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1 :23'Problems in Systems Neuroscience Edited by J. Leo van Hemmen UTATIONAL Terrence J. Seinowski

2 computational Neuroscience Series Editors Michael Strylcer Terrence J. Sejnowski Biophysics of Computation Chistof ICoch 23 Problems in Systems Neuroscience Edited by J. Leo van Hemmen and Terrence J. Sejnowslci

3 23 Problems in Systems Neuroscience Edited by J. Leo van Hemmen Terrence J. Sejnowslci OXFORD UNIVERSITY PRESS

4 OXFORD UNIVERSITY PRESS Oxford University Press, Inc., publishes works that further Oxford University's objective of excellence in research, scholarship, and education. Oxford New Yorlc Aucldand Cape Town Dar es Salaam Hong ICong ICarachi ICuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Copyright O 2006 by Oxford University Press, Inc. Published by Oxford University Press, Inc. 198 Madison Avenue, New Yorlc, New Yorlc Oxford is a registered trademark of Oxford University Press All rights reserved. No part of this 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 the prior permission of Oxford University Press. Library of Congress Cataloging-in-Publication Data 23 problems in systems neuroscience / edited by Leo Van Hemmen and Terrence Sejnowslti. p, cm. Includes bibliographical references and index. ISBN-13: ISBN-10: Neurobiology. 2. Biological systems. I. Title: Twenty three problems in systems neuroscience. 11. Hemmen, J. L, van (Tan Leonard) Sejnowslci, Terrence J. (Terrence Joseph) QP355.2.Al '6--dc Printed in the United States of America on acid-free paper

5 Preface As long as a branch of science offers an abundance of problems, so long is it alive; a lack of problems foreshadows extinction or the cessation of independent development. -David Hilbert in Paris, 8 August 1900 When invited in 1899 to give the opening address at the second International Congress of Mathematicians (ICM) in Paris the following year, David Hilbert ( ), one.of the greatest mathematicians of the last century and the father of Hilbert space, was facing the beginning of a new century. Henri Poincar6, who had a similar task in addressing the first ICM in Zurich, extolled the virtues of what had previously been accomplished in pure mathematics. Rather than focus on the glories of the past, Hilbert chose to make a break with tradition and instead emphasize what was not known. At the ICM on August 8, 1900, he outlined twenty-three key open mathematical problems as challenges to mathematicians for the twentieth century. These problems were influential in shaping the direction of mathematics. To understand Hilbert's motivation, let us retrace his reasoning in the introduction to his lecture entitled Mathematical problems1: The German text appeared in 1900 directly after the Paris meeting in Nachr. Kgl. Ges. d. Wiss. zu GdZtingen, math.-phys. Klnsse 3, It can also be found in volume 3 of Hilbert's collected works ( ). The translation above is by Dr. Mary Winston Newson and was published in 1902 in Bull. Arne,: Math. Soc. 8: : it reappeared in 2000 in Bull. Amer. Math. Soc. (new series) 37:

6 History teaches the continuity of the development of science. We know that every age has its own problems, which the following age either solves or casts aside as profitless and replaces by new ones. If we would obtain an idea of the probable development of mathematical knowledge in the immediate future, we must let the unsettled questions pass before our minds and look over the problems which the science of to-day sets and whose solution we expect from the future. To such a review of problems the present day, lying at the meeting of the centuries, seems to me well adapted. For the close of a great epoch not only invites us to look back into the past but also directs our thoughts to the unknown future. The deep significance of certain problems for the advance of mathematical science in general and the important role that they play in the work of the individual investigator are not to be denied. As long as a branch of science offers an abundance of problems, so long is it alive; a lack of problems foreshadows extinction or the cessation of independent development. Just as every human undertaking pursues certain objects, so also mathematical research requires its problems. It is by the solution of problems that the investigator tests the temper of his steel; he finds new methods and new outloolts, and gains a wider and freer horizon. It is difficult and often impossible to judge the value of a problem correctly in advance; for the final award depends upon the grain which science obtains from the problem. Nevertheless we can ask whether there are general criteria which mark a good mathematical problem. An old French mathematician said: "A mathematical theory is not to be considered complete until you have made it so clear that you can explain it to the &-st man whom you meet on the street." This clearness and ease of comprehension, here insisted on for a mathematical theory, I should still more demand for a mathematical problem if it is to be perfect; for what is clear and easily comprehended attracts, the complicated repels us. As for systems neuroscience, why add more, if-mutatis mutandis-it has all been said so clearly a century ago? The same text, with "mathematical science" replaced by "systems neuroscience," applies to the twenty-first century. The complexity of the brain and the protean nature of behavior remain the most elusive area of science and also the most important. There is no single brilliant individual who could serve as the David Hilbert of systems neuroscience, so we have invited twenty-three experts from the many areas of systems neuroscience to formulate one problem each. We thank the Max Planck Society for hosting a wonderful meeting on "Problems in Systems Neuroscience" in Dresden on September 4 to 8, 2000, that formed the core of the authors in this collection. We have asked several other colleagues to contribute to the twenty-three challenging questions in systems neuroscience that are included. It took Hilbert two years to get his problems published in English. It took us even longer to get the twenty- vi Preface

7 three different essays collected together in this volume. Although it is not comprehensive, and it is, like Hilbert's original list of problems, idiosyncratic, nonetheless it may serve as a source of inspirations for future explorers of the brain. We have organized the chapters into five themes that range from evolution to qualia, each theme posed as a general question. Although each of the chapters was independently written and can be read separately, there are some common issues that reflect contemporary concerns. J. Leo van Hemmen Terrence J. Sejnowski Preface vii

8 Contents Contributors xiii PART I How Have Brains Evolved? 1. Shall We Even Understand the Fly's Brain? 3 Gilles Laurent 2. Can We Understand the Action of Brains in Natural Environments? 22 Hermann wagner and Bernhard Gaese 3. Hemisphere Dominance of Brain Function-Which Functions Are Lateralized and Why? 44 Giinter Ehret PART II How Is the Cerebral Cortex Organized? 4. What Is the Function of the Thalamus? 65 S. Murray Sherman 5. What Is a Neuronal Map, How Does It Arise, and What Is It Good For? 83 J. Leo van Hemmen 6. What Is Fed Back? 103 Jean Bullier

9 PART Ill How Do Neurons Interact? 7. How Can the Brain Be So Fast? 135 WuIfram Gerstner 8. What Is the Neural Code? 143 C. van Vreeswijk 9. Are Single Cortical Neurons Soloists or Are They Obedient Members of a Huge Orchestra? 160 Tal Icenet, Amos Arieli, Misha Tsodylzs, and Amiram Grinvald 10. What Is the Other 85 Percent of V1 Doing? 182 Bruno A. Olshausen and David J. Field PART IV What Can Brains Compute? 11. Which Computation Runs in Visual Cortical Columns? 2 15 Steven W, Zucker 12. Are Neurons Adapted for Specific Computations? Examples from Temporal Coding in the Auditory System 245 C. E. Carr, S. Iyer, D. Soares, S. IGzlluri, and J. Z. Simon 13. How Is Time Represented in the Brain? 266 Andreas V. M. Herz 14. How General Are Neural Codes in Sensory Systems? 283 David McAlpine and Alan R. Palmer, 15. How Does the Hearing System Perform Auditory Scene Analysis? 303 Georg M. Iclump 16. How Does Our Visual System Achieve Shift and Size Invariance? 322 Laurenz Wiskott PART V Organization of Cognitive Systems 17. What Is Reflected in Sensory Neocortical Activity: External Stimuli or What the Cortex Does with Them? 343 Henning Scheich, Frank W. Ohl, Holger Schulze, Andreas Hess, and Andre' Brechmann x Contents

10 18. Do Perception and Action Result from Different Brain Circuits? The Three Visual Systems Hypothesis 367 Giacomo Rizzolatti and Vittorio Gallese 19. What Are the Projective Fields of Cortical Neurons? 394 Terrence J. Sejnowslzi 20. How Are the Features of Objects Integrated into Perceptual Wholes That Are Selected by Attention? 406 John R Reynolds 21. Where Are the Switches on This Thing? 423 L. F. Abbott 22. Synesthesia: What Does It Tell Us about the Emergence of Qualia, Metaphor, Abstract Thought, and Language? 432 V. S. Ramachandran and Edward M. Hubbard 23. What Are the Neuronal Correlates of Consciousness? 474 Francis C. Crick and Christof Koch Author Index 49 1 Subject Index 505 Contents xi

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