobak, Z. Nildasdy, A. Sik, M. Hsu, and A. Ylinen .................................... 145 VIII Contents Common Principles in Three Experimental Epilepsies R. D. Traub, J. G. R. Jefferys, and R. Miles . . . . . . . . . . . . . . . . .. 173 Oscillations in the Control of Eye and Head Movements. Are They Due in Part to Supra-Brainstem Synchronising Oscillations? A. Berthoz and P.-P. Vidal . . . . . . . . . . . . . . . . . . . . . . . . . . .. 185 Learning to Generalize from Single Examples in Dynamic Link Architecture W Konen and C. von der Malsburg ...................... 205 Relating Temporal Properties of Spike Trains from Area MT Neurons to the Behavior of the Monkey W Bair, C. Koch, W Newsome, and K. Britten ............... 221 Content and Context in Temporal Thalamocortical Binding R. LUnas, U. Ribary, M. JoUot, and x.-J. Wang. . . . . . . . . . . . . .. 251 Dynamic Cognitive Networks in the Human Brain A. Gevins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 273 In the Perception of Speech Time is of the Essence P. Taltal. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 291 Subject Index .................................... 301 Contributors Abeles, M. Department of Physiology, School of Medicine. The Hebrew University of Jerusalem, P. O. Box 12272, Jerusalem 91-120, Israel Bair, M. Computation and Neural Systems Program, California Institute of Techno logy, Pasadena, CA 91125, USA Bal, T. Section of Neurobiology, Sterling Hall of Medicine, Rm. C303, Yale Univer sity School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA Baranyi, A. Attila Joszef University, H-6701 Szeged, Hungary Barrie, J. M. Department of Molecular and Cell Biology, LSA 129, University of California, Berkeley, CA 94720, USA Bergman, H. Center for Neural Computation, The Hebrew University of Jerusalem, P. O. Box 1172, Jerusalem 91-010, Israel Berthoz, A. Laboratoire de Physiologie de la Perception et de l'Action, College de France-CNRS, 15, rue de l'Ecole de Medecine, F-75270 Paris Cedex 06, France Bragin, A. Institute of Theoretical and Experimental Biophysics, Puschino, Russia Bringuier, V. Institute Alfred Fessard, CNRS, Avenue de la Terrasse, F-91198 Gif sur Yvette, France X Contributors Britten, K. Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA Buzsaki, G. Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102, USA Chrobak, J. J. Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102, USA Freeman, WJ. Department of Molecular and Cell Biology, LSA 129, University of California, Berkeley, CA 94720, USA Fregnac, Y. Institut Alfred Fessard, CNRS, Avenue de la Terasse, F-91198 Gif sur Yvette, France Gevins, A. One Rincon Center, 101 Spear Street, Suite 204, San Francisco, CA 94105, USA H eiligenberg, W Scripps Institute of Oceanography, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0202, USA Hsu,M. Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102, USA Jefferys, J. G. R. Department of Physiology, St. Mary's Hospital Medical School, Imperial College, London W2 1 PG, Great Britain Joliot, M. S.H.F.J.-C.E.A., 4, place du General Leclerc, F-91406 Orsay, France Koch, C. Computation and Neural Systems Program, Division of Biology, 139-74, California Institute of Technology, Pasadena, CA 91125, USA Konen, W Institut fUr Neuroinformatik, Ruhr-Universitiit Bochum, Universitiits straBe 142, D-44799 Bochum, Germany Contributors XI Krosigk, M. von Section of Neurobiology, Sterling Hall of Medicine, Rm. C303, Yale Univer sity School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA Llinas, R. Department of Physiology and Biophysics, New York University Medical Center, 550 First Avenue, New York, NY 10016, USA Maisburg, C. von der Institut fUr Neuroinformatik, Ruhr-Universitat Bochum, Universitats straBe 142, D-44799 Bochum, Germany McCormick, D. A. Section of Neurobiology, Sterling Hall of Medicine, Rm. C303, Yale Univer sity School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA Miles, R. Institut Pasteur, Laboratoire de Neurobiologie Cellulaire, 28 Rue du Dr. Roux, F-75724 Paris Cedex 15, France z. Nadasdy, Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102, USA Newsome, W. Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA Prut, Y. Center for Neural Computation, The Hebrew University of Jerusalem, P. O. Box 1172, Jerusalem 91-010, Israel Ribary, U. Department of Physiology and Biophysics, New York University Medical Center, 550 First Avenue, New York, NY 10016, USA Rouguel-Buser, A. Institut des Neurosciences, CNRS/UPMC, 9, Quai Saint Bernard, F-75005 Paris, France Sik, A. Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, Hungary Singer, W. Max Planck Institute for Brain Research, DeutschordenstraBe 46, D-60528 Frankfurt/Main, Germany XII Contributors Steriade, M. Laboratoire de Neurophysiologie, Faculte de Medecine, Universite Laval, Quebec, Canada G1K 7P4 Tallal, P. Rutgers University, 197 University Avenue, Newark, NJ 07102, USA Traub, R.D. IBM T. J. Watson Research Center, Yorktown Heights, NY 105987, USA; and Department of Neurology, Columbia University, New York, NY 10032, USA Vaadia, E. Center for Neural Computation, The Hebrew University of Jerusalem, P. O. Box 1172, Jerusalem 91-010, Israel Vidal, P.-P. Laboratoire de Physiologie de la Perception et de l'Action, College de France CNRS, 15, rue de l'Ecole de Medecine, F-75270 Paris Cedex 06, France Wang, X.-J. Department of Mathematics, The University of Chicago, 5734 University Avenue, Chicago, IL 60637, USA Ylinen, A. Department of Neurology, University of Kuopio, SF-70211 Kuopio, Finland