Dynamic Coordination in the Brain From Neurons to Mind EDITED BY Christoph von der Malsburg, William A. Phillips, and Wolf Singer STRÜNGMANN FORUM REPORTS Dynamic Coordination in the Brain From Neurons to Mind Strüngmann Forum Reports Julia Lupp, series editor The Ernst Strüngmann Forum is made possible through the generous support of the Ernst Strüngmann Foundation, inaugurated by Dr. Andreas and Dr. Thomas Strüngmann. This Forum was supported by funds from the Deutsche Forschungsgemeinschaft (German Science Foundation) Dynamic Coordination in the Brain From Neurons to Mind Edited by Christoph von der Malsburg, William A. Phillips, and Wolf Singer Program Advisory Committee: Sten Grillner, William A. Phillips, Steven M. Silverstein, Wolf Singer, Olaf Sporns, and Christoph von der Malsburg The MIT Press Cambridge, Massachusetts London, England © 2010 Massachusetts Institute of Technology and the Frankfurt Institute for Advanced Studies Series Editor: J. Lupp Assistant Editor: M. Turner Photographs: U. Dettmar Typeset by BerlinScienceWorks All rights reserved. No part of this book may be reproduced in any form by electronic or mechanical means (including photocopying, recording, or information storage and retrieval) without permission in writing from the publisher. MIT Press books may be purchased at special quantity discounts for business or sales promotional use. For information, please email [email protected] or write to Special Sales Department, The MIT Press, 55 Hayward Street, Cambridge, MA 02142. The book was set in TimesNewRoman and Arial. Printed and bound in the United States of America. Library of Congress Cataloging-in-Publication Data Ernst Strüngmann Forum (5th : 2009 : Frankfurt am Main, Germany) Dynamic coordination in the brain : from neurons to mind / edited by Christoph von der Malsburg, William A. Phillips, and Wolf Singer. p. ; cm. — (Strüngmann Forum reports) Fifth Ernst Strüngmann Forum held Aug. 16–21, 2009, Frankfurt am Main. Includes bibliographical references and index. ISBN 978-0-262-01471-7 (hardcover : alk. paper) 1. Neural circuitry—Congresses. 2. Brain—Localization of functions— Congresses. 3. Cognitive neuroscience—Congresses. I. Malsburg, Christoph von der, 1942– II. Phillips, William A., 1936– III. Singer, W. (Wolf) IV. Title. V. Series: Strüngmann Forum reports. [DNLM: 1. Brain—physiology—Congresses. 2. Brain—physiopathology— Congresses. 3. Cognition—physiology—Congresses. 4. Neural Pathways— physiology—Congresses. 5. Neurons—physiology—Congresses. 6. Psychophysiology—Congresses. WL 300 E727d 2010] QP363.3.E76 2009 612.8'2—dc22 2010014715 10 9 8 7 6 5 4 3 2 1 Contents The Ernst Strüngmann Forum vii List of Contributors ix Preface xiii 1 Dynamic Coordination in Brain and Mind 1 William A. Phillips, Christoph von der Malsburg, and Wolf Singer 2 Cortical Circuits: Consistency and Variability 25 across Cortical Areas and Species Jon H. Kaas 3 Sequence Coding and Learning 35 Gilles Laurent 4 What Can Studies of Comparative Cognition Teach 43 Us about the Evolution of Dynamic Coordination? Uri Grodzinski and Nicola S. Clayton 5 Evolution of Dynamic Coordination 59 Evan Balaban, Shimon Edelman, Sten Grillner, Uri Grodzinski, Erich D. Jarvis, Jon H. Kaas, Gilles Laurent, and Gordon Pipa 6 Modeling Coordination in the Neocortex at the 83 Microcircuit and Global Network Level Anders Lansner and Mikael Lundqvist 7 Oscillation-supported Information Processing and Transfer 101 at the Hippocampus–Entorhinal–Neocortical Interface György Buzsáki and Kamran Diba 8 What Are the Local Circuit Design Features 115 Concerned with Coordinating Rhythms? Miles A. Whittington, Nancy J. Kopell, and Roger D. Traub 9 Coordination in Circuits 133 Mayank Mehta, György Buzsáki, Andreas Kreiter, Anders Lansner, Jörg Lücke, Kevan Martin, Bita Moghaddam, May-Britt Moser, Danko Nikoli, and Terrence J. Sejnowski 10 Coordination: What It Is and Why We Need It 149 Christoph von der Malsburg 11 Neocortical Rhythms: An Overview 159 Wolf Singer 12 Stimulus-driven Coordination of Cortical Cell 169 Assemblies and Propagation of Gestalt Belief in V1 Yves Frégnac, Pedro V. Carelli, Marc Pananceau, and Cyril Monier vi Contents 13 Coordination in Brain Systems 193 Edvard I. Moser, Maurizio Corbetta, Robert Desimone, Yves Frégnac, Pascal Fries, Ann M. Graybiel, John-Dylan Haynes, Laurent Itti, Lucia Melloni, Hannah Monyer, Wolf Singer, Christoph von der Malsburg, and Matthew A. Wilson 14 “Hot Spots” and Dynamic Coordination in Gestalt Perception 215 Ilona Kovács 15 Coordination in Sensory Integration 229 Jochen Triesch, Constantin Rothkopf, and Thomas Weisswange 16 Neural Coordination and Human Cognition 235 Catherine Tallon-Baudry 17 Failures of Dynamic Coordination in Disease States 245 and Their Implications for Normal Brain Function Steven M. Silverstein 18 Coordination in Behavior and Cognition 267 Andreas K. Engel, Karl Friston, J. A. Scott Kelso, Peter König, Ilona Kovács, Angus MacDonald III, Earl K. Miller, William A. Phillips, Steven M. Silverstein, Catherine Tallon-Baudry, Jochen Triesch, and Peter Uhlhaas Bibliography 301 Subject Index 345 The Ernst Strüngmann Forum Founded on the tenets of scienti c independence and the inquisitive nature of the human mind, the Ernst Strüngmann Forum is dedicated to the continual expansion of knowledge. Through its innovative communication process, the Ernst Strüngmann Forum provides a creative environment within which ex- perts scrutinize high-priority issues from multiple vantage points. This process begins with the identi cation of themes. By nature, a theme constitutes a problem area that transcends classic disciplinary boundaries. It is of high-priority interest and requires concentrated, multidisciplinary input to address the issues involved. Proposals are received from leading scientists active in their eld and are selected by an independent Scienti c Advisory Board. Once approved, a steering committee is convened to re ne the scienti c parameters of the proposal and select the participants. Approximately one year later, a focal meeting is held to which circa forty experts are invited. Preliminary discussion around this theme began in the hallways of FIAS in 2007, shortly after Christoph von der Malsburg and I arrived in Frankfurt. Our talks expanded to include Bill Phillips, who was visiting FIAS at the time, and Wolf Singer. In August, 2008, the steering committee—comprised of Sten Grillner, Bill Phillips, Steve Silverstein, Wolf Singer, Olaf Sporns, and Christoph von der Malsburg—met to identify the key issues for debate and select the participants for the focal meeting, which was held in Frankfurt am Main, Germany, from August 16–21, 2009. The activities and discourse surrounding a Forum begin well before par- ticipants arrive in Frankfurt and conclude with the publication of this volume. Throughout each stage, focused dialog is the means by which participants examine the issues anew. Often, this requires relinquishing long-established ideas and overcoming disciplinary idiosyncrasies that might otherwise inhibit joint examination. However, when this is accomplished, a unique synergism results and new insights emerge. This volume conveys the synergy that arose from a group of diverse ex- perts, each of whom assumed an active role, and is comprised of two types of contributions. The rst provides background information on key aspects of the overall theme. These chapters have been extensively reviewed and revised to provide current understanding of the topics. The second (Chapters 5, 9, 13, and 18) summarizes the extensive discussions that transpired. These chapters should not be viewed as consensus documents nor are they proceedings; they transfer the essence of the discussions, expose the open questions that still remain, and highlight areas for future research. An endeavor of this kind creates its own unique group dynamics and puts demands on everyone who participates. Each invitee contributed not only their viii The Ernst Strüngmann Forum time and congenial personality, but a willingness to probe beyond that which is evident, and I wish to extend my sincere gratitude to all. A special word of thanks goes to the steering committee, the authors of the background pa- pers, the reviewers of the papers, and the moderators of the individual working groups (Sten Grillner, Terry Sejnowski, Bob Desimone, and Steve Silverstein). To draft a report during the Forum and bring it to its [ nal form in the months thereafter is no simple matter, and for their efforts, we are especially grateful to Evan Balaban, Mayank Mehta, Edvard Moser, and Andreas Engel. Most importantly, I wish to extend my appreciation to the chairpersons, Christoph von der Malsburg, Bill Phillips, and Wolf Singer, whose support throughout this project was invaluable. A communication process of this nature relies on institutional stability and an environment that encourages free thought. The generous support of the Ernst Strüngmann Foundation, established by Dr. Andreas and Dr. Thomas Strüngmann in honor of their father, enables the Ernst Strüngmann Forum to conduct its work in the service of science. In addition, the following valu- able partnerships are gratefully acknowledged: the Scienti c Advisory Board, which ensures the scienti c independence of the Forum; the German Science Foundation, which provided nancial support for this theme; and the Frankfurt Institute for Advanced Studies, which shares its vibrant intellectual setting with the Forum. Long-held views are never easy to put aside. Yet, when