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 ...... 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 Xl Angular Velocity ...... 60 CONTENTS 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 ..... 92

CHAPTER 7 Circadian Systems: Entrainment 95 Colin S. Pittendrigh

Introduction ...... 95 Entrainment: General Features 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 Xli The Limits of Entrainment: Frequency Following ...... 106 Frequency Demultiplication ...... 106 CONTENTS Entrainment by "Skeleton" Photoperiods ...... 106 Entrainment by "Complete" Photoperiods ...... 110 The Stability of Entrained Steady States ...... 114 Skeleton Photoperiods ...... 114 Complete Photoperiods ...... 117 Seasonal Change in the External Day: T and PRC Shape ...... 117 Seasonal Change in the External Day: Complex Pacemakers ...... 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 ...... 163 XUl Photoreceptor Localization ...... 163 CONTENTS Neural Mechanisms in Entrainment ...... 168 References ...... 169

CHAPTER 10 Genetics and Development of Circadian Rhythms in Invertebrates 173 Ronald J. Konopka 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 XIV Plasticity of Phase ...... 220 Coupling Strength ...... 220 CONTENTS Temporal Order in the Absence of Environmental Time Cues ...... 221 Internal Synchrony between Rhythms ...... 221 Internal Phase-Angle Shifts ...... 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 243 Michael Menaker and Sue Binkley

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 257 Fred C. Davis

Introduction ...... 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 xv

Adaptive Daily Strategies in Behavior 275 CONTENTS Serge Daan

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 291 The Anticipation of Periodic Food 293 The Strategy of Habits ...... 294 References ...... 296

CHAPTER 16

Clock-Controlled Orientation in Space ...... 299 Hans C. WallrafJ

Introduction...... 299 Biological Clocks in Astro-Orientation .. 299 The Sun as an Orientational Cue ...... 300 The Moon as an Orientational Cue .. 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 . 311 Jiirgen AschofJ and Riitger Wever

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. 327 References ...... 329 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 XVll

Circannual Systems ...... 391 CONTENTS 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 ...... 408

CHAPTER 22

Insect Photoperiodism ...... 411 D. S. Saunders

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 XV111 CHAPTER 23

CONTENTS Photoperiodism in Vertebrates ...... 449 Klaus Hoffmann

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

PART IV RHYTHMS NOT DIRECTLY RELATED TO ENVIRONMENTAL CYCLES

CHAPTER 25

Short-Term Rhythms in Activity...... 491 Serge Daan and Jiirgen Aschoff Causal Considerations...... 492 Functional Considerations ...... 495 References ...... 497 CHAPTER 26 XIX

Temporal Characteristics of Sleep ...... 499 CONTENTS Wilse B. Webb and Michael G. Dube

Introduction...... 499 A Background of Sleep and Other Biological Rhythms ...... 499 Sleep as a Biological Rhythm ...... 501 Dimensions of Sleep ...... 501 Temporal Characteristics of Human Sleep ...... 501 Comparative Aspects ...... 502 Ontogenetic Aspects...... 506 Time Schedules of Sleep and Wakefulness ...... 508 Ultradian Rhythms and Sleep ...... 510 Ultradian Rhythms within Sleep ...... 510 Ultradian Sleep Rhythms and Wakefulness ...... 512 Sleep and Hormonal Rhythms ...... 513 The Central Nervous System and Sleep Rhythms ...... 515 References ...... 517

CHAPTER 27

Cyclic Function of the Mammalian Ovary 523 Constance S. Campbell and Fred W. Turek

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