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Brain Dynamics Series Induced Rhythms in the Brain

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Page 1: Brain Dynamics Series - Springer

Brain Dynamics Series

Induced Rhythms in the Brain

Page 2: Brain Dynamics Series - Springer

Brain Dynamics Series

Induced Rhythms in the Brain

Edited by

E. Ba§ar T.R. Bullock

Preface by V.B. Mountcastle

With 93 figures, some in color

Springer Science+Business Media, LLC

Page 3: Brain Dynamics Series - Springer

Eroi Başar Institute of Physiology Medical University Liibeck Ratzeburger Allee 160 D-2400 Liibeck I GERMANY

Theodore H. Bullock Department of Neurosciences, 0201 University of California, San Diego La Iolla, CA 92093 USA

Library of Congress Cataloging-in-Publication Data lnduced rhythms in the brain / edited by E. Başar, T.H. Bullock;

preface by V.B. Mountcastle. p. cm. - (Brain d ynamics series)

Inc\udes bibliographical references and index. ISBN 0-8176-3537-8 (alk. paper). - ISBN 3-7643-3537-8 (alk. paper)

1. Vis ual cortex. 2. Electroencephalography. 3. Visual evoked response. 1. Başar, EroI. II. Bullock, Theodore Holmes. III. Series.

[DNLM: 1. Brain-physiology. 2. Evoked Potentials. 3. Periodicity. WL 300 142] QP383.l2.I53 1991 612.8'2-dc20 DNLM/DLC for Library ofCongress 92-7081

CIP

Printed on acid-free paper.

© Springer Science+Business Media New York, 1992 Copyright is not claimed for works ofU.S. Government employees.

Originally published byBirkhăuser Boston in 1992 Softcover reprint ofthe hardcover 1 st edition 1992

AII rights reserved. No part ofthis publication may be reproduced, stored in a retrieval system or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without prior permission of the copyright owner. The use of general descriptive names, trademarks, etc. in this publication even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone. While the advice and information in this book are believed to be true and accurate at the date of going to press, neither the authors nor the editors nor the publisher can accept any legal responsi­bility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Permission to photocopy for intern al or personal use, or the internal or personal use of specific c\ients, is granted by Springer Science+Business Media, LLC for libraries and other users registered with the Copyright

Clearance Center (CCC), provided that the base fee of $0.00 per copy, plus $0.20 per page is paid directly to CCC, 21 Congress Street, Salem, MA 01970, U.S.A. Special requests should be addressed directly to Springer Science+Business Media, LLC

ISBN 978-1-4757-1283-4 ISBN 978-1-4757-1281-0 (eBook) DOI 10.1007/978-1-4757-1281-0

Typeset by Asco Trade Typesetting Ltd., Hong Kong.

9 8 7 6 5 4 3 2 1

Page 4: Brain Dynamics Series - Springer

Brain Dynamics

Series Editors:

Erol Ba~ar (Editor in Chief), Medical University of Lubeck W.J. Freeman, University of Cali fomi a, Berkeley W.-D. Heiss, Max-Planck-Institut fUr Neurologische Forschung D. Lehmann, University Hospital, Zurich F.H. Lopes da Silva, University of Amsterdam E.-J. Speckmann, University of Munster

Books in the Series:

Dynamics of Sensory and Cognitive Processing by the Brain E. Ba~ar, editor ISBN 0-387-16994-6

Brain Dynamics: Progress and Perspectives E. Ba~ar and T.H. Bullock, editors ISBN 0-387-50867-8

Chaos in Brain Function E. Ba~ar, editor ISBN 0-387-52329-4

Induced Rhythms in the Brain E. Ba~ar and T.H. Bullock, editors ISBN 0-8176-3537-8

Forthcoming:

Slow Potential Changes in the Brain W. Haschke, E.-1. Speckmann, and A. Roitbak, editors ISBN 0-8176-3583-1

Page 5: Brain Dynamics Series - Springer

Publisher's Note

With this volume, the publication of the Brain Dynamics Series is being trans­ferred from Springer-Verlag Heidelberg to Birkhauser Boston.

The aim of this Series continues to be the publication of monographs and multi-authored subject collections in interdisciplinary neuroscience research, clinical as well as basic, with emphasis on "brain dynamics", the complex interactions of the ever-changing states of the brain's machinery.

The transfer of the Series (of which most of the Editors are European) to Birkhauser Boston will further reaffirm the importance of international coop­eration in research on the brain, and help strengthen the neuroscience publi­cation bridge between scientists in Europe and in the United States.

Books in the Brain Dynamics Series will include the following subject areas:

EEG, MEG, evoked and event-related brain responses Neural populations and neural networks Neuropathology and brain function Model epilepsies Brain imaging Dynamics of neural populations at the cellular level Comparative neurophysiology Chaotic dynamics in brain function Cognitive functions of the brain

Page 6: Brain Dynamics Series - Springer

Contents

Contributors

Preface Vernon B. Mountcastle

Introduction to Induced Rhythms: A Widespread, Heterogeneous Class of Oscillations Theodore H. Bullock ..................................... .

Oscillations in the Striate Cortex

1 Mechanisms Underlying the Generation of Neuronal Oscillations in Cat Visual Cortex Charles M. Gray, Andreas K. Engel, Peter Konig,

Xlll

xvii

and Wolf Singer ......................................... 29

2 Stimulus-Specific Synchronizations in Cat Visual Cortex: Multiple Microelectrode and Correlation Studies from Several Cortical Areas Reinhard Eckhorn, Thomas Schanze, Michael Brosch, Wageda Salem, and Roman Bauer .......................... 47

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x Contents

Cortical Rhythms. Ongoing (EEG) and Induced (ERPs)

3 The Rhythmic Slow Activity (Theta) of the Limbic Cortex: An Oscillation in Search of a Function Fernando Lopes da Silva .................................. 83

4 Is There any Message Hidden in the Human EEG? Hellmuth Petsche and Peter Rappelsberger ................... 103

5 Event-Related Synchronization and Desynchronization of Alpha and Beta Waves in a Cognitive Task Gert Pfurtscheller and Wolfgang Klimesch ................... 117

6 Magnetoencephalographic Evidence for Induced Rhythms Knud Saermark. Keld B. Mikkelsen. and Erol Ba§ar ........... 129

7 Rostrocaudal Scan in Human Brain: A Global Characteristic of the 40-Hz Response During Sensory Input Rodolfo R. Uinas and Urs Ribary .......................... 147

8 Evoked Potentials: Ensembles of Brain Induced Rhythmicities in the Alpha, Theta and Gamma Ranges Erol Ba§ar. Canan Ba§ar-Eroglu. Ralph Parnejjord. Elke Rahn and Martin Schurmann .................................... 155

9 Predictions on Neocortical Dynamics Derived from Studies in Paleocortex Walter J. Freeman ....................................... 183

10 A Comparison of Certain Gamma Band (40-HZ) Brain Rhythms in Cat and Man Robert Galambos ........................................ 201

11 Human Visual Evoked Potentials: Induced Rhythms or Separable Components? George R. M angun ....................................... 217

Thalamic Oscillations

12 Network Properties of the Thalamic Clock: Role of Oscillatory Behavior in Mood Disorders Gy8rgyBuzsaki .......................................... 235

Page 8: Brain Dynamics Series - Springer

Contents

13 Mesopontine Cholinergic Systems Suppress Slow Rhythms and Induce Fast Oscillations in Thalamocortical Circuits

XI

Mircea Steriade, Roberto Curro Dossi, and Denis Pare ,......... 251

14 Oscillations in CNS Neurons: A Possible Role for Cortical Interneurons in the Generation of 40-Hz Oscillations Rodolfo R. Llinas ........................................ 269

Cellular and Subcellular Mechanisms Based on Invertebrate and Simple Systems

15 Modification of Oscillator Function by Electrical Coupling to Nonoscillatory Neurons Eve Marder, L.F. Abbott, Thomas B. Kepler, and Scott L. Hooper .......................................... 287

16 Biological Timing: Circadian Oscillations, Cell Division, and Pulsatile Secretion Felix Strumwasser

17 Comparison of Electrical Oscillations in Neurons with Induced or Spontaneous Cellular Rhythms due to Biochemical Regulation

297

Albert Goldbeter ......................................... 309

18 Signal Functions of Brain Electrical Rhythms and their Modulation by External Electromagnetic Fields W Ross Adey ........................................... 325

Theories and Models

19 Inhibitory Interneurons can Rapidly Phase-Lock Neural Populations William W Lytton and Terrence J. Sejnowski ................. 357

20 The Problem of Neural Integration: Induced Rhythms and Short-Term Correlations Giulio Tononi, Olaf Sporns, and Gerald M. Edelman ............ 367

21 Flexible Linking of Visual Features by Stimulus-Related Synchronizations of Model Neurons Reinhard Eckhorn, Peter Dicke, Martin Arndt and Herbert Reitboeck ....................................... 397

Page 9: Brain Dynamics Series - Springer

XII Contents

22 Synergetics of the Brain: An Outline of Some Basic Ideas H. Haken ............................................... 417

Epilogue

Brain Natural Frequencies are Causal Factors for Resonances and Induced Rhythms Erol Baljar .............................................. 425

Index ....................................................... 469

Page 10: Brain Dynamics Series - Springer

Contributors

WRossAdey Pettis Memorial Veteran's Hospital Lorna Linda, California, USA

L. F. Abbott Brandeis University Waltham, Massachusetts, USA

Martin Arndt Institut fiir Angewandte Physik und

Biophysik Philipps-Universitat Marburg Marburg, Germany

Erol Ba~ar Institut fiir Physiologie Medizinische Universitat Lubeck Lubeck, Germany

Canan Baliar-Eroglu Institut fur Physiologie Medizinische Universitiit Lubeck Lubeck, Germany

Roman Bauer Institut fiir Angewandte Physik und

Biophysik Philipps-Universitiit Marburg Marburg, Germany

Michael Brosch Institut fiir Angewandte Physik und

Biophysik Philipps-Universitiit Marburg Marburg, Germany

Theodore H. Bullock Department of Neurosciences 0201 University of California, San Diego La Jolla, California, USA

Gyorgy Buzsaki Center for Molecular and Behavioral

Neuroscience Rutgers University Newark, New Jersey, USA

Roberto Curro Dossi Universite Laval Faculte de Medecine Cite Universitaire Quebec, Canada

Peter Dicke Institut fiir Angewandte Physik und

Biophysik Philipps-Universitiit Marburg Marburg, Germany

Page 11: Brain Dynamics Series - Springer

XIV

Reinhard Eckhorn Institut fiir Angewandte Physik und

Biophysik Philipps-Universitat Marburg Marburg, Germany

Gerald M. Edelman The Neurosciences Institute of the

Neurosciences Research Program New York, New York, USA

Andreas K. Engel Neurophysiologische Abteilung Max-Planck-Institut fiir Hirnforschung Frankfurt, Germany

Walter J. Freeman Department of Molecular & Cell Biology Division of Neurobiology University of California Berkeley, California, USA

Robert Galambos University of California at San Diego School of Medicine La Jolla, California, USA

Albert Goldbeter Faculte des Sciences Universite Libre de Bruxelles Bruxelles, Belgium

Charles M. Gray The Salk Institute for Biological Studies San Diego, California, USA

H.Haken Institut fiir Theoretische Physik und

Synergetik Universitat Stuttgart Stuttgart, Germany

Scott L. Hooper Department of Biology Brandeis University Waltham, Massachusetts, USA

Thomas B. Kepler Department of Physiology and Biophysics Mt. Sinai Medical School New York, New York, USA and Center for Neurobiology and Behavior College of Physicians and Surgeons of

Columbia University New York, New York, USA

Contributors

Wolfgang Klimesch Department of Physiological Psychology Institute of Psychology University of Salzburg Salzburg, Austria

Peter Konig Neurophysiologische Abteilung Max-Planck-Institut fiir Hirnforschung Frankfurt, Germany

Rodolfo R. Llinas Department of Physiology & Biophysics NYU Medical Center New York, New York, USA

Fernando Lopes da Silva Department of Experimental Zoology University of Amsterdam Amsterdam, The Netherlands

William W Lytton Computational Neurobiology Laboratory Howard Hughes Medical Institute The Salk Institute for Biological Studies La Jolla, California, USA

George R. M angun Department of Psychiatry and Program in

Cognitive Neuroscience Dartmouth Medical School Hanover, New Hampshire, USA

Eve Marder Department of Biology Brandeis University Waltham, Massachusetts, USA

Keld B. Mikkelsen Laboratory of Physics I Technical University of Denmark Lyngby, Denmark

Vernon B. Mountcastle Philip Bard Labs of Neurophysiology Johns Hopkins University School

of Medicine Baltimore, Maryland, USA

Denis Pare Universite Laval Faculte de Medecine Cite Universitaire Quebec, Canada

Page 12: Brain Dynamics Series - Springer

Contributors

Ralph ParnefJord Institut fiir Physiologie Medizinische Universitat Liibeck Liibeck, Germany

Hellmuth Petsche Institut fiir Neurophysiologie­

Hirnforschung Universitat Wien Wien, Austria

Gert Pfurtscheller Department of Medical Informatics Institute of Biomedical Engineering Graz University of Technology Graz, Austria

Elke Rahn Institut fiir Physiologie Medizinische Universitat Liibeck Liibeck, Germany

Peter Rappelsberger Institut fiir Neurophysiologie­

Hirnforschung Universitat Wien Wien, Austria

Herbert Reitboeck Institut fiir Angewandte Physik und

Biophysik Philipps-Universitat Marburg Marburg, Germany

Urs Ribary Department of Physiology and Biophysics NYU Medical Center New York, New York, USA

Knud Saermark Laboratory of Physics I Technical University of Denmark Lyngby, Denmark

Wageda Salem Institut fiir Angewandte Physik und

Biophysik Philipps-Universitat Marburg Marburg, Germany

Thomas Schanze Institut fiir Angewandte Physik und

Biophysik Philipps-Universitat Marburg Marburg, Germany

Martin Schiirmann Institut fiir Physiologie Medizinische Universitat Liibeck Liibeck, Germany

Terrence J. Sejnowski Computational Neurobiology Laboratory Howard Hughes Medical Institute The Salk Institute for Biological Studies La Jolla, California, USA

Wolf Singer Neurophysiologische Abteilung Max-Planck-Institut fiir Hirnforschung Frankfurt, Germany

Olaf Sporns The Neurosciences Institute of the

Neurosciences Research Program New York, New York, USA

Mircea Steriade Universite Laval Faculte de Medecine Cite Universitaire Quebec, Canada

Felix Strumwasser Marine Biological Laboratory Woods Hole, Massachusetts, USA

Giulio Tononi The Neurosciences Institute of the

Neurosciences Research Program New York, New York, USA

xv

This book derives in part from a work session organized and chaired by Professors Ba~ar and Bullock and hosted by the Neurosciences Institute of the Neurosciences Research Pro­gram, Rockefeller University, April 9-11, 1990. The support of this organization is gratefully acknowledged.

Page 13: Brain Dynamics Series - Springer

Preface

It is easy to imagine the excitement that pervaded the neurological world in the late 1920's and early 1930's when Berger's first descriptions of the electro­encephalogram appeared. Berger was not the first to discover that changes in electric potential can be recorded from the surface of the head, but it was he who first systematized the method, and it was he who first proposed that explanatory correlations might be found between the electroencephalogram, brain processes, and behavioral states. An explosion of activity quickly fol­lowed: studies were made of the brain waves in virtually every conceivable behavioral state, ranging from normal human subjects to those with major psychoses or with epilepsy, to state changes such as the sleep-wakefulness transition. There evolved from this the discipline of Clinical Electroencepha­lography which rapidly took a valued place in clinical neurology and neuro­surgery. Moreover, use of the method in experimental animals led to a further understanding of such state changes as attention-inattention, arousal, and sleep and wakefulness. The evoked potential method, derived from electro­encephalography, was used in neurophysiological research to construct pre­cise maps of the projection of sensory systems upon the neocortex. These maps still form the initial guides to studies of the cortical mechanisms in sensation and perception. The use of the event-related potential paradigm has proved useful in studies of the brain mechanisms of some cognitive functions of the brain.

The use of electroencephalography in the study of basic brain mechanisms reached a peak in the 1940-50's; thereafter such studies plateaued and ceased to be attractive to most experimental neuroscientists. I believe this was due to the growing conviction that while slow wave events recorded from the surface

Page 14: Brain Dynamics Series - Springer

XV1l1 Preface

of the head or the brain itself might reflect some aspects of behavioral states, their study had, in spite of herculean efforts, revealed little of brain mecha­nisms. The central questions became as follows. Are slow wave events passive epiphenomena in the sense that they reflect summed potential changes caused by the net ionic current flow through the extracellular space of the brain, currents produced by cellular events of several types? Indeed, the net current flow at any moment might very well be produced by any of a variety of patterns of actions in the populations of neurons contributing to it. Or, con­trarily, are at least some slow wave events active agents of signal transmission within and between neuronal populations? The first proposition came to dominate main-stream thinking in neuroscience for several decades.

Rather suddenly, however, a paradigm change is upon us, for the proposi­tion that slow wave events are active agents for signal transmission now stands as a testable hypothesis with some evidence to support it. Such a radical change has not occurred by chance. It is due to the development of new theories and concepts, new methods of data collection and analysis, and more importantly to skillful studies over a long period of time by investiga­tors like Freeman, Bullock, Petsche, Ba~ar and Galambos, followed now by a host of others. Many of these individuals have contributed to the present volume. All neuroscientists are indebted to them for opening-for re-opening -this old and now once again new window through which to observe the workings of the brain.

This book deals with a particular class of slow wave events-the induced rhythms. Bullock emphasizes in a masterly introduction that induced brain rhythms have been studied for a long time and were frequently surmised by earlier investigators to be related to higher order brain functions. He defines them as a widespread, heterogeneous class of oscillations that includes a rhythm not present in the stimulus-an oscillation caused or modulated by stimuli or state changes that do not directly drive the successive cycles of the slow wave rhythm; thus they differ from both spontaneous and driven oscilla­tions. Interest in these phenomena was stimulated anew in the decades of the 1960's and 1970's by the seminal studies of Walter Freeman and his col­leagues on the olfactory system. Study of induced rhythms has now been extended to include many neural systems in many species, in a number of different behavioral states. The general proposition driving the field is that the stimulus induced slow wave oscillations are related to / are signs of/generate or are generated by / are representations of/those higher-order neural opera­tions intercalated between initial central sensory processing and such com­plex brain functions as perception, or the willing and execution of movement patterns, or storage in memory-in short, those functions whose study makes up a large part of what is now called by the inclusive term of Cognitive Neuroscience. Currently, the most actively investigated and potentially illu­minating derivative hypothesis is that the oscillations induced by sensory stimuli in spatially separate parts of a cortical sensory area, or in different cortical areas or other brain regions constitute, when coherent, a mechanism

Page 15: Brain Dynamics Series - Springer

Preface XIX

for binding together neural activities evoked by parts of complex stimuli into correlated activity in distributed neural ensembles. When that activity is co­herent it is thought to be important in generating the neural basis of holistic perceptions like pattern recognition; when incoherent it is not. How far this idea will lead is uncertain, but all will recognize its heuristic value.

The chapters in this book are written by active investigators who provide here a cross section of the state of knowledge in the field. Different ones of these scientists hold different views concerning the active agent/passive epiphenomenon question described above. Regardless of the outcome of that debate, the studies described in this book provide a mass of new information about the function of the brain, function viewed from a different perspective than that of presently received opinion. It is thus of great interest and impor­tance for all neuroscientists.

Philip Bard Laboratories of Neurophysiology Johns Hopkins University School of Medicine

Vernon B. Mountcastle