Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep
Introduction
Animals spend their lives in two apparently mutually exclusive states, wakefulness and sleep. Wakefulness enables animals to adaptively interact with their environment, while sleep serves a vital [1], yet unknown function [2]. Sleep necessarily occurs at the expense of wakefulness, yet adaptive waking performance is contingent upon sleep [3]. Thus, animals face a situation in which sleep and wakefulness are inevitably in conflict. However, several animals have essentially side-stepped this problem by simultaneously engaging in both wakefulness and sleep; one cerebral hemisphere sleeps while the other remains awake, a unique state known as unihemispheric sleep.
The following review is intended to serve as a comprehensive synopsis on unihemispheric sleep. While significant reviews exist on unihemispheric sleep in aquatic mammals [4], [5], [6], no single source has incorporated the diverse and often obscure literature on unihemispheric sleep in other animals. Moreover, in the past few years a renewed interest in unihemispheric sleep has resulted in several significant findings that warrant discussion within the context of previous work on unihemispheric sleep. In the interest of providing the reader with an exhaustive review of the subject, we have incorporated virtually every study on unihemispheric sleep, including descriptive studies based on small sample sizes. Although conclusions based on such studies are necessarily tentative, their inclusion simultaneously highlights the breadth and limits of our understanding of unihemispheric sleep. Finally, throughout the review we present several speculative perspectives on unihemispheric sleep. In doing so, we hope to provide the impetus for developing further research and insight into unihemispheric sleep, and sleep in general.
We will discuss unihemispheric sleep at various levels throughout this review. The background, behavioral ecology and evolutionary history of unihemispheric sleep will be discussed for each taxonomic group in which sleep occurs unihemispherically; aquatic mammals (i.e. Cetacea, Pinnipedia and Sirenia), birds, and possibly reptiles. When appropriate, significant parallels and differences between groups will be highlighted. For organizational and historic reasons, much of the review will follow the chronological sequence in which discoveries were made. Following a discussion of each group, we will review the potential neurophysiological mechanisms involved in unihemispheric sleep, including a discussion regarding why only one type of sleep (i.e. slow-wave sleep, SWS) occurs unihemispherically. Although humans do not sleep unihemispherically, several related findings that hint at a tendency for unihemispheric sleep in humans will also be included. Throughout the review, promising areas for future research will be identified, especially those which may yield clues to the function of sleep. Finally, having demonstrated the adaptive advantages of being able to sleep unihemispherically, we will attempt to answer the more difficult, and rarely asked question: Why do most mammals sleep bihemispherically?
Section snippets
What is unihemispheric sleep?
A definition of unihemispheric sleep is necessarily contingent upon a definition of sleep itself. Sleep can be distinguished from wakefulness using both behavioral and physiological criteria. Behaviorally, sleep is characterized as a period of sustained quiescence in a species-specific posture or site, with reduced responsiveness to external stimulation. However, with sufficient stimulation sleeping animals rapidly return to wakefulness [7], [8]. In mammals and birds, behavioral sleep is
Cetaceans: dolphins, porpoises and whales
The order Cetacea is comprised of two suborders of exclusively aquatic mammals, Odontoceti (dolphins, porpoises and toothed whales) and Mysticeti (filter-feeding baleen whales) [23] (but see Ref. [24]). Based on fossil [25], [26] and molecular [24], [27] evidence, the closest living relatives to Cetaceans are the even-toed ungulates (Artiodactyla). Interestingly, within Artiodactyla, Cetaceans appear most closely related to the semi-aquatic hippopotamuses [28]. To date, USWS has been identified
Background of avian unihemispheric sleep
And smale fowles … slepen al the night with open yë Chaucer (1386).
In the prologue to Chaucer's, The Canterbury Tales, birds are observed sleeping with an open eye. Nearly 600 years later, scientists revealed that this observation was not just a tale. Spooner [97] was the first to demonstrate an association between unilateral eye closure and USWS in birds. During EEG studies of young chickens (Gallus gallus domesticus), Spooner observed periods of unilateral eye closure associated with an
Reptiles
Despite displaying unequivocal behavioral signs of sleep, several conflicting electrophysiological correlates of behavioral sleep have been reported in reptiles (reviewed in Ref. [140]). Most studies report an association between behavioral sleep and intermittent high-amplitude, spikes and sharp waves in the EEG. However, a few studies report an association between behavioral sleep and high-amplitude, low-frequency activity, e.g. [141]. Complicating matters further are studies that failed to
Neurophysiological mechanisms of unihemispheric sleep
The neuroanatomical structures and neurophysiological processes responsible for USWS remain largely unknown. An understanding of the potential mechanisms behind USWS is contingent upon an understanding of sleep mechanisms in general. Since only SWS occurs unihemispherically, we will focus on those mechanisms involved in the alternation between SWS and wakefulness. Although virtually all of the research into sleep mechanisms is derived from mammals, several of these mechanisms probably also
Unihemispheric REM sleep?
Sleep in mammals and birds is composed of two distinct states, SWS and REM sleep, yet only SWS is known to occur unihemispherically. This raises the question as to why unihemispheric REM sleep has not been observed. Actually, the issue of unihemispheric REM sleep encompasses two questions: (1) why does REM sleep not occur unihemispherically with SWS in the other hemisphere; and (2) why does REM sleep not occur unihemispherically with wakefulness in the other hemisphere. Noting the similarity in
Human unihemispheric sleep?
Humans are not known to sleep unihemispherically. Even following transsection of the corpus callosum, or in humans lacking a callosum, sleep is invariably bihemispheric. Yet, certain studies, which have found interhemispheric asymmetries during BSWS in humans, seem to warrant discussion within the context of USWS. First, in a study of interhemispheric EEG asymmetry, Armitage et al. [190] found greater asymmetry in theta and delta activity during SWS (i.e. human stage 4 sleep) when compared to
Why do most mammals sleep bihemispherically?
Given the utility of sleeping unihemispherically, it is surprising that most mammals sleep bihemispherically. Sleep has been investigated in several of the major groups of mammals [18], [21], [205], [206], yet only aquatic mammals are known to sleep unihemispherically. The restricted occurrence of USWS in mammals becomes even more intriguing if the reptilian ancestors to mammals slept unihemispherically. Although the results from modern reptiles clearly remain equivocal with respect to USWS,
Conclusions
(1) A largely unexplored area in behavioral ecology is the inherent conflict between sleep and wakefulness. Wakefulness is clearly an adaptive state that allows animals to interact with their environment, yet its efficacy is contingent upon sleep, a vulnerable state of reduced responsiveness. The evolution of unihemispheric sleep exemplifies this point and serves as a unique solution to the problem. Although mammals and birds exhibit two types of sleep (i.e. SWS and REM sleep), only SWS occurs
Acknowledgements
We would like to thank the following people for their valuable comments on earlier drafts of this manuscript: Ruth Benca, Oleg Lyamin, Paul Manger, Chris Mathews and Chris Sinton. We also thank Oleg Lyamin, Paul Manger and Chris Sinton for their willingness to share several pieces of unpublished data that greatly enhanced the manuscript. Finally we thank the reviewers for their helpful comments.
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