Brain-Behavior Adaptations to Sleep Loss in the Nocturnally Migrating Swainson’S Thrush (Catharus Ustulatus)

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Brain-Behavior Adaptations to Sleep Loss in the Nocturnally Migrating Swainson’S Thrush (Catharus Ustulatus) BRAIN-BEHAVIOR ADAPTATIONS TO SLEEP LOSS IN THE NOCTURNALLY MIGRATING SWAINSON’S THRUSH (CATHARUS USTULATUS) Thomas Fuchs A Dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY August 2006 Committee: Verner P. Bingman, Advisor Donald S. Cooper Graduate Faculty Representative Kevin Pang Dale Klopfer Patricia Sharp © 2006 Thomas Fuchs All Rights Reserved iii ABSTRACT Verner P. Bingman, Advisor Many typically diurnal songbirds experience dramatic sleep loss during the migratory seasons because of their nocturnal flights. However, nocturnally migrating songbirds continue to function normally with no observable effect of sleep loss on their behavior. To mitigate the effects of sleep loss, nocturnal migrants may engage in daytime sleep, unihemispheric sleep, sleep during migratory flight, or increased quality of what sleep is available. Studying the Swainson’s thrush, a long-distance trans-gulf migrant, I investigated how avian migrants might compensate for sleep loss during the migratory season. Daytime behavior, nighttime behavior and forebrain EEG activity was recorded in thrushes when migratory and non-migratory. Behavioral sleeping postures and their EEG/brain correlates were identified throughout the 24 h light-dark cycle. Slow wave sleep (SWS) and rapid eye movement (REM) sleep were investigated, and the temporal profile of the two sleep states was analyzed. Brain activity (EEG power) in the delta frequency band (1.5 – 4Hz) was employed as a measure of sleep quality. Interestingly, the most prominent alterations in sleep and sleep-related behavior in nocturnally active migratory thrushes were found during the day. In contrast to their behavior when non-migratory, migratory Swainson’s thrushes engaged in numerous episodes of daytime sleep, unilateral eye closure, and an intermediate sleep-like state referred to as drowsiness. The electrophysiological recordings demonstrated that the observed behavior was accompanied by reliable sleep like changes in brain activity. In addition, EEG activity during episodes of unilateral iv eye closure was frequently accompanied byinterhemispheric asymmetries characteristic of unihemispheric sleep. The relatively brief but frequent daytime sleep states (“micro naps”) may represent an adaptive balance that enables migratory birds to compensate for extended periods of nocturnal sleep loss during the subsequent day without rendering them entirely vulnerable to environmental challenges like predation and the need to feed and store energy. Our findings also offer the intriguing possibility that avian migrants partially compensate for nocturnal sleep loss by taking lateralized naps during the day. Non-migratory Swainson’s thrushes exhibit a marked decrease in delta power during the night indicating a parallel decline in sleep quality. Decreasing SWS pressure, possibly in concert with a circadian REM sleep regulating mechanism, may explain increasing amounts of REM sleep during the latter part of the night. Evidence for compensatory changes in nighttime sleep in migratory thrushes is presented. The present work suggests that birds, like mammals, require a minimum amount of sleep. The finding that a nocturnal migrant, a species highly adapted to its migratory life style, requires compensatory sleep, strongly suggests that a basic need for sleep is shared by many if not all avian species. Furthermore, the observed sleep characteristics indicate that some aspects of avian and mammalian sleep are similarly regulated. Avian sleep, therefore, may provide further insight into processes involved in the regulation of sleep and resting states that likely generalize to many species, vertebrates and invertebrates alike. v ACKNOWLEDGMENTS I would like to express my deepest appreciation to Herr Bingman, my dissertation advisor, for guiding me through the process of conducting and writing this dissertation, and also for providing me with an opportunity to do what cannot be done easily these days (comparative sleep research). My sincere gratitude also goes to Drs Pat Sharp, Kevin Pang, Dale Klopfer and Donald Cooper, my dissertation committee, for offering invaluable advice and having a lot of patience with my rather erratic time schedule. I am also indebted to the J. P. Scott Center for Neurosience Brain and Behavior for awarding me a research fellowship during the last year of this project that allowed me to finally get my act together. Finally, I would like to thank my family and newly wed wife Ako for putting up with me during theses last stressful weeks. vi TABLE OF CONTENTS Page INTRODUCTION .... ....................................................................................................... 1 PART I: BEHAVIOR....................................................................................................... 7 Methods ....................................................................................................... 7 Results ....................................................................................................... 12 Discussion ....................................................................................................... 21 PART II: EEG RECORDINGS ......................................................................................... 25 General EEG Methods .......................................................................................... 25 Analysis ....................................................................................................... 28 Slow Wave Sleep and REM Sleep ......................................................................... 29 Slow Wave Sleep ....................................................................................... 29 REM Sleep................................................................................................. 31 Daytime Recordings .............................................................................................. 32 Analysis .................................................................................................... 32 Results ....................................................................................................... 36 Discussion ................................................................................................. 44 Nighttime Recordings............................................................................................ 47 Analysis .................................................................................................... 47 Results ....................................................................................................... 52 Non-migratory thrushes ................................................................ 52 Nighttime Sleep during the Migratory Season ................................ 64 Discussion.................................................................................................. 67 vii GENERAL DISCUSSION................................................................................................ 75 Daytime Sleep ....................................................................................................... 76 Unilateral Eye Closure........................................................................................... 78 Drowsiness ....................................................................................................... 81 Some Ecological Considerations............................................................................ 84 Comparative Aspects............................................................................................. 88 CONCLUSION ....................................................................................................... 95 APPENDIX I: Mammalian Neocortex and the Avian Wulst Formation (Hyperpallium): Similarities and Differences .............................................................................................. 98 APPENDIX II: Sleep in Invertebrates, Fish, Amphibians and Reptiles .............................. 102 Defining Sleep....................................................................................................... 102 Invertebrates ....................................................................................................... 104 Fish ....................................................................................................... 106 Amphibians ... ....................................................................................................... 107 Reptiles ....................................................................................................... 108 APPENDIX III: Neurophysiology of mammalian REM Sleep and Non-REM Sleep. Comparative Aspects ....................................................................................................... 112 Mammalian Non-REM Sleep................................................................................. 114 Comparing Mammalian and Avian Non-REM sleep .............................................. 118 Mammalian REM sleep ......................................................................................... 123 Avian REM sleep .................................................................................................. 126 Conclusions ....................................................................................................... 128 APPENDIX IV: REPLICATION IN THE HISTORY OF PSYCHOLOGY: PATRICK & GILBERT (1896)
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