Table Of ContentRESEARCH 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
