COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY
VOLUME LV COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY
VOLUME LV
The B rain
COLD SPRING HARBOR LABORATORY PRESS 1990 COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY VOLUME LV 9 1990 by The Cold Spring Harbor Laboratory Press International Standard Book Number 0-87969-059-3 (cloth) International Standard Book Number 0-87969-060-7 (paper) International Standard Serial Number 0091-7451 Library of Congress Catalog Card Number 34-8174
Printed in the United States of America All rights reserved
COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY
Founded in 1933 by REGINALD G. HARRIS Director of the Biological Laboratory 1924 to 1936
Previous Symposia Volumes
I (1933) Surface Phenomena XXVI (1961) Cellular Regulatory Mechanisms II (1934) Aspects of Growth XXVII (1962) Basic Mechanisms in Animal Virus Biology III (1935) Photochemical Reactions XXVII1 (1963) Synthesis and Structure of Macromolecules IV (1936) Excitation Phenomena XXIX (1964) Human Genetics V (1937) Internal Secretions XXX (1965) Sensory Receptors V1 (1938) Protein Chemistry XXXI (1966) The Genetic Code VII (1939) Biological Oxidations XXXI1 (1967) Antibodies VIII (1940) Permeability and ~he Nature of Cell Membranes XXXIII (1968) Replication of DNA in Microorganisms IX (1941) Genes and Chromosomes: Structure and Organi- XXXIV (1969) The Mechanism of Protein Synthesis zation XXXV (1970) Transcription of Genetic Material X (1942) The Relation of Hormones to Development XXXVI (1971) Structure and Function of Proteins at the XI (1946) Heredity and Variation in Microorganisms Three-dimensional Level XII (1947) Nucleic Acids and Nucleoproteins XXXVII (1972) The Mechanism of Muscle Contraction XIII (1948) Biological Applications of Tracer Elements XXXVII1 (1973) Chromosome Structure and Function XIV (1949) Amino Acids and Proteins XXXIX (1974) Tumor Viruses XV (1950) Origin and Evolution of Man XL (1975) The Synapse XVI (1951) Genes and Mutations XLI (1976) Origins of Lymphocyte Diversity XVII (1952) The Neuron XLII (1977) Chromatin XVIII (1953) Viruses XL[II (1978) DNA: Replication and Recombination XIX (1954) The Mammalian Fetus: Physiological Aspects of XLIV (1979) Viral Oncogenes Development XLV (1980) Movable Genetic Elements XX (1955) Population Genetics: The Nature and Causes of XLVI (1981) Organization of the Cytoplasm Genetic Variability in Population XLVII (1982) Structures of DNA XXI (1956) Genetic Mechanisms: Structure and Function XLVIll (1983) Molecular Neurobiology XXII (1957) Population Studies: Animal Ecology and De- XLIX (1984) Recombination at the DNA Level mography L (1985) Molecular Biology of Development XXII1 (1958) Exchange of Genetic Material: Mechanism and LI (1986) Molecular Biology of Homo sapiens Consequences LII (1987) Evolution of Catalytic Function XXIV (1959) Genetics and Twentieth Century Darwinism LIII (1988) Molecular Biology of Signal Transduction XXV (1960) Biological Clocks LIV (1989) Immunological Recognition
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ABELIOVICH, ASA, Dept. of Biology, Massachu- BERG, HOWARD, Dept. of Cellular and Develop- setts Institute of Technology, Cambridge mental Biology, Harvard University, Cam- ADAMS, PAUL, Dept. of Neurobiology and Be- bridge havior, Howard Hughes Medical Institute, BHUSHAN, VIKAS, University of California School State University of New York, Stony Brook of Medicine, San Francisco ADEREM, ALAN, Dept. of Cellular Physiology and Brzzi, EMILIO, Dept. of Brain and Cognitive Sci- Immunology, Rockefeller University, New ences, Massachusetts of Technology, Cam- York, New York bridge AGOSTON, DENES, Laboratory of Cell Biology and BLAKEMORE, COLIN, Dept. of Physiology, Uni- National Institute of Mental Health, Nation- versity of Oxford, England al Institutes of Health, Bethesda, Maryland BLISS, TIMOTHY, Dept. of Neurophysiology and ALBERINI, CRISTINA, Instituto di Chimica, Faculty Neuropharmacology, National Institute for of Medicine, University of Brescia, Italy Medical Research, London, England ALDRICH, RICHARD,Dept. of Neurobiology, Stan- BONHOEFFER, FRIEDRICH,Abteilung Physikalische ford University School of Medicine, Cali- Biologie, Max-Planck Institut, Tubingen, fornia Federal Republic of Germany ALLMAN, JOHN, Dept. of Biology, California In- BONHOEFFER, TOBIAS, Neurobiology Laboratory, stitute of Technology, Pasadena Rockefeller University, New York, New ALTMAN, JENNIFER, Saunders Scientific Publica- York tions, London, England BOWER, JAMES, Dept. of Biology, California Insti- ANDERSEN, PER, Institute of Neurophysiology, tute of Technology, Pasadena University of Oslo, Norway BRANDWEIN, HARVEY, Pall Corporation, Glen ANDERSEN, RICHARD, Dept. of Brain and Cogni- Cove, New York tive Sciences, Massachusetts Institute of BREFORT, GEORCES, Research Directorate, Technology, Cambridge Rhone-Poulenc/Sante, Antony, France ANDERSON, DAVID, Dept. of Biology, California BucK, L1NDA, Howard Hughes Medical Institute, Institute of Technology, Pasadena Columbia University College of Physicians & AXLE, RICHARD, Institute of Cancer Research, Surgeons, New York, New York Columbia University College of Physicians & BUELL, GARY, Pharmacia Genetics, La Jolla, Surgeons, New York, New York California BADING, HILMAR, Dept. of Neurobiology and BURROUS, MARY, Dept. of Neurobiology, Rocke- Molecular Genetics, Harvard Medical feller University, New York, New York School, Boston, Massachusetts BuscH, CHRISTOPI~ER, Dept. of Medical Re- BARABAN, JAY, Dept. of Neur0science, Johns search, Max-Planck Institut, Heidelberg, Hopkins University School of Medicine, Bal- Federal Republic of Germany timore, Maryland BUTMAN, JOHN, Dept. of Biology, Washington BARGMANN, COR1, Dept. of Biology, Massachu- University, St. Louis, Missouri setts Institute of Technology, Cambridge BYRNE, JOHN, Dept. of Neurobiology and BARINAGA, MARCIA, Science, Berkeley, California Anatomy, University of Texas Medical BAYLOR, DENIS, Dept. of Neurobiology, Stanford School, Houston University School of Medicine, California CADD, GARY, Dept. of Pharmacology, Howard BEGEMANN, MARTIN, Dept. of Molecular and De- Hughes Medical Institute, University of velopmental B~ology, Rockefeller Universi- Washington, Seattle ty, New York, New York CAPORALE, LYNN, Dept. of Industrial and Aca- BEKKERS, JOHN, Dept. of Molecular Neurobiol- demic Relations, Merck Sharp & Dohme Re- ogy, Sulk Institute, La Jolla, San Diego, search Laboratories, West Point, Pennsyl- California vania BENZER, SEYMOUR, Dept. of Biology, California CARDOZO, DAVID, Dept. of Neurobiology, Har- Institute of Technology, Pasadena vard Medical School, Boston, Massachusetts vi SYMPOSIUM PARTICIPANTS
CATE, JOHN, Depts. of Pathology and Laboratory National Institute of Mental Health, Bethes- Medicine, Medical University of South da, Maryland Carolina, Charleston DIAMOND, JEFF, Dept. of Ophthalmology, Uni- CEPKO, CONSTANCE, Dept. of Genetics, Harvard versity of California, San Francisco Medical School, Boston, Massachusetts DOWMAN, JOHN, Dept. of Neurosciences, Medical CHANDA, PRANAB, Depts. of Microbiology and Research Council, London, England Biotechnology, Wyeth-Ayerst Laboratories, DUFFY, CHARLES, Laboratory for Sensorimotor Philadelphia, Pennsylvania Research, National Eye Institute, National CHANGEUX, JEAN-PIERRE, Dept. of Molecular Institutes of Health, Bethesda, Maryland Neurobiology, Institut Pasteur, Paris, France DUHAMEL, JEAN-RENE, National Eye Institute, CHAVEZ-NORIEGA, LAURA, Salk Institute, La National Institutes of Health, Bethesda, JoUa, San Diego, California Maryland CHEN, JOSEPH, Depts. of Physiology and Bio- EDELMAN, GERALD, Neurosciences Research Pro- physics, New York University Medical Cen- gram, Rockefeller University Neurosciences ter, New York Institute, New York, New York CHU, HUNG-MING, Neuroscience Program, Har- ERKMAN, LINDA, Dept. of Biochemistry, Sciences vard University, Boston, Massachusetts II, The University, Geneva, Switzerland CHUN, JEROLD, Whitehead Institute, Cambridge, ESSEN, LARS-OLIVER, Institute of Neurobiology, Massachusetts University of Heidelberg, Federal Republic CLOTHIAUX, EUGENE, Center of Neuroscience and of Germany Physics, Brown University, Providence, FAGG, GRAHAM, Ciba-Geigy Ltd., Basel, Swit- Rhode Island zerland COHEN-CORY, SUSANA, Dept. of Neurobiology, FEKETE, DONNA, Dept. of Genetics, Harvard Rockefeller University, New York, New Medical School, Boston, Massachusetts York FINGER, WOLFGANG, Universitat Tubingen, Fed- COLBY, CAROL, Laboratory for Sensorimotor Re- eral Republic of Germany search, National Eye Institute, National In- FISCHBACH, GERALD, Depts. of Anatomy and stitutes of Health, Bethesda, Maryland Neurobiology, Washington University CONSTANTINE-PATON, MARTHA, Neuroscience School of Medicine, St. Louis, Missouri Program, Dept. of Biology, Yale University, FRIEDBERG, MARC, Dept. of Neurobiology, Brown New Haven, Connecticut University, Providence, Rhode Island COREY, DAVID, Dept. of Neurology, Massachu- FURTH, MARK, Dept. of Molecular and Cell Biolo- setts General Hospital, Boston gy, Regeneron Pharmaceuticals, Inc., Tar- COWAN, WILLIAM,Howard Hughes Medical Insti- rytown, New York tute, National Institutes of Health, Bethes- GARDNER, DANIEL, Dept. of Physiology, Cornell da, Maryland University Medical College, New York, New CRICK, FRANCIS, Salk Institute, La Jolla, San York Diego, California GASIC, GREGORY, Molecular Neurobiology Lab- CURRAN, THOMAS, Dept. of Molecular Oncology oratory, Salk Institute, La Jolla, San Diego, and Virology, Roche Institute of Molecular California Biology, Nutley, New Jersey GAUL, ULRIKE, Dept. of Cell and Molecular Biol- DAMASlO, ANTONIO, Dept. of Neurology, Uni- ogy, Howard Hughes Medical Institute, Uni- versity of Iowa Hospital and Clinics, Iowa versity of California, Berkeley City GEORGOPOULOS, APOSTOLOS, Dept. of Neuro- DAMASIO, HANNA, Dept. of Neurology, Universi- science, Johns Hopkins University School of ty of Iowa College of Medicine, Iowa City Medicine, Baltimore, Maryland DARNELL, ROBERT, Dept. of Neurology, Cornell GHEZ, CLAUDE, Dept. of Neurobiology and Be- University Medical College, New York, New havior, Research Foundation for Mental Hy- York giene, Inc., New York, New York DAXrA, MILTON, Dept. of Biochemistry and Bio- GILBERT,CHARLES, Dept. of Neurobiology, Rocke- physics, Columbia University, New York feller University, New York, New York DE CHARMS, CHRISTOPHER, Dept. of Physiology, GLASER, DONALD, Dept. of Physics and Neuro- University of California, San Francisco biology, University of California, Berkeley DESIMONE, ROBERT, Dept. of Neuropsychology, GOLDBERG, MICHAEL,National Eye Institute, Na- SYMPOSIUM PARTICIPANTS vii
tional Institutes of Health, Bethesda, Massachusetts Institute of Technology, Cam- Maryland bridge GOLDMAN, STEVEN, Dept. of Neurology, Cornell HORVITZ, H. ROBERT, Dept. of Biology, Howard University Medical College, New York, New Hughes Medical Institute, Massachusetts In- York stitute of Technology, Cambridge GOLDMAN-RAKIC, PATRICIA, Dept. of Neuro- HUBEL, DAVID, Dept. of Neurobiology, Harvard anatomy, Yale University School of Medi- Medical School, Boston, Massachusetts cine, New Haven, Connecticut HUDSPETH, JAMES, Dept. of Cell Biology and GOODMAN, COREr, Dept. of Molecular and Cell Neuroscience, University of Texas South- Biology, Howard Hughes Medical Institute, western Medical Center, Dallas, Texas University of California, Berkeley hyo, YUICHI, Center for Neurobiology and Be- GRANT, SETH, Center for Neurobiology and Be- havior, Columbia University, New York, havior, Howard Hughes Medical Institute, New York Columbia University, New York, New IzuMo, SEIGO, Dept. of Molecular Medicine, York Beth Israel Hospital, Boston, Massachusetts GREENGARD, PAUL, Dept. of Molecular and Cell- JACEWICZ, MICHAEL, Dept. of Neurology and ular Neuroscience, Rockefeller University, Neuroscience, Cornell University Medical New York, New York Center, New York, New York GREGA, DEBRA, Dept. of Research and Develop- JACK, JULIAN, University Laboratory of Physiolo- ment, Boehringer Mannheim Corporation, gy, Physiological Society, Oxford, England Indianapolis, Indiana JALONEN, TUULA, Dept. of Biomedical Sciences, GRILLNER, STEN, Nobel Institute for Neuro- University of Tampere, Finland physiology, Karolinska Institutet, Stock- JAN, LILY, Howard Hughes Medical Institute, holm, Sweden University of California, San Francisco GRUMET, MARTIN, Dept. of Developmental and JAN, YUH NUNG, Dept. of Physiology, University Molecular Biology, Rockefeller University, of California, San Francisco New York, New York JEN, JOANNA, Dept. of Molecular Neurobiology, HATrA, KOHEI, Institute of Neuroscience, Uni- Salk Institute, La Jolla, San Diego, Cali- versity of Oregon, Eugene fornia HEGDE, ASHOK, Centre for Cellular and Molecu- JESSELL, THOMAS, Depts. of Biochemistry and lar Biology, Hyderabad, India Molecular Biophysics, Columbia University HEINEMANN, STEPHEN, Dept. of Molecular College of Physicians & Surgeons, New Neurobiology, Salk Institute, La Jolla, San York, New York Diego, California JOHNSON, KENNETH, Dept. of Neuroscience, HEN, RENE, LGME de Centre National de Johns Hopkins University School of Medi- la Recherche Scientifique, Strasbourg, cine, Baltimore, Maryland France JONES, EDWARD, Depts. of Anatomy and Neuro- HILDAGO, ANDREA, Dept. of Neurology, Cornell biology, University of California College of University Medical College, New York, New Medicine, Irvine York JONES, KEVIN, Dept. of Physiology, Howard HIRANO, ARLENE, Dept. of Neurobiology, Rocke- Hughes Medical Institute, University of Cali- feller University, New York, New York fornia, San Francisco HIRSCH, JUDITH, Dept. of Neurobiology, Rocke- JORGENSEN, ERIK, Dept. of Biology, Massachu- feller, University, New York, New York setts Institute of Technology, Cambridge HOCKFIELD, SUSAN, Dept. of Neuroanatomy, JULESZ, BELA, Laboratory of Vision Research, Yale University School of Medicine, New California Institute of Technology and Rut- Haven, Connecticut gers University, New Brunswick, New Jersey HOGAN, NEVILLE,Dept. of Mechanical Engineer- KANDEL, ERIC, Center for Neurobiology and Be- ing, Massachusetts Institute of Technology, havior, Columbia University College of Phy- Cambridge, Massachusetts sicians & Surgeons, New York, New York HOMONOFF, MARC, New York, New York KAPLAN, JOSHUA, Dept. of Biology, Massachu- HOOK, VIVIAN, Uniformed Services University setts Institute of Technology, Cambridge Health Sciences, Bethesda, Maryland KATER, STANLEY,Depts. of Neuronal Growth and HOPKINS, NANCY, Center for Cancer Research, Development, Anatomy and Neurobiology, viii SYMPOSIUM PARTICIPANTS
Colorado State University, Fort Collins, Col- LOEB, GERALD, Dept. of Physiology, Queen's orado University, Kingston, Canada KAY, ALAN, Dept. of Biophysics, AT&T Bell Lu, BAI, Dept. of Molecular Neuroscience, Rocke- Laboratories, Murray Hill, New Jersey feller University, New York, New York KELNER, KATRINA, Science Magazine, Washing- MAC LEISH, PETER, Dept. of Neurobiology, ton, D.C. Rockefeller University, New York, New KENNEDY, MARY, Dept. of Biology, California York Institute of Technology, Pasadena, Cali- MAHAN, LAWRENCE, Dept. of Cell Biology, Na- fornia tional Institute of Mental Health, National KIMMEL, BRUCE, Dept. of Molecular and Cell Institutes of Health, Bethesda, Maryland Biology, University of California, Berkeley MARGOLSKEE, ROBERT, Dept. of Neurosciences, KIMURA, FUMITAKA, Dept. of Neurophysiology, Roche Institute of Molecular Biology, Nut- Biomedical Research Center, Osaka Uni- ley, New Jersey versity Medical School, Japan MARICQ, ANDREA, Dept. of Pharmacology, Uni- KLINZ, STEPHAN, ETH Institute of Neurobiology, versity of California, San Francisco Zurich, Switzerland MARONEY, ANNA, Dept. of Microbiology, How- KOCH, CHRISTOF, Dept. of Computational and ard Hughes Medical Institute, University of Neural Systems, California Institute of Tech- Pennsylvania, Philadelphia nology, Pasadena MAROTEAUX, Lvc, Institut de Chimie Biologique, KocH, MICHEL, European Molecular Biology Centre National Recherche Scientifique, Laboratory, Outstation Hamburg, Federal LGME, Strasbourg, France Republic of Germany MARRION, NEIL, Depts. of Neurobiology and Be- KONISHI, MARK, Dept. of Biology, California In- havior, Howard Hughes Medical Research stitute of Technology, Pasadena Laboratory, State University of New York, KOTRLA, KATHRYN, Dept. of Psychiatry, Baylor Stony Brook College of Medicine, Houston, Texas MARTIN, KEVAN, Dept. of Pharmacology, Medical KUBO, TAI, Dept. of Neurobiology and Behavior, Research Council, Oxford, England Columbia University College of Physicians & MCALLISTER, GEORGE, Neuroscience Research Surgeons, New York, New York Centre, Merck Sharp & Dohme Research KURODA, YOICHIRO, Dept. of Neurochemistry, Laboratories, Essex, England Tokyo Metropolitan Institute for Neuro- MCCARTHY, BRIAN, Depts. of Neurobiology and science, Japan Behavior, State University of New York, KUROKAWA, TAISUKE, Dept. of Physiology, Fukui Stony Brook Medical School, Japan McCLENDON, EVELYN, Depts. of Neurohiology LA MANTIA, ANTHONY, Depts. of Anatomy and and Anatomy, University of Texas Health Neurobiology, Washington University Science Center, Houston School of Medicine, St. Louis, Missouri McKAY, RONALD, Depts. of Brain and Cognitive LEHR, ANNE, Dept. of Cell Biology, National Sciences, and Biology, Massachusetts Insti- Institute of Mental Health, National Insti- tute of Technology, Cambridge tutes of Health, Bethesda, Maryland MCMAHAN, UEL JACK, Dept. of Neurobiology, LI, CONGYI, Cell and Molecular Biology Program, Stanford University School of Medicine, University of Wisconsin, Madison California LILLIEN, LAURA, Dept. of Genetics, Harvard MERZENICH, MICHAEL, Coleman Memorial Lab- Medical School, Boston, Massachusetts oratory, University of California, San Fran- LISBERGER, STEPHEN, Dept. of Physiology, Uni- cisco versity of California, San Francisco MIAKE-LYE, RYN, Cell Magazine, Cambridge, LIVINGSTONE, MARGARET, Dept. of Neurobiology, Massachusetts Harvard Medical School, Boston, Massachu- M1KLOS, GEORGE, Molecular Neurobiology setts Group, Australian National University, Can- LLINAS, RONDOLFO, Depts. of Physiology and berra Biophysics, New York University School of MILNER, BRENDA, Montreal Neurological Insti- Medicine, New York tute, McGill University, Canada Lo, MATTHEW, ICI Americas, Wilmington, De- MOLNAR, ZOLTAN, Physiology Laboratory, Uni- laware versity of Oxford, England SYMPOSIUM PARTICIPANTS ix
MONTAGUE, P. READ, Neurosciences Institute, Neurobiology, Washington University New York, New York School of Medicine, St. Louis, Missouri MORIGIWA, KATSUKO,Dept. of Physiology, Osaka OBERDOREER, MICHAEL, National Eye Institute, University Medical School, Japan National Institutes of Health, Bethesda, MORRIS, RICHARD, Dept. of Pharmacology, Uni- Maryland versity of Edinburgh Medical School, OVERBEEK, PAUL, Dept. of Cell Biology, Howard Scotland Hughes Medical Institute, Baylor College of MOUNTCASTLE, VERNON, Bard Laboratories, De- Medicine, Houston, Texas partment of Neuroscience, Johns Hopkins PATrERSON, PAUL, Dept. of Biology, California University School of Medicine, Baltimore, Institute of Technology, Pasadena Maryland PEINADO, ALEX, Dept. of Neurobiology, Rocke- MOVSHON, J. ANTHONY, Center for Neural Sci- feller University, New York, New York ence, New York University, New York POGGIO, GIAN, Dept. of Neuroscience, Bard MURAKOSHI, TAKAYUKI, Neurobiology Labora- Laboratories, Johns Hopkins University tory, Rockefeller University, New York, School of Medicine, Baltimore, Maryland New York POGGIO, TOMASCO, Artificial Intelligence Labora- MURASE, KAZUYUKI, Dept. of Information Sci- tory, Massachusetts Institute of Technology, ence, Fukui University, Japan Cambridge and IRST, Trento, Italy NAIRN, ANCUS, Dept. of Molecular and Cellular PRIETO, ANNE, Dept. of Molecular and Develop- Neuroscience, Rockefeller University, New mental Biology, Rockefeller University, York, New York New York, New York NAKANISHI, NOBUKI, Howard Hughes Medical PULSINELLI, WILLIAM, Dept. of Neurology, Cot- Institute, Columbia University College of nell University Medical College, New York, Physicians & Surgeons, New York, New New York York PVRVES, DALE, Depts of Anatomy and Neuro- NAKAYAMA, KEN, Smith-Kettlewell Eye Research biology, Washington University School of Institute, San Francisco, California Medicine, St. Louis, Missouri NATHANS, JEREMY, Dept. of Molecular Biology QUINN, WILLIAM, Depts. of Brain and Cognitive and Genetics, Howard Hughes Medical Insti- Sciences, and Biology, Massachusetts Insti- tute, Johns Hopkins School of Medicine, tute of Technology, Cambridge Baltimore, Maryland RAFE, MARTIN, Dept. of Biology, University Col- NAVE, KLAUS-ARMIN,Dept. of Molecular Neuro- lege, London, England biology, Salk Institute, La Jolla, San Diego, RAICHLE, MARCUS, Dept. of Radiation Sciences, California Washington University Medical Center, St. NEWSOME, WILLIAM, Dept. of Neurobiology, Louis, Missouri Stanford University School of Medicine, RAKIC, PASKO, Section of Neuroanatomy, Yale California University School of Medicine, New Haven, NICOLL, ROGER, Dept. of Pharmacology, Uni- Connecticut versity of California, San Francisco RAMIREZ, ROSAURA,Dept. of Biology, University NIKOLICS, KAROLY,Dept. of Developmental Biol- of Puerto Rico, Rio Piedras ogy, Genentech, Inc., South San Francisco, RAO, YI, Dept. of Physiology, University of Cali- California fornia, San Francisco NINIO, JACQUES, Institut Jacques Monod, Paris, REICHARDT, LOUIS, Dept. of Physiology, Howard France Hughes Medical Institute, University of Cali- NIRENBERG, SHEILA, Dept. of Genetics, Harvard fornia, San Francisco Medical School, Boston, New York REINAGEL, PAMELA, Harvard University, Boston, NODA, TERUMI, Dept. of Physiology, Fukui Medi- Massachusetts cal School, Japan ROBINSON, DAVID, Dept. of Opthamology, Johns NUMA, SHOSAKU, Depts. of Medical Chemistry Hopkins University, Baltimore, Maryland and Molecular Genetics, Kyoto University ROLLS, EDMUND, Dept. of Experimental Psy- Faculty of Medicine, Japan chology, University of Oxford, England O'CONNOR, WILLIAM, Dept. of Pharmacology, RONNETT, GABRIELE, Dept. of Neurology and Karolinska Institute, Stockholm, Sweden Neuroscience, Johns Hopkins University, O'LEARY, DENNIS, Depts. of Anatomy and Baltimore, Maryland x SYMPOSIUM PARTICIPANTS
ROUTTENBERG, ARYEH, Cresap Neuroscience Lab- SPARKS, DAVID, Dept. of Psychology, University oratory, Northwestern University, Evanston, of Pennsylvania, Philadelphia Illinois SQUIRE, LARRY,University of California, and Vet- RUBIN, MICHAEL, Dept. of Molecular and Cell- erans' Administration Medical Center, San ular Neuroscience, Rockefeller University, Diego New York, New York STARK, RACHEL, Dept. of Audiology and Speech RUVKUN, GARY, Dept. of Molecular Biology, Sciences, Purdue University, West Lafay- Massachusetts General Hospital, Boston ette, Indiana SAKMANN, BERT, Abteilung Zellphysiologie, Max- STEINMETZ, MICHAEL, Dept. of Neuroscience, Planck Institut, Heidelberg, Federal Repub- Johns Hopkins University School of Medi- lic of Germany cine, Baltimore, Maryland SANES, JOSHUA, Dept. of Anatomy and Neuro- STEVENS, CHARLES, Dept. of Molecular Neuro- biology, Washington University School of biology, Salk Institute, La Jolla, San Diego, Medicine, St. Louis, Missouri California SARON, CLIFFORD, Dept. of Neuroscience, Albert STRYKER, MICHAEL, Dept. of Physiology and Einstein College of Medicine, Bronx, New Neuroscience, University of California, San York Francisco SAWIN, ELIZABETH, Dept. of Biology, Massachu- SUBRAMANIAN, ALAP, Max-Planck Institut for setts Institute of Technology, Cambridge Molekulare Genetik, Berlin, Federal Re- SCHAEFFER, ERIC, Dept. of Molecular and Cell- public of Germany ular Neuroscience, Rockefeller University, SUGA, NUBUO, Dept. of Biology, Washington New York, New York University, St. Louis, Missouri SCHELLER, RICHARD, Herrin Laboratory, Dept. of SZAPIEL, SUSAN, Dept. of Neurobiology, Rocke- Biological Sciences, Stanford University, feller University, New York, New York California TAKEICHI, MASATOSHI, Dept. of Biophysics, Fa- SCHWARTZ,JAMES, Howard Hughes Medical Insti- culty of Science, Kyoto University, Japan tute, Columbia College of Physicians & TANK, DAVID, Computational Neuroscience Surgeons, New York, New York Group, Bell Laboratories, Murray Hill, New SCHWARZ, ULI, Dept. of Biochemistry, Max- Jersey Planck Institut, Tubingen, Federal Republic TOMICH, PAUL, Dept. of Chemical and Biological of Germany Screening, Upjohn Company, Kalamazoo, SEEBURG, PETER, Zentrum fur Molekulare Michigan Biologie, University of Heidelberg, ZMBH, TORRE, VINCENT, Dept. of Physics, Universita di Federal Republic of Germany Genova, Italy SEJNOWSKI, TERRENCE, Salk Institute and Uni- TSAO, FRITZ, Dept. of Psychology, Hillsdale Col- versity of California, San Deigo lege, Michigan SHATZ, CARLA, Dept. of Neurobiology, Stanford TSIEN, RICHARD,Dept. of Molecular and Cellular University School of Medicine, California Physiology, Stanford University Medical SHNEIDER, NEIL, Howard Hughes Medical Insti- Center, California tute, Columbia University, New York, New TSIEN, ROGER, Howard Hughes Medical Institute, York University of California, San Diego SHOOLMAN, HARVEY,Blackwell Scientific Publica- TULLY, TIM, Dept. of Biology, Brandeis Universi- tions Ltd., Oxford, England ty, Waltham, Massachusetts SIGUENZA, JUAN ALBERTO, Departamento de ULLMAN, SHIMON, Artificial Intelligence Labora- Morfologia/Medicina, Universidad Au- tory, Massachusetts Institute of Technology, tonoma de Madrid, Spain Cambridge SILVA, ALClNO, Center for Cancer Research, UNNIKRISHNAN, K.P., Dept. of Computer Sci- Massachusetts Institute of Technology, Cam- ence, General Motors Research Labora- bridge tories, Warren, Michigan SINGER, WOLF, Dept. of Neurophysiology, Brain VALENZUELA, DARIO, Dept. of Developmental Research, Max-Planck Institut, Frankfurt, Biology, Howard Hughes Medical Institute, Federal Republic of Germany Massachusetts General Hospital, Boston SMITH, MARTIN, Dept. of Chemical and Biological VAN ESSEN, DAVID, Dept. of Biology, California Screening, Upjohn Company, Kalamazoo, Institute of Technology, Pasadena Michigan VAN VACTOR,DAVID, Dept. of Biological Chemis- SYMPOSIUM PARTICIPANTS xi
try, University of California, Los Angeles Research Laboratories, Indianapolis, In- VANDENBERG, ROBERT, Garvan Institute of Medi- diana cal Research, St. Vincent's Hospital, Syd- WORLEY, PAUL, Dept. of Neuroscience, Johns ney, Australia Hopkins University School of Medicine, Bal- VETTER, MONICA, Dept. of Physiology, University timore, Maryland of California, San Francisco WURTZ, ROBERT, Laboratory for Sensorimotor VIVEROS, HUMBERTO, Division of Medicinal Bio- Research, National Eye Institute, National chemistry, Burroughs Wellcome Company, Institutes of Health, Bethesda, Maryland Research Triangle Park, North Carolina YAMAMORI, TETSUO, Dept. of Biology, California VOYVODIC, JAMES, Dept. of Biology, University Institute of Technology, Pasadena College, London, England YAMANE, T., Dept. of Biophysics, AT&T Bell WAGNER, JOHN, Dana-Farber Cancer Institute, Laboratories, Murray Hill, New Jersey Boston, Massachusetts YAMASAKI, SONNY, Laboratory for Sensorimotor WALTER, GERNOT, Dept. of Pathology, University Research, National Eye Institute, National of California, San Diego Institutes of Health, Bethesda, Maryland WATSON, JAMES, Cold Spring Harbor Laboratory, YANCOPOULOS, GEORGE, Regeneron Pharmaceuti- Cold Spring Harbor, New York cals, Inc., Tarrytown, New York WESTHEIMER, GERALD, Dept. of Molecular and YANG, XIAmIE, Dept. of Genetics, Harvard Cell Biology, University of California, Ber- Medical School, Boston, Massachusetts keley YIN, JERRY, Dept. of Brain and Cognitive Sci- WHITE, W. FROST, Dept. of Neuroscience, Pfizer ences, Massachusetts Institute of Technolo- Central Research, Groton, Connecticut gy, Cambridge WIESEL, TORSTEN, Dept. of Neurobiology, Rocke- Yu, VICTOR, Eukaryotic Regulatory Biology Pro- feller University, New York, New York gram, University of California, San Diego WILLIAMS, JOHN, Dept. of Neurophysiology and YUSTE, RAFAEL, Dept. of Neurobiology, Rocke- Neuropharmacy, National Institute for feller University, New York, New York Medical Research, London, England ZEKI, SEMIR, Dept. of Anatomy and Develop- WILLIAMSON, DAVID, Dept. of Developmental mental Biology, University College, Lon- and Molecular Biology, Rockefeller Uni- don, England versity, New York, New York ZHAO, BIAO, Dept. of Neurobiology and Be- WITUNSKI, MICHAEL, Kiawah Island, South Cara- havior, Columbia University, New York, olina New York WOOD, JOHN, Dept. of Molecular Genetics, Lilly First row: J.J.B. Jack; Wine and Cheese Party; D. Baylor Second row: H. Damasio, T. Sejnowski, C. Gilbert; S. Hockfield, L. Jan Third row: P. Andersen; H. Horvitz, B. Sawin, A. Abeliovich First row: S. Zeki, M. Raichle; R. Tsien, R.Tsien, T. Bonhoeffer, F. Bonhoeffer Second row: J. Witkowski, F. Crick; J. Byrne, C.F. Stevens First row: J.D. Watson, E. Watson, L.A. Hazen, F. Crick; T. Poggio, G.F. Poggio Second row: V.B. Mountcastle; T. Sejnowski; J.-P. Changeux Third row: C. Shatz, F. Bonhoeffer, C. Blakemore, M.C. Raft, P.H. Patterson Foreword
The brain will be to the next century what the gene has been to the 20th century. At the start of this century, we knew that genes were on chromosomes, but what they were chemically or how they functioned was a total mystery. Now, of course, much, much more is known about the brain. This has been far from a sleepy century for brain research, and an extraordinary accumulation of anatomical data is now being complemented by experiments localizing definite tasks to specific collections of nerve cells. But compared to the gene, the brain, at least in today's ignorance, seems an infinitely more daunting objective. No one has any precise ideas about how complex perceptions are stored in our brains, much less retrieved when our memories work as we wish. How we will reach these objectives is far from clear, except for the virtual truism that we should diversify our approaches and at least for the present not divert too many of our resources toward any one approach. We must also see to it that the theorists learn the facts of the experimentalists and that the experimentalists also begin seriously to learn what the neural modelers are up to. It was with this objective that we decided to hold the 1990 Symposium (our 55th) on The Brain. This was to be our sixth symposium that focused on nerve cells. In 1936, we focused on Excitation Phenomena; in 1952, on The Neuron; in 1966, on Sensory Perception; in 1975, on The Synapse; and in 1983, on Molecular Neurobiology. The intervals between neurobiology-oriented meetings have steadily shortened and will likely continue to do so given the increasing number of talented young scientists who now see the brain as the ultimate challenge for biology. In choosing the speakers, I needed much advice, and in particular, I thank Max Cowan, Francis Crick, Tom Jessell, Eric Kandel, Charles Stevens, and Terry Sejnowski. Later in organizing the final program and in selecting the order in which the symposium papers appear in these volumes, I particularly thank Eric Kandel, whose advice has been invaluable to me since the start of our neurobiology summer teaching program in 1971. The final program contained 105 presentations given over a one-week-long period before an audience that totaled 320. On opening night, there were splendid introductory talks by Shosaku Numa, Martin Raft, Sten Grillner, William Newsome, and Marcus Raichle. The summary, artfully given, was by Michael Stryker. The final result was a wonderful, although intellectu- ally exhausting, experience that more than justified the money and time needed for its organization and execution. Financial support for such a large meeting as the Symposium comes from many sources. We gratefully acknowledge the National Institute of Mental Health (an Institute of the Alcohol, Drug Abuse, and Mental Health Administration); the National Cancer Institute, the National Institute of Child Health and Human Development, the National Institute of Neurological Disorders and Stroke (divisions of the National Institutes of Health); the U.S. Department of Energy; and the National Science Foundation. Essential funds also came from our Corporate Sponsors: Alafi Capital Company; American Cyanamid Company; AMGen Inc.; Applied Biosystems, Inc.; Becton Dickinson and Company; Boehringer Mannheim Corporation; Bristol-Meyers Squibb Company; Ciba-Geigy Corporation/Ciba- Geigy Limited; Diagnostic Products Corporation; E.I. du Pont de Nemours & Company; Eastman Kodak Company; Genentech, Inc.; Genetics Institute; Hoffmann-La Roche Inc.; Johnson & Johnson; Life Technologies, Inc. ; Eli Lilly and Company; Millipore Corporation; Monsanto Company; Pall Corporation; Perkin-Elmer Cetus Instruments; Pfizer Inc.; Phar- macia Inc.; Schering-Plough Corporation; The Upjohn Company; The Wellcome Research Laboratories, Burroughs Wellcome Co.; and Wyeth-Ayerst Research. Registration and housing for the participants were organized with care and courtesy by the staff of the Meetings Office: Maureen Berejka, Barbara Ward, Karen Otto, Diane Tighe, Michela McBride, and Marge Stellabotte. Jim Hope and his staff provided admirable catering, and once again Herb Parsons and his assistants delivered a flawless audiovisual service. These books were edited by Dorothy Brown, Patricia Barker, and Ralph Battey, assisted by Joan Ebert, Mary Cozza, and Inez Sialiano, and their production was overseen by Nancy Ford.
James D. Watson January 31, 1990
XV Contents
Symposium Participants V Foreword XV
Molecular Mechanisms for Signaling Molecular Insights into Excitation-Contraction Coupling S. Numa, T. Tanabe, H. Takeshima, A. Mikami, T. Niidome, S. Nishimura, B.A. Adams, and K. G. Beam
Molecular Studies of Voltage-gated Potassium Channels E. Isacoff, D. Papazian, L. Timpe, Y.-N. Jan, and L.-Y. Jan
Differences in Gating among Amino-terminal Variants of Shaker Potassium Channels R. W. Aldrich, T. Hoshi, and W.N. Zagotta 19
The GABA A Receptor Family: Molecular and Functional Diversity P.H. Seeburg, W. Wisden, T.A. Verdoorn, D.B. Pritchett, P. Werner, A. Herb, H. Liiddens, R. Sprengel, and B. Sakmann 29
Glutamate Receptor GluR-KI: Structure, Function, and Expression in the Brain M. Hollmann, S. W. Rogers, A. 0 'Shea-Greenfield, E.S. Deneris, T.E. Hughes, G.P. Gasic, and S. Heinemann 41
Quantal Analysis of Excitatory Synaptic Mechanisms in the Mammalian Central Ner- vous System J.J.B. Jack, D.M. Kullmann, A. U. Larkman, G. Major, and K.J. Stratford 57
Synaptic Transmission in Hippocampal Neurons: Numerical Reconstruction of Quantal IPSCs C. Busch and B. Sakmann 69
Excitatory Synaptic Integration in Hippocampal Pyramids and Dentate Granule Cells P. Andersen, M. Raastad, and J.F. Storm 81
Physiological Properties of Excitatory Synaptic Transmission in the Central Nervous System S. Hestrin, D.J. Perkel, P. Sah, T. Manabe, P. Renner, and R.A. Nicoll 87
Short-term Electrophysiological Actions of Insulin on Aplysia Neurons: Identification of a Possible Novel Modulatory Second-messenger Mechanism J.H. Schwartz, E. Shapiro, S.D. Brown, and A.R. Saltiel 95
Structure and Regulation of Type II Calcium/Calmodulin-dependent Protein Kinase in Central Nervous System Neurons M.B. Kennedy, M.K. Bennett, R.F. Bulleit, N.E. Erondu, V.R. Jennings, S.G. Miller, S.S. Molloy, B.L. Patton, and L.J. Schenker 101
Molecular Analysis of Proteins Associated with the Synaptic Vesicle Membrane J.K. Ngsee, W.S. Trimble, L.A. Elferink, B. Wendland, K. Miller, N. Calakos, and R. H. Scheller 111
Presynaptic Mechanisms in Hippocampal Long-term Potentiation T.V.P. Bliss, M.L. Errington, M.A. Lynch. and J.H. Williams 119
Computational Implications of NMDA Receptor Channels J.M. Bekkers and C.F. Stevens 131 xvii xviii CONTENTS
Modified Hebbian Rule for Synaptic Enhancement in the Hippocampus and the Visual Cortex T. Bonhoeffer, A. Kossel, J. Bolz, and A. Aertsen 137
Long-term Potentiation: Presynaptic Enhancement following Postsynaptic Activation of Ca++-dependent Protein Kinases R. W. Tsien and R. Malinow 147
Toward a Representational Hypothesis of the Role of Hippocampal Synaptic Plasticity in Spatial and Other Forms of Learning R.G.M. Morris 161
Neuronal and Network Determinants of Simple and Higher-order Features of Associa- tive Learning: Experimental and Modeling Approaches J.H. Byrne, D.A. Bax- ter, D.V. Buonomano, and J.L. Raymond 175
Long-term Facilitation in Aplysia." Persistent Phosphorylation and Structural Changes S. Schacher, D. Glanzman, A. Barzilai, P. Dash, S.G.N. Grant, F. Keller, M. Mayford, and E.R. Kandel 187
Genetic Dissection of Memory Formation in Drosophila melanogaster T. Tully, S. Boynton, C. Brandes, J.M. Dura, R. Mihalek, T. Preat, and A. Villella 203
Synaptic Regulation of Immediate-Early Genes in Brain P.F. Worley, A.J. Cole, T.H. Murphy, B.A. Christy, Y. Nakabeppu, and J.M. Baraban 213
Inducible Proto-oncogene Transcription Factors: Third Messengers in the Brain? T. Curran, C. Abate, D.R. Cohen, P.F. Macgregor, F.J. Rauscher III, J.L. Sonnen- berg, J.A. Connor, and J.I. Morgan 225
Neural Development An Analysis of the Cell-Cell Interactions That Control the Proliferation and Differen- tiation of a Bipotential Glial Progenitor Cell in Culture M.C. Raft, I.K. Hart, W.D. Richardson, and L.E. Lillien 235
Role of Helix-Loop-Helix Proteins in Drosophila Neurogenesis H. Vaessin, M. Caudy, E. Bier, L.-Y. Jan, and Y.-N. Jan 239
Generation of Neuronal Diversity: Analogies and Homologies with Hematopoiesis H. Nawa, T. Yamamori, T. Le, and P.H. Patterson 247
Contributions of Cell-extrinsic and Cell-intrinsic Factors to the Differentiation of a Neural-crest-derived Neuroendocrine Progenitor Cell N. Mori, S.J. Birren, R. Stein, D. Stemple, D.J. Vandenbergh, C. W. Wuenschell, and D.J. Anderson 255
Studies of Cortical Development Using Retrovirus Vectors C.L. Cepko, C.P. Austin, C. Walsh, E.F. Ryder, A. Halliday, and S. Fields-Berry 265
Guidance of Developing Axons by Diffusible Chemoattractants M. Placzek, M. Tessier-Lavigne, T. Yamada, J. Dodd, and T.M. Jessell 279
Mechanisms Regulating Cell Number and Type in the Mammalian Central Nervous System R. McKay, N. Valtz, M. Cunningham, and T. Hayes 291
Place-dependent Cell Adhesion, Process Retraction, and Spatial Signaling in Neural Morphogenesis G.M. Edelman and B.A. Cunningham 303 CONTENTS xix
Cadherin Subclasses: Differential Expression and Their Roles in Neural Morphogenesis M. Takeichi, H. lnuzuka, K. Shimamura, T. Fujimori, and A. Nagafuchi 319
Molecular Genetics of Neuronal Recognition in Drosophila." Evolution and Function of Immunoglobulin Superfamily Cell Adhesion Molecules G. Grenningloh, A.J. Bieber, E. J. Rehm, P. M. Snow, Z. R. Traquina, M. Hortsch, N. H. Patel, and C. S. Goodman 327
Neuronal Receptors That Regulate Axon Growth L.F. Reichardt, B. Bossy, S. Carbonetto. I. de Curtis, C. Emmett, D.E. Hall, M.J. Ignatius, F. Lefcort, E. Napolitano, T. Large, K.M. Neugebauer, and K.J. Tomaselli 341
Directional Cues for Retinal Axons B. Stahl, Y. von Boxberg, B. Miiller, J. Walter, U. Schwarz, and F. Bonhoeffer 351
Neuronal Growth Cone as an Integrator of Complex Environmental Information S.B. Kater and P.B. Guthrie 359
Neurotrophic Factors, Their Receptors, and the Signal Transduction Pathways They Activate G.D. Yancopoulos, P.C. Maisonpierre, N.Y. Ip, T.H. Aldrich, L. Belluscio, T.G. Boulton, M.H. Cobb. S.P. Squinto, and M.E. Furth 371
Compartmentalization of Acetylcholine Receptor Gene Expression during Develop- ment of the Neuromuscular Junction J. P. Changeux, C. Babinet, J. L. Bessereau, A. Bessis, A. Cartaud, J. Cartaud, P. Daubas, A. Devillers- Thi~ry, A. Duclert, J. A. Hill, B. Jasmin, A. Klarsfeld, R. Laufer, H.O. NghiOm, J. Piette, M. Roa, and A. M. Salmon 381
M r 42,000 ARIA: A Protein That May Regulate the Accumulation of Acetylcholine Receptors at Developing Chick Neuromuscular Junctions D.L. Falls, D.A. Har- ris, F.A. Johnson, M.M. Morgan, G. Corfas, and G.D. Fischbach 397
The Agrin Hypothesis U.J. McMahan 407
S-Laminin J.R. Sanes, D.D. Hunter, 7". L. Green, and J.P. Merlie 419
NMDA Receptor as a Mediator of Activity-dependent Synaptogenesis in the Develop- ing Brain M. Constantine-Paton 431
Construction of Modular Circuits in the Mammalian Brain D. Purves and A.-S. LaMantia 445
Target Selection by Cortical Axons: Alternative Mechanisms to Establish Axonal Connections in the Developing Brain D. D. M. O'Leary, A. R. Bicknese, J. A. De Carlos, C.D. Heffner, S.E. Koester, L.J. Kutka, and T. Terashima 453
Pioneer Neurons and Target Selection in Cerebral Cortical Development C.J. Shatz, A. Ghosh, S.K. McConnell, K.L. Allendoerfer, E. Friauf, and A. Antonini 469
Activity-dependent Regulation of Gene Expression in Adult Monkey Visual Cortex E.J. Jones, D.L. Benson, S.H.C. Hendry, and P.J. Isackson 481
Factors Involved in the Establishment of Specific Interconnections between Thalamus and Cerebral Cortex C. Blakemore and Z. Molndr 491
Expression of Neural Proteoglycans Correlates with the Acquisition of Mature Neuro- nal Properties in the Mammalian Brain S. Hockfield, R.G. Kalb, S. Zaremba, and H. Fryer 505 xx CONTENTS
Experimental and Theoretical Studies of the Organization of Afferents to Single Orientation Columns in Visual Cortex M.P. Stryker, B. Chapman, K.D. Miller, and K.R. Zahs 515
Sensory and Motor Systems Chemosensory Cell Function in the Behavior and Development of Caenorhabditi, elegans C. L Bargmann, J.H. Thomas, and H.R. Horvitz 529
Bacterial Microprocessing H. C. Berg 539
Ultrastructural Correlates of Mechanoelectrical Transduction in Hair Cells of the Bullfrog's Internal Ear R.A. Jacobs and A.J. Hudspeth 547
Model of Phototransduction in Retinal Rods V. Torre, S. Forti, A. Menini, and M. Campani 563
Similar Algorithms in Different Sensory Systems and Animals M. Konishi 575
Specialized Subsystems for Processing Biologically Important Complex Sounds: Cross- correlation Analysis for Ranging in the Bat's Brain N. Suga, J.F. Olsen, and J. A. Butman 585
Associative Memory Function in Piriform (Olfactory) Cortex: Computational Modeling and Neuropharmacology M.E. Hasselmo, M.A. Wilson, B.P. Anderson, and J.M. Bower 599
Neural Image Transformation in the Somatosensory System of the Monkey: Com- parison of Neurophysiological Observations with Responses in a Neural Network Model I.N. Bankman, S.S. Hsiao, and K. O. Johnson 611
Protein-Chromophore Interactions in Rhodopsin Studied by Site-directed Mutagenesis J. Nathans 621
Cone Excitations and Color Vision 7". W. Kraft, C.L. Makino, R.A. Mathies, J. Lugtenburg, J.L. Schnapf, and D.A. Baylor 635
Color Puzzles D, Hubel and M. Livingstone 643
Parallelism and Functional Specialization in Human Visual Cortex S. Zeki 651
Lateral Interactions in Visual Cortex C.D. Gilbert, J.A. Hirsch, and T.N. Wiesel 663
Modular and Hierarchical Organization of Extrastriate Visual Cortex in the Macaque Monkey D.C. Van Essen, D.J. Felleman, E.A. DeYoe, J. Olavarria, and J. Knierim 679
Neuronal Mechanisms of Motion Perception W.T. Newsome, K.H. Britten, C.D. Satzman, and J.A. Movshon 697
Visual Cortical Signals Supporting Smooth Pursuit Eye Movements J.A. Movshon, S. G. Lisberger, and R.J. Krauzlis 707
Functional Specialization for Visual Motion Processing in Primate Cerebral Cortex R.H. Wurtz, D.S. Yamasaki, C.J. Duffy, and J.-P. Roy 717 CONTENTS xxi
Representation of Visuomotor Space in the Parietal Lobe of the Monkey M.E. Goldberg, C.L. Colby, and J.-R. Duhamel 729
Hierarchical Processing of Motion in the Visual Cortex of Monkey R.A. Andersen, R.J. Snowden, S. Treue, and M. Graziano 741
Cortical Neural Mechanisms of Stereopsis Studied with Dynamic Random-dot Stereo- grams G. F. Poggio 749
The Grain of Visual Space G. Westheimer 759
Neural Models of Binocular Depth Perception S.R. Lehky, A. Pouget, and T.J. Sejnowski 765
Cellular Network Underlying Locomotion as Revealed in a Lower Vertebrate Model: Transmitters, Membrane Properties, Circuitry, and Simulation S. Grillner, P. Wall~n, and G. Viana di Prisco 779
Understanding Sensorimotor Feedback through Optimal Control G.E. Loeb, W.S. Levine, and J. He 791
Population Coding of the Direction, Amplitude, and Velocity of Saccadic Eye Move- ments by Neurons in the Superior Colliculus D.L. Sparks, C. Lee, and W.H. Rohrer 805
Properties of Pathways That Mediate Motor Learning in the Vestibulo-ocular Reflex of Monkeys S.G. Lisberger, D.M. Broussard, and H.M. Bront~-Stewart 813
Teaching Neural Networks to Process Temporal Signals for Oculomotor Con- trol D.B. Arnold and D.A. Robinson 823
Motor-Space' Coding in the Central Nervous System F.A. Mussa-Ivaldi, S.F. Giszter, and E. Bizzi 827
Roles of Proprioceptive Input in the Programming of Arm Trajectories C. Ghez, J. Gordon, M.F. Ghilardi, C.N. Christakos, and S.E. Cooper 837
Neural Coding of the Direction of Reaching and a Comparison with Saccadic Eye Movements A. P. Georgopoulos 849
Cognitive Neuroscience Cortical Neuronal Periodicities and Frequency Discrimination in the Sense of Flut- ter V.B. Mountcastle, M.A. Steinmetz, and R. Romo 861
Adaptive Mechanisms in Cortical Networks Underlying Cortical Contributions to Learning and Nondeclarative Memory M.M. Merzenich, G.H. Recanzone, W.M. Jenkins, and K.A. Grajski 873
Three-dimensional Object Recognition S. Ullman 889
A Theory of How the Brain Might Work T. Poggio 899
Toward a Neural Understanding of Visual Surface Representation K. Nakayama and S. Shimojo 911 xxii CONTENTS
Haptic Illusions: Experiments on Human Manipulation and Perception of "Virtual Objects" N. Hogan, B.A. Kay, E.D. Fasse, and F.A. Mussa-Ivaldi 925
Intrinsic Electrical Properties of Nerve Cells and Their Role in Network Oscil- lation R. Llin6s 933
Formation of Cortical Cell Assemblies W. Singer, C. Gray, A. Engel, P. KOnig, A. Artola, and S. BrOcher 939
Some Reflections on Visual Awareness F. Crick and C. Koch 953
Attentional Control of Visual Perception: Cortical and Subcortical Mechanisms R. Desimone, M. Wessinger, L. Thomas, and W. Schneider 963
Early Vision Is Bottom-up, Except for Focal Attention B. Julesz 973
Cytochrome Oxidase and Functional Coding in Primate Striate Cortex: A Hypoth- esis J. Allman and S. Zucker 979
Anatomical Explorations of Mind: Studies with Modern Imaging Techniques M.E. Raichle 983
Frontal Lobes and Memory for the Temporal Order of Recent Events B. Milner, M.P. McAndrews, and G. Leonard 987
Theoretical and Neurophysiological Analysis of the Functions of the Primate Hip- pocampus in Memory E.T. Rolls 995
Memory: Organization of Brain Systems and Cognition L, R. Squire, S. Zola-Morgan, C.B. Cave, F. Haist, G. Musen, and W.A. Suzuki 1007
Neocortical Memory Circuits P.S. Gotdman-Rakic, S. Funahashi, and C.J. Bruce 1025
Neural Regionalization of Knowledge Access: Preliminary Evidence A.R. Damasio, H. Damasio, D. Tranel, and J.P. Brandt 1039
Summary M. P. Stryker 1049
Author Index 1069 Subject Index 1071