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The Role of Neuroplasticity in the Response to Drugs, 78 The Role of Neuroplasticity in the Response to Drugs DEPARTMENT OF HEALTH AND HUMAN SERVICES Public Health Service Alcohol, Drug Abuse, and Mental Health Administration The Role of Neuroplasticity in the Response to Drugs Editors: David P. Friedman, Ph.D. Doris H. Clouet, Ph.D. Neurosciences Research Branch Division of Preclinical Research National Institute on Drug Abuse NIDA Research Monograph 78 1987 U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES Public Health Service Alcohol, Drug Abuse, and Mental Health Administration National Institute on Drug Abuse 5600 Fishers Lane Rockville, Maryland 20857 For sale by the Superintendent of Documents, U.S. Government Printing Office Washington, DC 20402 NIDA Research Monographs are prepared by the research divisions of the National Institute on Drug Abuse and published by its Office of Science. The primary objective of the series is to provide critical reviews of research problem areas and techniques, the content of state-of-the-art conferences, and integrative research reviews. Its dual publication emphasis is rapid and targeted dissemination to the scientific and professional community. Editorial Advisors MARTIN W. ADLER, Ph.D. MARY L. JACOBSON Temple University School of Medicine National Federation of Parents for Philadelphia, Pennsylvania Drug-Free Youth Omaha, Nebraska SYDNEY ARCHER, Ph.D. Rensselaer Polytechnic lnstitute Troy, New York REESE T. JONES, M.D. Langley Porter Neuropsychiatric lnstitute RICHARD E. BELLEVILLE, Ph.D. San Francisco, California NB Associates. Health Sciences RockviIle. Maryland DENISE KANDEL, Ph.D. KARST J. BESTEMAN College of Physicians and Surgeons of Alcohol and Drug Problems Association Columbia University of North America New York, New York Washington, D. C. GILBERT J. BOTVIN, Ph.D. Cornell University Medical College HERBERT KLEBER, M.D. Yale University School of Medicine New York, New York New Haven. Connecticut JOSEPH V. BRADY, Ph.D. The Johns Hopkins University School of Medicine RICHARD RUSSO Baltimore, Maryland New Jersey State Department of Health Trenton, New Jersey THEODORE J. CICERO, Ph.D. Washington University School of Medicine St Louis, Missouri NIDA Research Monograph Series CHARLES R. SCHUSTER, Ph.D. Director, NIDA JEAN PAUL SMITH, Ph.D. Acting Associate Director for Science, NIDA Acting Editor Parklawn Building, 5600 Fishers Lane, RockviIle, Maryland 20857 The Role of Neuroplasticity in the Response to Drugs ACKNOWLEDGMENT This monograph is based upon papers and discussion from a technical review on the role of neuroplasticlty in the response to drugs which took place on September 22 and 23, 1986, at Rockville, Maryland. The meeting was sponsored by the Office of Science and the Division of Preclinical Research, National Institute on Drug Abuse. COPYRIGHT STATUS The National Institute on Drug Abuse has obtained permission from the copyright holders to reproduce certain previously published material as noted in the text. further reproduction of this copyrighted material is permitted only as part of a reprinting of the entire publication or chapter. For any other use, the copyright holder's permission is requlred. In additlon, the figures on pages 193, 194, and 197 are modified from copyrighted material. Before reprinting, readers are advised to determine the copyright status of these figures or to secure permission of the copyright holders. All other material in this volume except quoted passages from copyrighted sources is in the public domain and may be used or reproduced without permission from the Institute or the authors. Citation of the source is appreciated. The U. S. Government does not endorse or favor any specific commercial product or company. Trade, proprietary, or company names appearing in this publication are used only because they are considered essential in the context of the studies reported herein. DHHS Publication No. (ADM)90-1533 Alcohol, Drug Abuse, and Mental Health Administration Printed 1987, Reprinted 1990 NIDA Research Monographs are indexed in the Index Medicus. They are selectively included in the coverage of American Statistics Index Biosciences Information Service, Chemical Abstracts, Current Contents, Psychological Abstracts, and Psychopharmacology Abstracts. iv Preface On September 22 and 23, 1986, the National Institute on Drug Abuse held a technical review meeting entitled "The Role of Neuro- plasticity in the Response to Drugs" to review those factors that may alter the response of the central nervous system to a drug. Historically, researchers investigating the development of an increased or decreased response to a drug of abuse after its initial dose or after chronic administration have related these response changes to the continued presence of the drug. The mechanisms by which these adaptations were produced have remained largely unknown. In the last few years, however, there have been significant advances in understanding the plastic capacities of neural tissue, both in the developing nervous system and in the adult brain, that may shed light on the ability of the nervous system to alter its response to drugs. Adaptation in both the central and peripheral nervous systems may occur in milliseconds or take months, will differ from one discrete brain area to another, and will be specific for the external or internal stimu- lus evoking the response. Because one purpose of this technical review was to encourage the use of new ideas and methods from neuroscience in studies of abused drugs, participants included speakers who are interested in neural plasticity per se, those who are applying these concepts to response changes induced by neuro- transmitters and modulators, as well as those studying drug abuse problems directly. In the hope that this commingling would encourage neuroscientists to enter the drug abuse field, and to stimulate the use of new methodologies by researchers already in the field, material generated by this meeting has already been incorporated into a program announcement by the Neurosciences Branch, Division of Preclinical Research. The first group of speakers discussed plasticity in the developing nervous system. Because of the constant change taking place in the nervous system during development, and because the timing of developmental events depends on events that have already occurred, it is during development that the nervous system is most vulner- able to drugs. Some of the reasons for this vulnerability and v some of the consequences resulting from manipulation of the developing organism during this vulnerable period were described. B. MCEWEN ("External Factors Influencing Brain Development") dis- cussed the relative contributions of genetic and environmental factors in the development of the nervous system. Because envi- ronmental stimuli can act on the genome, however, the distinction between the two types of influences may, in some cases, not be particularly important. Steroid hormones, which are released by a variety of environmental stressors, act on the genome through spe- cific brain steroid receptors linked to a second messenger that causes repression or derepression of gene activity. Through this mechanism, extrinsic or intrinsic hormones can affect the develop- ment, cyclic activation, adaptation, amount of damage, and degree of reinnervation of the nervous system. Thus, epigenetic factors found in the environment can alter the phenotypic expression of a variety of neuronal traits. Drugs that alter the contribution of the genome to the adaptabil- ity of the nervous system will have long-term effects, whereas drugs that do not alter the normal contribution of the genetic complement will have actions of shorter duration. J. LICHTMAN ("Rearrangement of Synapses During Development") con- tinued the discussion of the vulnerability of the developing brain to external factors, such as drugs of abuse, by reviewing the way in which synaptic connections are made. Since synapses in differ- ent regions of the nervous system follow different rules of devel- opment, he described typical examples. At the neuromuscular junction, where, in the adult, a single nerve synapses on each muscle fiber, the maturing muscles have several axon terminals competing to occupy the end plate. As development progresses, all but one nerve retract to form the adult pattern. Similarly, in parts of the parasympathetic nervous system, each developing gang- lionic neuron is initially innervated by several axons, each of which arises from a different neuron. In this system also, multi- ple innervation becomes single, or at least reduced, by elimina- tion of some of the original afferents. In some areas of the central nervous system, a similar phenomenon is observed. Many climbing fibers impinge upon a single cerebel- lar Purkinje cell in young brains, but only one fiber innervates the adult cell. An analogous but more complex arrangement exists in the visual cortex, where, in the adult, information from each retina dominates alternating bands of cortex in a pattern called ocular dominance columns. In the developing brain, however, reti- nal inputs overlap. If input from one eye is eliminated during a short critical period during development, the ocular dominance columns fail to develop. Thus, in the changing patterns of devel- opment, there can be many sites and times at which the developing nervous system is vulnerable to external stimuli. vi L. SPEAR ("Drug-Vulnerable Events in Neuronal Development: Implications for the Selection of Test Methodologies") categorized the ways in which drugs influence
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