Handbook of Behavioral Neurobiology Volume 4 Biological Rhythms HANDBOOK OF BEHAVIORAL NEUROBIOLOGY General Editor: Frederick A. King Yerkes Regional Primate Research Center, Emory University, Atlanta, Georgia Editorial Board: Vincent G. Dethier Robert W. Goy David A. Hamburg Peter Marler James L. McGaugh William D. Neff Eliot Stellar Volume 1 Sensory Integration Edited by R. Bruce Masterton Volume 2 Neuropsychology Edited by Michael S. Gazzaniga Volume 3 Social Behavior and Communication Edited by Peter Marler and J. G. Vandenbergh Volume 4 Biological Rhythms Edited by Jiirgen Aschoff Volume 5 Motor Coordination Edited by Arnold L. Towe and Erich S. Luschei A Continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediately upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher. Handbook of Behavioral Neurobiology Volume 4 Biological Rhythms Edited by Jiirgen Aschoff Max-Planck Institut fur Verhaltensphysiologie Andechs, German Federal Republic PLENUM PRESS, NEW YORK AND LONDON Library of Congress Cataloging in Publication Data Main entry under title: Biological rhythms. (Handbook of behavioral neurobiology; v. 4) Includes index. 1. Biological rhythms. I. Aschoff, J iirgen. II. Series. QP84.6.B56 591.1'882 80-21037 ISBN 978-1-4615-6554-3 ISBN 978-1-4615-6552-9 (eBook) DOl 10.1007/978-1-4615-6552-9 © 1981 Plenum Press, New York Softcover reprint of the hardcover 1st edition 1981 A Division of Plenum Publishing Corporation 227 West 17th Street, New York, N.Y. 10011 All righ ts 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 Contributors JDRGEN ASCHOFF, Max-Planck-Institut fur Verhaltensphysiologie, Andechs, West Germany SUE BINKLEY, Department of Biology, Temple University, Philadelphia, Pennsylvania JOHN BRADY, Department of Zoology and Applied Entomology, Imperial College of Sci­ ence and Technology at Silwood Park, Ascot, Berks, England CONSTANCE S. CAMPBELL, Department of Biological Sciences, Northwestern University, Evanston, Illinois PETER COLQUHOUN, Medical Research Council Perceptual and Cognitive Performance Unit, University of Sussex, Brighton, England SERGE DAAN, Zoology Department, Groningen State University, Haren, The Netherlands FRED C. DAVIS, Department of Anatomy and Brain Research Institute, University of Cal­ ifornia at Los Angeles, School of Medicine, Los Angeles, California MICHAEL G. DUBE, Department of Psychology, University of Florida, Gainesville, Florida JAMES THOMAS ENRIGHT, Scripps Institution of Oceanography, University of California­ San Diego, La Jolla, California EBERHARD GWINNER, Max-Planck-Institut fiir Verhaltensphysiologie, Radoljzell-Miig­ gingen, West Germany KLAUS HOFFMANN, Max-Planck-Institut fur Verhaltensphysiologie, Andechs, West Germany RONALD J. KONOPKA, Division of Biology, 216-76, California Institute of Technology, Pas­ adena, California MICHAEL MENAKER, Department of Biology, University of Oregon, Eugene, Oregon v VI MARTIN C. MOORE-EDE, Department of Physiology, Harvard Medical School, Boston, Massachusetts CONTRIBUTORS DIETRICH NEUMANN, Zoologisches Institut der Universitiit Kijln, KiJln, West Germany TERRY L. PAGE, Department of Biology, Vanderbilt University, Nashville, Tennessee THEODOSIOS PAVLIDIS, Department of Electrical Engineering and Computer Science, Princeton University, Princeton, New Jersey COLIN S. PITIENDRIGH, Hopkins Marine Station, Stanford University, Pacific Grove, California BENJAMIN RUSAK, Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada D. S. SAUNDERS, Department of Zoology, University of Edinburgh, Edinburgh, Scotland FRANK M. SULZMAN, Department of Physiology, Harvard Medical School, Boston, Massachusetts FRED W. TUREK, Department of Biological Sciences, Northwestern University, Evanston, Illinois HANS G. WALLRAFF, Max-Planck-Institut jilr Verhaltensphysiologie, Seewiesen, West Germany WILSE B. WEBB, Department of Psychology, University of Florida, Gainesville, Florida ROTGER WEVER, Max-Planck-Institut jilr Verhaltensphysiologie Andechs, West Germany Preface Interest in biological rhythms has been traced back more than 2,500]ears to Archilochus, the Greek poet, who in one of his fragments suggests ",,(i,,(VWO'KE o'olos pv{}J.tos txv{}pW7rOVS ~XH" (recognize what rhythm governs man) (Aschoff, 1974). Reference can also be made to the French student of medicine J. J. Virey who, in his thesis of 1814, used for the first time the expression "horloge vivante" (living clock) to describe daily rhythms and to D. C. W. Hufeland (1779) who called the 24-hour period the unit of our natural chronology. However, it was not until the 1930s that real progress was made in the analysis of biological rhythms; and Erwin Bunning was encouraged to publish the first, and still not outdated, monograph in the field in 1958. Two years later, in the middle of exciting discoveries, we took a breather at the Cold Spring Harbor Symposium on Biological Clocks. Its survey on rules considered valid at that time, and Pittendrigh's anticipating view on the temporal organization of living systems, made it a milestone on our way from a more formalistic description of biological rhythms to the understanding of their structural and physiological basis. In the meantime, rhythm research has attracted a steadily increasing number of work­ ers from various disciplines, and the stock of well-documented facts has grown quickly. It therefore seems timely that 20 years after the Cold Spring Harbor Symposium a new effort is made to summarize our knowledge. Volume 4 of the Handbook of Behavioral Neuro­ biology has in its title the term "rhythms," which is broader and less precise than "clocks." Hence, it is possible to include here discussions of rhythmic phenomena that do not nec­ essarily represent time-measuring devices-for example, the short-term rhythms in loco­ motor activity of animals, the temporal characteristics of sleep, and the ovarian cycle. On the other hand, rhythms of higher frequencies such as the firing of a receptor neurone, heart rate, and respiration are not treated. Instead, emphasis is placed on those rhythms which have evolved in adaptation to temporal programs in the environment, which have become part of the genetic makeup of organisms, and which can be used by organisms as true clocks. Daily (tidal and lunar) and annual rhythms are the main objectives. These Vll ... V1ll have in common that they behave like self-sustaining oscillations and that they can be entrained by periodic factors in the environment; together, they form the special class of the PREFACE so-called circarhythms. Circadian rhythms are treated in 14 of the 27 chapters. Discussions include the formal properties of entrainment, surveys on rhythms in behavior of invertebrates and vertebrates, their neural and endocrine control, the genetics and ontogeny of circadian rhythms and their adaptive significance. Two chapters are devoted to human circadian rhythms. In Part III, a discussion of tidal and lunar rhythms is followed by four chapters on annual rhythms, including photoperiodism in insects and vertebrates, and a chapter on human annual rhythms. Although each of the authors follows his own ideas of how to master his task, they all adhere to the same basic concept, including a common terminology (cf. the Glos­ sary). From their chapters, a unified picture emerges of the multioscillatory structure of biological systems and its control by central pacemakers. In essence, then, this volume dem­ onstrates that in behavior and neurobiology temporal organization is of as much relevance as is spatial organization. The study of the physiological mechanisms underlying circarhythms is a rapidly developing field, and the question of how discrete is the clock from the rest of the body (Pittendrigh, 1976) may soon be answered in the circadian case (M. Suda, O. Hayaishi, and H. Nakagawa, 1979). The overview given in this volume on the present state of the art hopefully will stimulate further research and, hence, become obsolete in some of its parts. However, I think it may also provide a valuable source of information for years to come. ]ORGEN ASCHOFF REFERENCES Aschoff, J. Speech after dinner. In J. Aschoff, F. Ceresa, and F. Halberg (Eds.), Chronobiological Aspects of Endocrinology. Chronobiologia, 1974, 1 (Suppl. 1),483-495. Bunning, E. Die Physiologische Uhr. Berlin: Springer Verlag, 1958. Chovnik, A. (Ed). Biological Clocks. Cold Spring Harbor Symposia in Quantitative Biology, 1961, 25. Pittendrigh, C. S. Circadian clocks: What are they? In J. W. Hastings and H. G. Schweiger (Eds.), The Molecular Basis of Circadian Rhythms (Dahlem Konferenzen 1975). Berlin: Life Sciences Research Reports, 1976. Suda, M., Hayaishi, 0., and Nakagawa, H. (Eds.). Biological Rhythms and Their Central Mechanism. Amsterdam: Elsevier, North Holland, 1979. Contents PART I INTRODUCTION CHAPTER 1 A Survey on Biological Rhythms . 3 Jiirgen Aschoff A Spectrum of Rhythms. 3 The Four "Circarhythms" . 5 Ultradian and Infradian Rhythms . 7 Interaction among Rhythms and Their Teleonomy . 7 References . 8 CHAPTER 2 Methodology . 11 James Thomas Enright Introduction. 11 A Schematic Example. 12 Complications for Interpretation. 14 The Search for Sustained Freerunning Rhythms . 14 The Demonstration of Entrainment