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COLLOQUIUM ON NEUROBIOLOGY OF PAIN

NATIONAL ACADEMY OF SCIENCES
WASHINGTON, D.C. 1999



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COLLOQUIUM ON NEUROBIOLOGY OF PAIN COLLOQUIUM ON NEUROBIOLOGY OF PAIN NATIONAL ACADEMY OF SCIENCES WASHINGTON, D.C. 1999

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN NATIONAL ACADEMY OF SCIENCES Colloquium Series In 1991, the National Academy of Sciences inaugurated a series of scientific colloquia, five or six of which are scheduled each year under the guidance of the NAS Council’s Committee on Scientific Programs. Each colloquium addresses a scientific topic of broad and topical interest, cutting across two or more of the traditional disciplines. Typically two days long, colloquia are international in scope and bring together leading scientists in the field. Papers from colloquia are published in the Proceedings of the National Academy of Sciences (PNAS).

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN National Academy of Sciences Colloquium Arnold and Mabel Beckman Center, Irvine The Neurobiology of Pain December 11–13, 1998 PROGRAM Friday, December 11, 1998 Introduction Ronald Dubner, Colloquium Organizer Session I: Channels Chair and Discussion Leader John Hunter, Department of Analgesia, Roche Bioscience Stephen G. Waxman, Department of Neurology, Yale University School of Medicine Sodium Channels and the Pathophysiology of Pain Michael Gold, Department of Oral and Craniofacial Biological Sciences, University of Maryland Dental School TTX-R INa and Inflammatory Hyperalgesia Daniel Weinreich, Department of Pharmacology and Experimental Therapeutics, University of Maryland, School of Medicine Which Potassium Channels Keep Vagal Afferent Neurons Mellow? Discussant Peter McNaughton, Department of Physiology, King’s College London Heat-Activated Ion Currents in Nociceptors–Transduction and Sensitization Session II: Receptors Chair and Discussion Leader Patrick Mantyh, Department of Preventive Sciences, School of Dentistry, University of Minnesota Amy B. MacDermott, Department of Physiology and Cellular Biophysics and Center for Neurobiology and Behavior, Columbia University AMPA and Kainate Receptor Expression by DRG Neurons in Culture Edwin W. McCleskey, Vollum Institute, Oregon Health Sciences University The Role of Sensory Modality-Selective Gene Transcription in Opioid Analgesia Michael W. Salter, Programmes in Brain and Behavior and Cell Biology, Hospital for Sick Children, and Department of Physiology, University of Toronto NMDA Receptors and Src in Synaptic Plasticity Discussant Edward R. Perl, Department of Physiology, University of North Carolina School of Medicine, Chapel Hill Receptor Expression and Regulation as Mechanisms Underlying Pain and Pain Pathology

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN Saturday, December 12, 1998 Introduction Michael Gold, Colloquium Organizer Tribute to John Liebeskind Gregory Terman, Department of Anesthesiology, University of Washington, Seattle Session III A: Systems and Imaging Chair and Discussion Leader Donna Hammond, Anesthesia and Critical Care, University of Chicago William D. Willis, Department of Anatomy and Neurosciences, University of Texas Medical Branch, Galveston, Texas Evidence for a Visceral Pain Pathway in the Dorsal Column of the Spinal Cord Tony L. Yaksh, Anesthesiology Research Laboratory, University of California The Spinal Biology in Humans and Animals of Pain States Generated by Persistent Small Afferent Input Discussant Gerald Gebhart, Department of Pharmacology, University of Iowa Session III B: Systems and Imaging Chair and Discussion Leader James Campbell, Department of Neurology, Johns Hopkins University Medical School Howard Fields, University of California, San Francisco Neuropeptides and Brainstem Pain Modulating Circuits Kenneth L. Casey, Neurological Service, Veterans Administration Medical Center, Ann Arbor, Michigan Forebrain Mechanisms of Nociception and Pain: Analysis through Imaging Discussant M. Catherine Bushnell, McGill University, Montreal What Are the Essential Cerebral Components? Session IV: Growth Factors and Cytokines Chair and Discussion Leader Kenneth Hargreaves, Department of Endodontics, University of Texas Health Sciences Center William Snider, Department of Neurology, Washington University Medical Center Trophic Factor Regulation of Nociceptor Development Lorne M. Mendell, Department of Neurobiology and Behavior, State University of New York at Stony Brook Neurotrophins and Pain Linda R. Watkins, Department of Psychology, University of Colorado at Boulder Immune-to-Brain Communication: Implications for Sickness and Pain Discussant Stephen B. McMahon, Neuroscience Research Centre, King’s College London Multiple Trophic Factor Influences on Nociceptive System

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN Saturday, December 12, 1998 Session V: Development and Plasticity Chair and Discussion Leader Ronald Dubner, Department of Oral and Craniofacial Biological Sciences, University of Maryland Dental School Maria Fitzgerald, Department of Anatomy and Developmental Biology, University College London Postnatal Changes in Dorsal Horn Cell Activity–The Development of Spinal Sensory Processing Clifford J. Woolf, Department of Anesthesia and Critical Care, Massachusetts General Hospital and Harvard Medical School Signal- and Activity-Dependent Plasticity in the Somatosensory System–Unraveling the Cellular and Molecular Mechanisms of Pain David J. Mayer, Department of Anesthesiology, Medical College of Virginia Cellular Mechanisms of Hyperalgesia and Morphine Tolerance and Their Interactions Discussant Gary Bennett, Department of Neurology, Allegheny University, Philadelphia The Revolution in Pain Research Banquet for Colloquium Attendees Banquet Speaker John Loeser, Department of Neurological Surgery and Anesthesiology, University of Washington Medical Center Sunday, December 13, 1998 Session VI: Molecular Genetics Chair and Discussion Leader Charles Inturrisi, Department of Pharmacology, Cornell University Medical College Allan Basbaum, Department of Anatomy, University of California, San Francisco The Neurochemistry of Acute and Persistent Pain Michael A. Moskowitz, Department of Neurosurgery and Neurology, Massachusetts General Hospital Migraine Pathophysiology and Treatment Mechanisms Jeffrey Mogil, Department of Psychology, University of Illinois at Urbana The Genetics of Pain and Pain Inhibition: From Mice to Molecules George Uhl, National Institute on Drug Abuse, National Institutes of Health The Mu Opiate Receptor as a Model Gene for Individual Differences in Pain and Pain Modulation Discussant Frank Porreca, Department of Pharmacology, University of Arizona Health Sciences Center Antisense Oligodeoxynucleotides against the TTX-Resistant Sodium Channel, PN3, Prevent and Reverse Chronic, Inflammatory and Neuropathic Pain in the Rat

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN List of Attendees Lisa Aimone George S. Aitken, Delta Medical Dental Centre David J. Anderson, California Institute of Technology David Andrew, Barrow Neurological Institute K. Roger Aoki, Allergan Dietrich Arndts, Boehringer Ingelheim Ronald K. Ashley Laura Audell Victor Babenko, Aalborg University Leif K. Bakland, Loma Linda University School of Dentistry Allan Basbaum, University of California, San Francisco Gary Bennett, MCP Hahnemann University Jack M. Berger, University of Southern California School of Medicine Scott Bowersox, Elan Pharmaceuticals Walter Bowles, University of Minnesota Robert Brennan, University of California, Los Angeles Cathy Bushnell, McGill University James Campbell, John Hopkins University Yuqing Cao, University of California, San Francisco Ken Casey, University of Michigan Lin Chang, University of California, Los Angeles Jenny Chen, University of California, Los Angeles Zhou-Feng Chen, California Institute of Technology Ken Chow, Allergan Glenn Clark, University of California, Los Angeles Patricia Claude, University of Texas, Health Science Center at San Antonio Amy D. Clegg Joseph R. Cohen, University of California, Los Angeles Sean P. Cook, Oregon Health Sciences University-Vollum Institute, L-474 Santosh Coutinho, University of California, Los Angeles Marie Csete, California Institute of Technology Minglei Cui, Allergan Bennet Davis Xinzhong Dong, California Institute of Technology Emma Dormand, California Institute of Technology Ronald Dubner, University of Maryland Dental School Helena Ennes, University of California, Los Angeles Mark Erlander, RW Johnson Pharmalogical Research Institute Stephen EspitiaJack L. Feldman, University of California, Los Angeles Howard Fields, University of California, San Francisco Maria Fitzgerald, University College London Christopher M. Flores, University of Texas Nicholas Fuller, Cedars-Sinai Medical Center-The Pain Center Gerald Gebhart, University of Iowa Daniel W. Gil, Allergan, Inc. Michael Gold, University of Maryland Dental School Jay A. Goldstein Robert Grimm Paul Haerich, Loma Linda University Aldric Hama Donna Hammond, University of Chicago Michael Hans Kenneth Hargreaves, University of Texas, Health Science Center at San Antonio Michael Hayward, Oregon Health Sciences University Standiford Helm David Helton, B. Braun Medical Inc. Michael A. Henry, University of Colorado Health Science Center H. Haydon Hill, Rehabilitation Medicine Associates Dianne Hodges, CoCensys, Inc. Lynda C. Honour John Hunter, Roche Victor Ilyin, CoCensys, Inc Charles Inturrisi, Cornell University Douglass L. Jackson, University of Washington-School of Dentistry Stephen W. Jenkins, Allergan, Inc. Russell Johnson, University of California, Los Angeles Gerald J. Jonak, Dupont Wade Kingery, Veterans Adminstration Cheryl Kitt, National Institutes of Health Beat Knusel, Allergan, Inc Brad Kolls Chris Konkoy Lawrence Kruger, University of California, Los Angeles Medical Center Nancy Lan, CoCensys Inc. Letitia Lau Jacqueline E. Lee, University of Colorado, Boulder Julia Liebeskind Wei-Jen Lin, Allergan John Loeser

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN Lin Luo, RW Johnson Pharmalogical Research Institute Z. David Luo, University of California, San Diego Kabirullah Lutfy, University of California, Los Angeles Amy MacDermott, Columbia University Nigel T. Maidment, University of California, Los Angeles Celine Maillot, West Los Angeles V.A. Medical Center Phil Malan, The University of Arizona Mario G. Maldonado Annika Malmberg, University of California, San Francisco Corinne Manetto, Cedars-Sinai Comprehensive Cancer Center Patrick Mantyh, University of Minnesota Jianren Mao, VCU Wendy Martin, Glaxo Wellcome, Inc. William J. Martin, University of California, San Francisco Juan Carlos Marvizon, University of California, Los Angeles Emeran A. Mayer, University of California, Los Angeles, Division of Digestive Diseases Ed McCleskey, Oregon Health Sciences University Steve McMahon, King’s College London Peter McNaughton, King’s College London Lorne Mendell, State University of New York, Sunny Brook Robert L. Merrill, University of California, Los Angeles School of Dentistry Somsak Mitrirattanakul, University of California, Los Angeles Jeffrey Mogil, University of Illinois at Urbana Champaign Derek Molliver, Washington University of Saint Louis Carlo V. Morpurgo Mike Moskowitz, Harvard University Million Mulugeta, West Los Angeles V.A. Medical Center Alexander Nemirovsky John K. Neubert Alan Newman Michael Ossipov, University of Arizona A. Pace-Floridia Pamela Pierce Palmer, University of California, San Francisco Ed Perl, University of North Carolina Karla Petersen, University of California, San Francisco Frank Porreca, University of Arizona Joshua P. Prager, California Pain Medical Center Robert W. Presley, Pain Care Specialists Steven Graff Radford, University of California, Los Angeles John L. Reeves II, University of California, Los Angeles Ke Ren, University of Maryland Linda J. Rever Steven Richeimer, University of California, Davis Ruth Riley, University of California, San Francisco Susan Roche, Orofacial Pain Management Clinic Gary G. Rosengarten, The Pain Center, CSMC Mike Salter, University of Toronto Christine Sang Harry Sernaker, University of Maryland Seth Silbert, Oregon Health Sciences University-Vollum Inst. William Snider, Washington University Michael C. Son Linda S. Sorkin, University of California, San Diego Athena Spanoyannis, Allergan Inc. Igor Spigelman, University of California, Los Angeles, School of Dentistry Yvette Tache, University of California, Los Angeles Brad Taylor, University of California, San Francisco Edgar Tenorio, Elan Pharmaceuticals Gregory Terman Arnold Towe, University of Washington Jodie Trafton, University of California, San Francisco George Uhl, National Institute of Health Clayton Varga, PRI Douglas R. Wall Wendy M. Walwyn, University of California John Y.-X. Wang, Elan Pharmaceuticals Yu Hua Wang, University of California, Los Angeles Linda Watkins, University of Colorado Steve Waxman, Yale University Jen Yu Wei, University of California, Los Angeles, School of Medicine Daniel Weinreich, University of Maryland Ursula Wesselman, Johns Hopkins University Larry A. Wheeler, Allergan Joan Wilentz, National Institute of Dental and Cranofacial Research William Willis, University of Texas Medical Branch Steven P. Wilson, University of South Carolina School of Medicine Richard Woodward, Cocensys Inc. Clifford Woolf, Harvard University Tony Yaksh, University of California, San Diego Jen Yu, University of California, Irvine Medical Center

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN P ROCEEDINGS OF THE N ATIONAL A CADEMY OF S CIENCES OF THE U NITED S TATES OF A MERICA Table of Contents Papers from a National Academy of Sciences Colloquium on The Neurobiology of Pain     The neurobiology of pain Ronald Dubner and Michael Gold   7627–7630     John C. Liebeskind (1935–1997): A tribute Gregory W. Terman   7631–7634     Sodium channels and pain S. G. Waxman, S. Dib-Hajj, T. R. Cummins, and J. A. Black   7635–7639     A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain Frank Porreca, Josephine Lai, Di Bian, Sandra Wegert, Michael H. Ossipov, Richard M. Eglen, Laura Kassotakis, Sanja Novakovic, Douglas K. Rabert, Lakshmi Sangameswaran, and John C. Hunter   7640–7644     Tetrodotoxin-resistant Na+ currents and inflammatory hyperalgesia Michael S. Gold   7645–7649     Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons Ruth Cordoba-Rodriguez, Kimberly A. Moore, Joseph P. Y. Kao, and Daniel Weinreich   7650–7657     Ion channels gated by heat P. Cesare, A. Moriondo, V. Vellani, and P. A. McNaughton   7658–7663     Causalgia, pathological pain, and adrenergic receptors Edward R. Perl   7664–7667     Forebrain mechanisms of nociception and pain: Analysis through imaging Kenneth L. Casey   7668–7674     A visceral pain pathway in the dorsal column of the spinal cord William D. Willis, Elie D. Al-Chaer, Michael J. Quast, and Karin N. Westlund   7675–7679     The spinal biology in humans and animals of pain states generated by persistent small afferent input Tony L. Yaksh, Xiao-Ying Hua, Iveta Kalcheva, Natsuko Nozaki-Taguchi, and Martin Marsala   7680–7686     Supraspinal contributions to hyperalgesia M. O. Urban and G. F. Gebhart   7687–7692     Neurotrophins and hyperalgesia X.-Q. Shu and L. M. Mendell   7693–7696     Src, a molecular switch governing gain control of synaptic transmission mediated by N-methyl-D-aspartate receptors Xian-Min Yu and Michael W. Salter   7697–7704

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COLLOQUIUM ON NEUROBIOLOGY OF PAIN     Pain perception: Is there a role for primary somatosensory cortex? M. C. Bushnell, G. H. Duncan, R. K. Hofbauer, B. Ha, J.-I. Chen, and B. Carrier   7705–7709     Implications of immune-to-brain communication for sickness and pain Linda R. Watkins and Steven F. Maier   7710–7713     Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord S. W. N. Thompson, D. L. H. Bennett, B. J. Kerr, E. J. Bradbury, and S. B. McMahon   7714–7718     The postnatal development of spinal sensory processing Maria Fitzgerald and Ernest Jennings   7719–7722     Transcriptional and posttranslational plasticity and the generation of inflammatory pain Clifford J. Woolf and Michael Costigan   7723–7730     Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions David J. Mayer, Jianren Mao, Jason Holt, and Donald D. Price   7731–7736     Does a neuroimmune interaction contribute to the genesis of painful peripheral neuropathies? Gary J. Bennett   7737–7738     Distinct neurochemical features of acute and persistent pain Allan I. Basbaum   7739–7743     The genetic mediation of individual differences in sensitivity to pain and its inhibition Jeffrey S. Mogil   7744–7751     The µ opiate receptor as a candidate gene for pain: Polymorphisms, variations in expression, nociception, and opiate responses George R. Uhl, Ichiro Sora, and Zaijie Wang   7752–7755