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

Volume 2

Volume 3

Volume 4

Volume 5

Sensory Integration Edited by R. Bruce Masterton

Neuropsychology Edited by Michael S. Gazzaniga

Social Behavior and Communication Edited by Peter Marler and J. G. Vandenbergh

Biological Rhythms Edited by Jiirgen Aschoff

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

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

80-21037

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 Sci­ence 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 Cal­ifornia 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 California­San Diego, La Jolla, California

EBERHARD GWINNER, Max-Planck-Institut fiir Verhaltensphysiologie, Radoljzell-Miig­gingen, West Germany

KLAUS HOFFMANN, Max-Planck-Institut fur Verhaltensphysiologie, Andechs, West Germany

RONALD J. KONOPKA, Division of Biology, 216-76, California Institute of Technology, Pas­adena, California

MICHAEL MENAKER, Department of Biology, University of Oregon, Eugene, Oregon

v

VI

CONTRIBUTORS

MARTIN C. MOORE-EDE, Department of Physiology, Harvard Medical School, Boston, Massachusetts

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 Neuro­biology 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 nec­essarily 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

PREFACE

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 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 Glos­sary). 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 dem­onstrates 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 Environmental Effects on Freerunning Period ...................... 17 Measurement of Phase Shift . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 Plasticity of Rhythm Properties .................................. 18

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

IX

x CHAPTER 3

CONTENTS Data Analysis .................................... , ................ . 21

James Thomas Enright

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

Some General Properties of the Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

Descriptive versus Inferential Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

Descriptive Statistics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

Objectivity in Measurement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

Determining Phase-Reference Points. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

Determining Amplitude of an Oscillation . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 Estimating the Period of a Rhythm ............................... 26 Descriptive Statistics: An Overview ............................... 32

Inferential Uses of Statistics. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32

The Use and Abuse of Standard Inferential Methods. . . . . . . . . . . . . . . . . . 32

Rhythm-Specific Issues in Inferential Statistics . . . . . . . . . . . . . . . . . . . . . . 34

Subjective Probability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

Summary......... ...... ....................................... 38

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

CHAPTER 4

Mathematical Models. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

Theodosios Pavlidis

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

Basic Concepts from the Theory of Oscillators ........................ 42

Dynamic Models of the Circadian Pacemaker. . . . . . . . . . . . . . . . . . . . . . . . . 44

Review of Models Dealing with Continuous Light. . . . . . . . . . . . . . . . . . . . . 47 Instances of the Dynamic Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 Population Phenomena. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 General Features of Populations of Oscillators . . . . . . . . . . . . . . . . . . . . . . . . 50 Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53

PART II DAILY RHYTHMS

CHAPTER 5

Circadian Systems: General Perspective. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57

Colin S. Pittendrigh

Innate Temporal Programs: Biological Clocks Measuring Environmental Time. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 Clocklike Properties of the "Circa-"Oscillators . . . . . . . . . . . . . . . . . . . . . . . . 58

Recognition of Local Time: Pacemaker Entrainment. . . . . . . . . . . . . . . . . . 59

Measurement of the Lapse of Time: Homeostasis of Pacemaker Period and Angular Velocity ............................................. . 60

Origin and Diversification of the Pacemaker's Clock Functions .......... . 60

Circadian Programs: Transition from Exogenous Temporal Order to Endogenous Temporal Organization ............................. . 60 Pacemaker Period and Generation Time .......................... . 61

Evolutionary Opportunism: Diversification of Pacemaker Functions . .... . 62

Pacemaker versus Program. . . . . ......................... . 63

Unicellular Systems . .......................................... . 63 Pacemaker Localization in Multicellular Systems ................... . 64

Pacemaker Localization and Zeitgeber Pathways . ................... . 65

Multiple Pacemakers: Mutual Coupling .......................... . 66 Pacemaker and Slave Oscillations: Hierarchical Entrainment . ......... . 68 Pacemaker and Slaves: The Temporal Program .................... . 68 Distortion of the Temporal Program by Exotic Light Cycles . .......... . 71

Photoperiodism: Seasonal Change in the Temporal Program ............ . 71

Convergence: Unity in the Diversity of Circadian Systems .............. . 76 References . . . . . . . . . ........................ . 77

CHAPTER 6

Freerunning and Entrained Circadian Rhythms ...................... . 81

Jiirgen Aschoff

Introduction ..... 81

Freerunning Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81

Dependence of Frequency on External and Internal Factors. . . . . . . . . 81

Variability of Frequency . . . . . . . . . . . . . . . . . . . . . . . . . . 84

Entrained Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . 86

Diversity of Zeitgebers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86

Entrainability and Phase Relationships . . . . . . . . . . . . . . . . . . . . . 86

Phase Shift of the Zeitgeber. . . . . . . . . . . . 90 Concluding Remarks. . . . . . . . . . . . . . . . . . . 91

References .....

CHAPTER 7

Circadian Systems: Entrainment

Colin S. Pittendrigh

Introduction ..... .

Entrainment: General Features

92

95

95 95

Discrete versus Continuous Entrainment Mechanisms . . . . . . . . . . . . . . . . . . 96

The Phase-Response Curves (PRCs) of Circadian Pacemakers. . . . . . . . . . . 98

Kinetics of Pacemaker Phase Shifts: Limit-Cycle Behavior. . . . . . . . . . . . . . . 103

Discrete Entrainment of the Pacemaker by Exotic Light Cycles. . . . . . . . . . . 104

The Phase Relation,1/;, of Pacemaker and Zeitgeber in Entrained Steady States. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104

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The Limits of Entrainment: Frequency Following . .................. . Frequency Demultiplication .................................... .

Entrainment by "Skeleton" Photoperiods ............................ .

Entrainment by "Complete" Photoperiods ........................... .

The Stability of Entrained Steady States ............................ .

Skeleton Photoperiods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Complete Photoperiods ........................................ .

Seasonal Change in the External Day: T and PRC Shape .............. .

Seasonal Change in the External Day: Complex Pacemakers ............ .

106 106 106 110 114 114 117

117

119 System Entrainment versus Pacemaker Entrainment ................... 121

Perspective. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

CHAPTER 8

Behavioral Rhythms in Invertebrates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

John Brady

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

Locomotor Activity Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126

Feeding Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

Mating Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

Rhythms in Reproductive Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

Gated Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133

Rhythms in Orientation Behavior .................................. 134 Time Sense . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135

Rhythmicity in Learning ......................................... 136 Rhythmic Changes in Responsiveness. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136 Overall Circadian Organization of Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . 137 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140

CHAPTER 9

Neural and Endocrine Control of Circadian Rhythmicity in Invertebrates 145

Terry L. Page

Introduction ........................ .'. . . . . . . . . . . . . . . . . . . . . . . . . . . 145

Circadian Pacemakers in the Nervous System . . . . . . . . . . . . . . . . . . . . . . . . . 146

Pacemakers in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146

Localization via Transplantation ................................. 148 Localization via Lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150 Multiple Pacemakers .......................................... 155

Circadian Rhythmicity and Sensorimotor Integration . . . . . . . . . . . . . . . . . . . 159

Circadian Modulation of CNS and Neurosecretory Activity. . . . . . . . . . . . . 159 Circadian Modulation of Sensory Input . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162

Photoreception and Entrainment .................................. . Photoreceptor Localization ..................................... . Neural Mechanisms in Entrainment . ............................ .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

CHAPTER 10

Genetics and Development of Circadian Rhythms in Invertebrates Ronald J. Konopka

163 163 168 169

173

Developmental Ontogeny of the Pacemaker and Overt Rhythms . . . . . . . . . . 173 Genetics of the Pacemaker and Overt Rhythms. . . . . . . . . . . . . . . . . . . . . . . . 177

Multigene Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177 Single-Gene Analysis .......................................... 178

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 180

CHAPTER 11

Vertebrate Behavioral Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183 Benjamin Rusak

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183 Mammals .............. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185

Activity ..................................................... 185 Learning and Memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

Birds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194 Activity ..................................................... 196

Reptiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198 Amphibians. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200 Fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201 Activity ..................................................... 201

Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 204 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205

CHAPTER 12

Internal Temporal Order . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215 Martin C. Moore-Ede and Frank M. Sulzman

Internal Temporal Order in Steady-State-Entrained Conditions .......... 215 Determinants of Rhythm Waveform. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216 Phase Maps of the Circadian System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 Inherited Features of Internal Temporal Order. . . . . . . . . . . . . . . . . . . . . . 219

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Plasticity of Phase ............................................ . Coupling Strength . ........................................... .

Temporal Order in the Absence of Environmental Time Cues ........... .

Internal Synchrony between Rhythms ............................ . Internal Phase-Angle Shifts .................................... .

220

220

221 221

222 Alterations in Circadian Waveform ............................... 222

Increased Plasticity of Phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223

Anatomical and Physiological Basis of Internal Temporal Order. . . . . . . . . . 223

Abstract Models of Internal Organization .......................... 224

Qualitative Models of the Circadian Timing System . . . . . . . . . . . . . . . . . . 231

Importance of Internal TemporalOrder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235

Advantages of a Periodic Internal System. . . . . . . . . . . . . . . . . . . . . . . . . . . 236

Consequences of Failures in Strict Internal Temporal Order. . . . . . . . . . . . 236 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 238

CHAPTER 13

Neural and Endocrine Control of Circadian Rhythms in the Vertebrates

Michael Menaker and Sue Binkley 243

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243

Perception of Entraining Signals .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244

Primary Pacemaking Structures. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247

The Avian Pineal Organ. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247

The Mammalian Suprachiasmatic Nuclei . . . . . . . . . . . . . . . . . . . . . . . . . . 252

Damped Oscillators and Driven Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . 253 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 253

CHAPTER 14

Ontogeny of Circadian Rhythms Fred C. Davis

Introduction ................................................... .

257

257 Emergence of Organization ....................................... 258

Measurement of Developing Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258 Development of Overt Rhythmicity in Humans. . . . . . . . . . . . . . . . . . . . . . 260

Physiology of Emerging Rhythmicity in the Rat . . . . . . . . . . . . . . . . . . . . . 262

Development of the Circadian System. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265 Role of the Environment in the Ontogeny of Rhythms . . . . . . . . . . . . . . . . . . 266

Light-Dark Cycles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266 The Mother as a Zeitgeber . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267 The Internal Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268

Aging. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268 Prospectus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270

CHAPTER 15

Adaptive Daily Strategies in Behavior

Serge Daan

275

Introduction: Selection Pressures for Daily Rhythms ................... 275

The Community: Nocturnal and Diurnal Ways of Life. . . . . . . . . . . . . . . . . 279

Night and Day in Evolutionary Radiation . . . . . . . . . . . . . . . . . . . . . . . . . . 280

Temporal Specialization . . . . . . . . .. ........................ 280

Temporal Segregation . . . . . . . . . . . . . . . . . . . . . . . . . . 281

Temporal Niche Shifts ..... . . . . . . . . . . . . . . . . . . . . . . . . . . 282

The Species: Daily Allocation of Time and Energy. . . . . . . . . . . 283

Foraging and Food Intake ......................... . . . . . . . . . . 285

Daily Movements and Migration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287

Reproduction an~ Life History . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289

The Individual: Daily Habits. . . . . . . . . . . . . . . . . . . . . . . . . . . . 291

Time Memory in Honeybees The Anticipation of Periodic Food The Strategy of Habits .......... .

References ........... .

CHAPTER 16

Clock-Controlled Orientation in Space .................................. .

Hans C. WallrafJ

Introduction. . . . . . . . . . ....... . Biological Clocks in Astro-Orientation ..

The Sun as an Orientational Cue ............... . The Moon as an Orientational Cue ..

291 293 294

296

299

299

299

300

305 The Stars as Orientational Cues . . . . . . . . . . . . . . . . . . . . 306

Other Aspects of Periodic Change of Oriented Activities. . . . . . . . . . . . . . 306 Periodic Change of Direction ...................... 306 Periodic Change of Locomotion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

CHAPTER 17

The Circadian System of Man .

Jiirgen AschofJ and Riitger Wever 311

Patterns of Rhythms: Reproducibility and Dependence on Conditions. . 311

Freerunning Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315

Entrainment by Artificial Zeitgebers . . . . . . . . . . . . . . . . . . . . . 317 Internal Desynchronization and Partial Entrainment . . . . . . . . . . . . . . 319

Shift Experiments and Flights . . . . . . . . . . . . . . . . . . . . . . . 325 Application to Problems in Medicine. References ....... .

327 329

xv

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· XVI CHAPTER 18

CONTENTS Rhythms in Performance ............................................ . 333 Peter Colquhoun

- Introduction: The Measurement of Performance Rhythms. . . . . . . . . . . . . . . 333 Time-of-Day Effects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335 Round-the-Clock Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 338 Effects of Phase Shifts of the Zeitgeber .... . . . . . . . . . . . . . . . . . . . . . . . . . . 340 Motivation, Situational Factors, and Individual Differences. . . . . . . . . . . . . . 343 Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 346 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347

PART III TIDAL, LUNAR, AND ANNUAL RHYTHMS

CHAPTER 19

Tidal and Lunar Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351 Dietrich Neumann

Tidal Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351 Environmental Conditions between Tidemarks . . . . . . . . . . . . . . . . . . . . . . 351 Temporal Adaptations of Behavior to Intertidal Conditions. . . . . . . . . . . . . 353

Circatidal Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356 Other Mechanisms for Tidal Timing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 361 The Modulation of Tidal Rhythms by Daily and Semimonthly Components. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 366

Lunar Rhythms ................................................ 367 Environmental Conditions Related to the Phases of the Moon. . . . . . . . . . . 367 Lunar-Rhythmic Adaptations of Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . 368 Semimonthly and Monthly Timing of Reproductive Behavior. . . . . . . . . . . 371

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 377

CHAPTER 20

Annual Rhythms: Perspective. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 381 Eberhard Gwinner

The Phenomenon of Seasonality. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 381 Ultimate Factors Controlling Annual Rhythms. . . . . . . . . . . . . . . . . . . . . . . . 383 Proximate Factors Controlling Annual Rhythms. . . . . . . . . . . . . . . . . . . . . . . 384

Proximate Factors Identical or Closely Related to Ultimate Factors. . . . . . 385 Proximate Factors Temporally Separated from Ultimate Factors . . . . . . . . 386 Circannual Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 386

Hierarchical Organization of Proximate Factors .. . . . . . . . . . . . . . . . . . . . 387 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 388

CHAPTER 21

Circannual Systems ................................................. . 391

Eberhard Gwinner

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391

Demonstration and Distribution of Circannual Rhythms . . . . . . . . . . . . . . . . 392

Properties of Circannual Rhythms under Constant Environmental Conditions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 394

Persistence of Circannual Rhythms ............................... 394

Range of Circannual Period Lengths: Transients. . . . . . . . . . . . . . . . . . . . . 395

Dependence of T on External Conditions. . . . . . . . . . . . . . . . . . . . . . . . . . . 395

Innateness of Circannual Rhythms. . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . 396 Relationship between Various Circannual Functions within an Individual Organism. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 396

Synchronization of Circannual Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397

Zeitgebers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397

Behavior within the Range of Entrainment . . . . . . . . . . . . . . . . . . . . . . . . . 399

Mechanisms of Circannual Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 400

General Remarks ............................................. 400

Circadian Rhythms as Possible Components of Circannual Rhythms . . . . . 400

A Sequence of Stages? If So, at What Level? . . . . . . . . . . . . . . . . . . . . . . . . 403

Adaptive Significance of Circannual Rhythms. . . . . . . . . . . . . . . . . . . . . . . . . 404

Timing of Seasonal Activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 404

Programming of Temporal Patterns. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 406

References ........ .

CHAPTER 22

Insect Photoperiodism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. S. Saunders

408

411

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 411 The Photoperiodic Response. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412

Photoperiodic Response Curves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412 Sensitive and Responsive Stages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 414 The Effects of Temperature on the Photoperiodic Response ............ 415 The Effects of Latitude and Altitude: Geographical Populations and the Genetics of the Response. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418

The Physiology of Photoperiodic Induction . . . . . . . . . . . . . . . . . . . . . . . . . . . 419 Photoreception and Spectral Sensitivity of the Photoperiodic Response . . . . 419 Time Measurement in Insect Photoperiodism: The "Nature" of the Clock. 421

An Attempted Rationalization of the Various Propositions to Account for Photoperiodic Induction in Insects. . . . . . . . . . . . . . . . . . . . . . . . 441

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 443

.. XVll

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CONTENTS

CHAPTER 23

Photoperiodism in Vertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Klaus Hoffmann

449

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449 Mammals ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449

The Photoperiodic Signal . . . . . . . . . . . . . . . . . . . . . . . .. ............. 450

Photoperiodic Effects on Puberty .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 451 Spontaneous Process and Photoperiodic Refractoriness ................ 451 Organs and Physiological Processes Involved. . . . . . . . . . . . . . . . . . . . . . . . 452 Endocrine Aspects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 458

Birds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 461

The Photoperiodic Mechanism. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 462 Photoperiodic Refractoriness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463 Organs and Physiological Processes Involved. . . . . . . . . . . . . . .. . . . . . . . . 463

Endocrine Aspects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 464 Lower Vertebrates .............................................. 465 Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 466 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 466

CHAPTER 24

- Annual Rhythms in Man. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 475 Jiirgen Aschoff

Preface ....................................................... . 475 Seasons in Physiology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 476 Mortality, Suicides, and Conception Rates .......................... 478

Treatment of Data. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478 Long- Term Trends in Acrophase and Amplitude ... . . . . . . . . . . . . . . . . . 479 Dependence on Latitude . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481

Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 485 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486

CHAPTER 25

PART IV RHYTHMS NOT DIRECTLY RELATED TO ENVIRONMENTAL CYCLES

Short-Term Rhythms in Activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 491 Serge Daan and Jiirgen Aschoff

Causal Considerations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 492 Functional Considerations ........................................ 495 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 497

CHAPTER 26

Temporal Characteristics of Sleep ..................................... .

Wilse B. Webb and Michael G. Dube

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

A Background of Sleep and Other Biological Rhythms ................. .

Sleep as a Biological Rhythm ..................................... .

Dimensions of Sleep .......................................... .

Temporal Characteristics of Human Sleep . ........................ . Comparative Aspects . ......................................... . Ontogenetic Aspects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Time Schedules of Sleep and Wakefulness ......................... .

Ultradian Rhythms and Sleep .................................... .

Ultradian Rhythms within Sleep ................................ .

Ultradian Sleep Rhythms and Wakefulness . ....................... . Sleep and Hormonal Rhythms .................................... .

The Central Nervous System and Sleep Rhythms ..................... .

References .................................................... .

CHAPTER 27

Cyclic Function of the Mammalian Ovary

Constance S. Campbell and Fred W. Turek

499

499

499

501

501

501

502

506

508

510 510

512

513

515

517

523

Rhythmic Variables Associated with the Ovarian Cycle . . . . . . . . . . . . . . . . . 524

The Cycle of the Ovary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 524

The Cycle of Hormones. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526

Behavioral Aspects of the Ovarian Cycle ........................... 528 Factors That Alter Characteristics of the Ovarian Cycle within a Given

Species. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 530

Light. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 530 Temperature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 531 Nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 532

Social Factors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 532 Interspecific Differences in the Temporal Occurrence of Ovarian Cycles. . . . 533

Seasonal versus Nonseasonal Breeders. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 533 Continuous Estrous, Polyestrous, and Monestrous Cyclers. . . . . . . . . . . . . . 538

The Relationship of Ovarian Cycles to the Circadian System. . . . . . . . . . . . . 538 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 540

Glossary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547

Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549

XIX

CONTENTS