CEREBRAL CORTEX Volume 14 Neurodegenerative and Age-Related Changes in Structure and Function of Cerebral Cortex CEREBRAL CORTEX Series Editors: Edward G. Jones and Alan Peters Advisory Committee Antonio R. Damasio, Iowa City, Iowa Irving T. Diamond, Durham, North Carolina Michael S. Gazzaniga, Hanover, New Hampshire Patricia Goldman-Rakic, New Haven, Connecticut Jon H. Kaas, Nashville, Tennessee Thomas L. Kemper, Boston, Massachusetts Kevan A. C. Martin, Zurich, Switzerland John H. Morrison, New York, New York Kathleen S. Rockland, Iowa City, Iowa Adam M. Sillito, London, England Philip S. Ulinksi, Chicago, Illinois Volume 1: Cellular Components of the Cerebral Cortex Volume 2: Functional Properties of Cortical Cells Volume 3: Visual Cortex Volume 4: Association and Auditory Cortices Volume 5: Sensory-Motor Areas and Aspects of Cortical Connectivity Volume 6: Further Aspects of Cortical Function, Including Hippocampus Volume 7: Development and Maturation of Cerebral Cortex Volume 8A: Comparative Structure and Evolution of Cerebral Cortex, Part I Volume 8B: Comparative Structure and Evolution of Cerebral Cortex, Part II Volume 9: Normal and Altered States of Function Volume 10: Primary Visual Cortex in Primates Volume 11: The Barrel Cortex of Rodents Volume 12: Extrastriate Cortex in Primates Volume 13: Models of Cortical Circuits Volume 14: Neurodegenerative and Age-Related Changes in Structure and Function of Cerebral Cortex Series Editors: Edward G. Jones and Alan Peters CEREB CORTEX Volume 14 N eurodegenerative and Age-Related Changes in Structure and Function of Cerebral Cortex Edited by ALAN PETERS Boston University School of Medicine Boston, Massachusetts and JOHN H. MORRISON Mount Sinai Medical Center New York, New York Springer Science+Business Media, LLC The Library of Congress cataloged the first volume of this title as follows: Main entry under title: Cerebral cortex. Includes bibliographical references and index. Contents: v. 1. Cellular components ofthe cerebral cortex. 1. Cerebral cortex-Collected works. 1. Peters, Alan, 1929- II. Jones, Edward G., 1939- . [DNLM: 1. Cerebral cortex-Anatomy and histology. 2. Cerebral cortex-Physio1ogy. WL 307 C4136] QP383.C45 1984 612'.825 84-1982 ISBN 978-1-4613-7216-5 ISBN 978-1-4615-4885-0 (eBook) DOI 10.1007/978-1-4615-4885-0 © 1999 Springer Science+Business Media New York Originally published by Kluwer Academic /P1enum Publishers in 1999 Softcover reprint ofthe hardcover Ist edition 1999 AII rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher Sir John Carew Eccles (1903-1997) John Eccles died peacefully at his home near Locarno on May 2, 1997. During the course of a long life, he dominated a whole era of neuroscience, not only through his works but also through the large number of neuroscientists that he trained and who went on to become leaders in their field. Trained by Charles Sherrington at Oxford, Eccles was in many ways the living embodiment of the Sherringtonian tradition in neuropsychology. His life in science was one from which many drew inspiration but one that few could hope to emulate. A skillful technician and a tireless experimenter, he could intellectually and physically exhaust whole relays of much younger persons. At the peak of his career, his scientific output was prodigious and groundbreaking. During his highly productive years at Canberra, which became the Mecca to which virtually every neurophysiologist of a generation was drawn, Eccles was richly blessed with resources of material and personnel. But it was not always so: the first intracellular recordings from motoneurons, which led ultimately to the Nobel Prize, were begun before moving to Canberra, under conditions that were far from optimal and that would have made a lesser person blanch. Eccles deserved his place in the sun. A formidable debater, Eccles never shirked the task of vigorously promoting his current ideas, yet he dropped them with a generous spirit when evidence to the contrary was marshaled against them. Indeed, his tergiversations often served to highlight an incremental advance in scientific understanding. By the time he joined the editorial advisory board of Cerebral Cortex in 1984, his experimental career had been over for some years, Canberra and its successor laboratories at Chicago and Buffalo being long past. But he was still in full command of his intellectual powers, knew everyone who was doing anything significant in the field, and offered us many suggestions that were helpful in ensuring the success of our venture. Not content with being a mere adviser, he contributed to Volume 2 with a theory of the operation of the neocortex. The chapter ranged widely, from anatomical modularity through the role of calcium in long-term synaptic plasticity to models of memory and cognition, stressing the links between memory and cognitive experience and reflecting that "all experiencing is tinged with remembering." It was a style of writing that few scientists can command today, but typical of the man behind the pen. John Eccles's passing presages the end of an era in neuroscience, an era in which the foundations of modern cellular neurophysiology were laid. His was not the sole contribution by any means, but such was the force of his personality, the power of his intellect, and his influence on a generation of neuroscientists, that, like one of similar attributes in the early seminal era of physiology, Johannes Muller, he was truly one of its colossi. Edward G.Jones Davis, California Contributors John R. Absher Cingulum NeuroSciences Institute, Winston-Salem, North Carolina 27101; and Departments of Physiol ogy, Pharmacology, and Neurology, Wake Forest Uni versity School of Medicine, Winston-Salem, North Carolina 27157-1083 Marilyn S. Albert Departments of Psychiatry and Neurology, Massa chusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02118 Amy F. T. Arnsten Section of Neurobiology, Yale Medical School, New Haven, Connecticut 06510-8001 Gene J. Blatt Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachu setts 02118 Constantin Booras Department of Psychiatry, HUG Belle-Idee, Univer sity of Geneva School of Medicine, CH-1225 Geneva, Switzerland; and Kastor Neurobiology of Aging Lab oratories, Mount Sinai School of Medicine, New York, New York 10029 Eva Braak Department of Anatomy, J. W. Goethe University, D-60590 Frankfurt, Germany Heiko Braak Department of Anatomy, J. W. Goethe University, D-60590 Frankfurt, Germany Peter B. Crino Department of Neurology, University of Pennsylva nia School of Medicine, Philadelphia, Pennsylvania 19104 vii viii James H. Eberwine Departments of Pharmacology and Psychiatry, Uni CONTRIBUTORS versity of Pennsylvania School of Medicine, Phila delphia, Pennsylvania 19104 Lindsay A. Farrer Departments of Medicine (Genetics Program) and Neurology, Boston University School of Medicine, and Department of Epidemiology and Biostatistics, Boston University School of Public Health, Boston, Massachusetts 02118 Fred H. Gage Laboratory of Genetics, The Salk Institute, LaJolla, California 92037 James W. Geddes Sanders-Brown Center on Aging and Department of Anatomy and Neurobiology, University of Kentucky, Lexington, Kentucky 40536-0230 Stephen D. Ginsberg The Center for Neurodegenerative Disease Re search, Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Med icine, Philadelphia, Pennsylvania 19104-4283 James G. Herndon Yerkes Regional Primate Research Center, Emory University, Atlanta, Georgia 30322 Asao Hirano Division of Neuropathology, Department of Pathol ogy, Montefiore Medical Center, Bronx, New York 10467 Patrick R. Hof Kastor Neurobiology of Aging Laboratories, Fishberg Research Center for Neurobiology and Department of Geriatrics and Adult Development, and Depart ment of Ophthalmology, Mount Sinai School of Medicine, New York, New York 10029 Thomas L. Kemper Departments of Pathology, Anatomy and Neurobiol ogy, and Neurology, Boston University School of Medicine, Boston, Massachusetts 02118 Ronald J. Killiany Department of Neuroanatomy and Neurobiology, Boston University School of Medicine, Boston, Mas sachusetts 02118 J. H. Kordower Research Center for Brain Repair, Department of Neurological Sciences, Rush Alzheimer's Disease Center, Rush Presbyterian-St. Luke's Medical Center, Chicago, Illinois 60612 Virginia M.-Y. Lee The Center for Neurodegenerative Disease Re search, Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Med icine, Philadelphia, Pennsylvania 19104-4283 Alex Martin National Institute of Mental Health, Bethesda, Mary ix land 20892-1366 CONTRIBUTORS Eliezer Masliah Departments of Neurosciences and Pathology, Uni versity of California, San Diego, La Jolla, California 92093-0624 John H. Morrison Kastor Neurobiology of Aging Laboratories, Fishberg Research Center for Neurobiology and Department of Geriatrics and Adult Development, Mount Sinai School of Medicine, New York, New York 10029 Mark B. Moss Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachu setts 02118 E.J. Mufson Research Center for Brain Repair, Department of Neurological Sciences, Rush Alzheimer's Disease Center, Rush Presbyterian-St. Luke's Medical Center, Chicago, Illinois 60612 Imaharu Nakano Department of Neurology, Jichi Medical School, Tochigi-ken, 329-0498 Japan Timothy J. Nicholson Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachu setts 02118 Alan Peters Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachu setts 02118 Daniel A. Peterson Laboratory of Genetics, The Salk Institute, La Jolla, California 92037; present address: Department of Neu roscience, Finch University of Health Sciences, The Chicago Medical School, North Chicago, Illinois 60064-3095 Douglas L. Rosene Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachu setts 02118; and Yerkes Regional Primate Research Center, Emory University, Atlanta, Georgia 30322 M. Luise Schmidt The Center for Neurodegenerative Disease Re search, Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Med icine, Philadelphia, Pennsylvania 19104-4283 David P. Salmon Department of Neurosciences, University of Califor nia, San Diego, La Jolla, California 92093-0948 x D. Larry Sparks Sun Health Research Institute, Sun City, Arizona CONTRIBUTORS 85351; and Division of Medical Examiner's Service, Kentucky Justice Cabinet, Frankfort, Kentucky 40601 John Q. Trojanowski The Center for Neurodegenerative Disease Re search, Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Med icine, Philadelphia, Pennsylvania 19104-4283 Brent A. Vogt Cingulum NeuroSciences Institute, Winston-Salem, North Carolina 27101; and Departments of Physiol ogy, Pharmacology, and Neurology, Wake Forest Uni versity School of Medicine, Winston-Salem, North Carolina, 27157-1083 Leslie J. Vogt Cingulum NeuroSciences Institute, Winston-Salem, North Carolina 27101; and Departments of Physiol ogy, Pharmacology, and Neurology, Wake Forest Uni versity School of Medicine, Winston-Salem, North Carolina 27157-1083 Kent E. Vrana Cingulum NeuroSciences Institute, Winston-Salem, North Carolina 27101; and Departments of Physiol ogy, Pharmacology, and Neurology, Wake Forest Uni versity School of Medicine, Winston-Salem, North Carolina 27157-1083 MarkJ. West Department of Neurobiology, University of Aarhus, 8000 Aarhus C, Denmark