Sexual Differentiation of the Brain edited by Akira Matsumoto, Ph.D. CRC Press Boca Raton London New York Washington, D.C. © 2000 by CRC Press LLC Library of Congress Cataloging-in-Publication Data Sexual differentiation of the brain / edited by Akira Matsumoto. p. cm. Includes bibliographical references and index. ISBN 0-8493-1165-9 (alk. paper) 1.Neuroendocrinology. 2. Brain—Differentiation. 3. Sex. differentiation. I. Matsumoto, Akira, 1943– . QP356.4.S49 1999 612.8'2—dc21 99-37571 CIP This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. Neither this book nor any part may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, microfilming, and recording, or by any information storage or retrieval system, without prior permission in writing from the publisher. All rights reserved. Authorization to photocopy items for internal or personal use, or the personal or internal use of specific clients, may be granted by CRC Press LLC, provided that $.50 per page photocopied is paid directly to Copyright Clearance Center, 27 Congress Street, Salem, MA 01970 USA. The fee code for users of the Transactional Reporting Service is ISBN 0-8493-1165-9/00/$0.00+$.50. The fee is subject to change without notice. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. The consent of CRC Press does not extend to copying for general distribution, for promotion, for creating new works, or for resale. Specific permission must be obtained in writing from CRC Press for such copying. Direct all inquiries to CRC Press LLC, 2000 Corporate Blvd., N.W., Boca Raton, Florida 33431. © 2000 by CRC Press LLC. No claim to original U.S. Government works International Standard Book Number 0-8493-1165-9 Library of Congress Card Number 99-37571 Printed in the United States of America 1 2 3 4 5 6 7 8 9 0 Printed on acid-free paper © 2000 by CRC Press LLC Preface This monograph is dedicated to Dr. Yasumasa Arai who retired from the pro- fessorship in anatomy at the Juntendo University School of Medicine in March 1998. He is an internationally established scientist, contributing to the advance of neuroendocrinology and neuroscience for more than 30 years. He is a member of the Editorial Boards of Hormones and Behavior and the Journal of Neuroendocrinology. He has conducted important research in the under- standing of sexual differentiation of the brain and sex steroid influences on neural and behavioral functions. Sex steroids exert influences on modulating neural development and neu- ral circuit formation in developing the sex steroid–sensitive neuroendocrine brain. Estrogen or aromatizable androgen can act as a neurotrophic factor on neural tissues, stimulating axonal and dendritic growth and synapse forma- tion. The development of sexual dimorphism in neural structures such as nuclear volume and synaptic organization may reflect sex steroid–modulat- ing neural development and synapse formation during the perinatal period. Recent neurobiological and molecular biological studies in this field have provided new information about mechanisms underlying sexual differentia- tion of the brain. Moreover, attempts have been made to clarify sex differ- ences in the human brain by using anatomical and noninvasive techniques such as MRI or PET. Psychological studies also have contributed in revealing the difference. All of the contributors, leading scientists in this field, have reviewed the most recent advances in studies on sexual differentiation of the brain. The monograph will provide a valuable insight into the current state of knowledge about this field. Akira Matsumoto © 2000 by CRC Press LLC Editor Akira Matsumoto, Ph.D., is an associate professor in the Department of Anatomy, Juntendo University School of Medicine, Tokyo (Japan). Dr. Mat- sumoto received a B.S. degree (biology, 1968) and a Ph.D. degree (biology, 1974) from the University of Tokyo, Tokyo (Japan). He has served on the fac- ulty of the Department of Anatomy, Juntendo University School of Medicine from 1974 to present. He received an International Society of Andrology Award (1993) and a Zoological Science Award (1997). He served as coeditor of the Atlas of Endocrine Organs (Springer–Verlag, 1992). He is a member of the Society of Neuroscience, the International Brain Research Organization, the International Society of Neuroendocrinology, the Society of Behavioral Neu- roendocrinology, the International Society of Andrology, the Japanese Asso- ciation of Anatomists, the Japanese Association of Endocrinology, the Japan Neuroscience Society, the Japanese Society for Comparative Endocrinology, and the Zoological Society of Japan. His research interests concern the orga- nizational and activational effects of sex steroids on neural function and structures in the mammalian neuroendocrine brain. He has a number of pub- lications on topics in this field in prominent journals. © 2000 by CRC Press LLC Contributors Laurie A. Abler, B.S., Wisconsin Regional Primate Research Center, Univer- sity of Wisconsin, Madison, Wisconsin Paola Agrati, Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Yasumasa Arai, Ph.D., Laboratory of Medical Education, Juntendo Universi- ty School of Medicine, Tokyo, Japan Arthur P. Arnold, Ph.D., Departments of Physiological Science and Neurobi- ology, Laboratory of Neuroendocrinology of the Brain Research Institute, Mental Retardation Research Center, University of California, Los Ange- les, California Laura Bolzoni, Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy S. Marc Breedlove, Ph.D., Department of Psychology, University of Califor- nia, Berkeley, California Alessia Brusadelli, Center Milano Molecular Pharmacology Laboratory, In- stitute of Pharmacological Sciences, University of Milan, Milan, Italy Gloria Patricia Cardona-Gomez, Instituto Cajal, Consejo Superior de Inves- tigaciones Cientificas, Madrid, Spain Julie Ann Chowen, Ph.D., Instituto Cajal, Consejo Superior de Investiga- ciones Cientificas, Madrid, Spain Scott E. Christensen, M.A., Department of Psychology, University of Califor- nia, Berkeley, California Paolo Ciana, Ph.D., Center Milano Molecular Pharmacology Laboratory, In- stitute of Pharmacological Sciences, University of Milan, Milan, Italy David Crews, Ph.D., Institute of Reproductive Biology, Section of Integrative Biology, University of Texas, Austin, Texas © 2000 by CRC Press LLC Maria Carmen Fernandez-Galaz, Ph.D., M.D., Instituto Cajal, Consejo Supe- rior de Investigaciones Cientificas, Madrid, Spain Luis Miguel Garcia-Segura, Ph.D., Instituto Cajal, Consejo Superior de In- vestigaciones Cientificas, Madrid, Spain Roger A. Gorski, Ph.D., Department of Neurobiology, University of Califor- nia Los Angeles School of Medicine, Los Angeles, California Elizabeth Hampson, Ph.D., Department of Psychology and Neurosciences Program, University of Western Ontario, London, Ontario, Canada Melissa Hines, Ph.D., Department of Psychology, City University, London, United Kingdom John B. Hutchison, Ph.D., St. John’s College, University of Cambridge, Cam- bridge, United Kingdom CB21TP Cynthia L. Jordan, Ph.D., Department of Psychology, University of Califor- nia, Berkeley, California Adriana Maggi, Ph.D., Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Elena Marini, Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Luciano Martini, M.D., Department of Endocrinology, University of Milan, Milan, Italy Akira Matsumoto, Ph.D., Department of Anatomy, Juntendo University School of Medicine, Tokyo, Japan Clara Meda, Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Shizuko Murakami, Ph.D. Department of Anatomy, Juntendo University School of Medicine, Tokyo, Japan Paola Negri-Cesi, Ph.D., Department of Endocrinology, University of Milan, Milan, Italy Sonoko Ogawa, Ph.D., Laboratory of Neurobiology and Behavior, The Rock- efeller University, New York, New York © 2000 by CRC Press LLC Cesare Patrone, Ph.D., Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Michael C. Penlington, Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Donald W. Pfaff, Ph.D., Laboratory of Neurobiology and Behavior, The Rockefeller University, New York, New York Flavio Piva, Ph.D., Department of Endocrinology, University of Milan, Mi- lan, Italy Angelo Poletti, Ph.D., Department of Endocrinology, University of Milan, Milan, Italy Giuseppe Pollio, Ph.D., Center Milano Molecular Pharmacology Laboratory, Institute of Pharmacological Sciences, University of Milan, Milan, Italy Monica Rebecchi, Center Milano Molecular Pharmacology Laboratory, Insti- tute of Pharmacological Sciences, University of Milan, Milan, Italy Jon Sakata, Institute for Neuroscience, University of Texas, Austin, Texas Yoshie Sekine, B. Human S., Department of Anatomy, Juntendo University School of Medicine, Tokyo, Japan Nancy M. Sherwood, Ph.D., Department of Biology, University of Victoria, Victoria, British Columbia, Canada Rodolfo H. Sialino, Center Milano Molecular Pharmacology Laboratory, In- stitute of Pharmacological Sciences, University of Milan, Milan, Italy Richard B. Simerly, Ph.D., Division of Neuroscience, Oregon Regional Pri- mate Research Center, Beaverton, Oregon and Program in Neuroscience and Department of Cell and Developmental Biology, Oregon Health Sci- ences University, Portland, Oregon Ei Terasawa, Ph.D., Wisconsin Regional Primate Research Center and De- partment of Pediatrics, University of Wisconsin, Madison, Wisconsin Jose Luis Trejo, Instituto Cajal, Consejo Superior de Investigaciones Cientifi- cas, Madrid, Spain Elisabetta Vegeto, Ph.D., Center Milano Molecular Pharmacology Laborato- ry, Institute of Pharmacological Sciences, University of Milan, Milan, Italy © 2000 by CRC Press LLC James C. Woodson, M.A., Department of Psychology, University of Califor- nia Los Angeles, Los Angeles, California Harold H. Zakon, Ph.D., Section of Neurobiology and Institute for Neuro- science, University of Texas, Austin, Texas © 2000 by CRC Press LLC Contents 1. Sexual Differentiation of the Brain:AHistorical Review Yasumasa Arai 2. Genetic Contributions to the Sexual Differentiation of Behavior Sonoko Ogawa and Donald W. Pfaff 3. InVitro Study for Effects of Estrogen on Estrogen Receptor-Transfected Neuroblastoma Cells Paola Agrati, Laura Bolzoni, Alessia Brusadelli, Paolo Ciana, Elena Marini, Clara Meda, Cesare Patrone, Michael C. Penlington, Giuseppe Pollio, Monica Rebecchi, Rodolfo H. Sialino, ElisabettaVegeto, and Adriana Maggi 4. Steroid Metabolism in the Brain: Role in Sexual Differentiation Paola Negri-Cesi, Angelo Poletti, Luciano Martini, and Flavio Piva 5. Estrogen in Gender-Specific Neural Differentiation John B. Hutchison 6. Glial CellsAre Involved in Organizational andActivational Effects of Sex Hormones in the Brain Luis Miguel Garcia-Segura, Gloria P. Cardona–Gomez, Jose Luis Trejo, Maria C. Fernandez-Galaz, and Julie Ann Chowen 7. Sex Steroids and Weakly Electric Fish:AModel System for Activational Mechanisms of HormoneAction Harold H. Zakon 8. Evolution of Brain Mechanisms Controlling Sexual Behavior David Crews and Jon Sakata © 2000 by CRC Press LLC 9.Hormonal and Nonhormonal Mechanisms of Sexual Differentiation of the Zebra Finch Brain: Embracing the Null Hypothesis ArthurP. Arnold 10. Sexual Differentiation of a Neuromuscular System Scott E. Christensen, S. Marc Breedlove, and Cynthia L. Jordan 11. Development of Sexually Dimorphic Forebrain Pathways Richard B. Simerly 12. Sexual Differentiation of Neuronal Circuitry in the Hypothalamus Akira Matsumoto, Yoshie Sekine, Shizuko Murakami, andYasumasa Arai 13. Structural Sex Differences in the Mammalian Brain: Reconsidering the Male/Female Dichotomy James C. Woodson and Roger A. Gorski 14. Gonadal Hormones and Sexual Differentiation of Human Behavior: Effects of Psychosexual and Cognitive Development Melissa Hines 15. Sexual Differentiation of Spatial Functions in Humans Elizabeth Hampson 16. The Luteinizing Hormone–Releasing Hormone System in the Developing Monkey Brain EiTerasawa, Laurie A. Abler, and Nancy M. Sherwood © 2000 by CRC Press LLC
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