ReviewCetacean sleep: An unusual form of mammalian sleep
Introduction
That sleep is an essential part of the life of animals is well known; indeed, it has been demonstrated that under some conditions lack of sleep is fatal (Rechtschaffen et al., 1983, Shaw et al., 2002). Despite this, the answer to the function of sleep, at its most basic level, has not been discovered, i.e. we cannot yet say why animals need to sleep. Sleep, or sleep-like, behavior has been observed and measured in many animal species, both vertebrate and invertebrate, but the exact phylogenetic boundaries defining the occurrence of sleep, and types of sleep, have not yet been determined. In the class Mammalia, all studies directed towards observing sleep have found it, in varying amounts and with different sleep topographies, e.g. some mammals have more rapid eye movement (REM) sleep than others (e.g. Zepelin et al., 2005, Siegel et al., 1999). The studies of sleep amongst various mammalian species have yet to reveal any specific or definitive links related to phylogeny, phenotype, life history, or environment; however, it has been seen that immaturity at birth is related to increased amounts of REM sleep, and that larger body size is related to a lower total sleep time in land mammals (e.g. Zepelin et al., 2005, Siegel, 2003, Siegel, 2005, Lesku et al., 2006), but these trends are not strongly predictive.
The present review focuses on the study of sleep in cetaceans, a group of mammals that, arguably, face an unusual, or even extreme, environment in which mammalian sleep must occur. Studies of cetacean sleep have led to one of the most unusual findings to date in respect of sleep in mammals, this being the unihemispheric nature of slow waves (Mukhametov, 1987, Mukhametov et al., 1977, Mukhametov and Polyakova, 1981, Ridgway, 2002, Lyamin et al., 2004), i.e. cetaceans have the slow waves in one half of their brain at a time, while the other half of the brain has low voltage activity. This asymmetrical EEG state occurs in all cetaceans studied to date, with each half of the brain exhibiting approximately 4 h of SWS per day in the bottlenose dolphin, Tursiops truncatus (the most intensively studied species). Added to this unusually lateralized sleep pattern has been the lack of finding of any distinct form of REM sleep in the Cetacea (Mukhametov, 1988, Mukhametov, 1995), i.e. the polygraphic signs of REM sleep, if it exists, are rare or unclear. These findings have made the study of sleep in whales and dolphins one of the most interesting topics in terms of the life history of cetaceans and more generally for mammalian sleep evolution.
In the present review we outline the history of the discovery of lateralized SWS in cetaceans, examining the hints derived from early behavioral observations through to the definitive polygraphic recordings of sleep. We then detail what has been found in these and several more recent studies of cetacean sleep to build as complete a picture as possible of cetacean sleep phenomenology. Following this we compare what is known about the anatomy and physiology of the somnogenic system from representative mammals (mostly rats, cats, monkeys and humans) with what is known in cetaceans, highlighting areas where our knowledge in cetaceans is deficient and areas of interest for future studies. Finally, we examine the various hypotheses forwarded regarding the evolution of cetacean sleep phenomenology, and attempt to define what selection pressures may have been contributing or underlying factors in the positive evolutionary selection of this phenotypically unusual form of mammalian sleep.
Section snippets
Lilly's predictions
John Lilly, who pioneered early experimental physiological studies of dolphins, proposed several theories regarding dolphin physiology, including specific proposals regarding sleep in the dolphin, and in doing so generated many novel ideas (Lilly, 1964). Lilly proposed that respiration in dolphins was controlled at the thalamo-cortical level of the CNS rather than the respiratory centers located in the medulla and at the pontomedullary junction, surmising that dolphins and porpoises “lack our
Behavioral and physiological aspects of cetacean sleep
Several observational studies of dolphins have attempted to describe aspects of what was assumed to be sleep (Lilly, 1964, McCormick, 1969, McCormick, 2007, Flanigan, 1974a, Flanigan, 1974b, Flanigan, 1975a, Flanigan, 1975b, Flanigan, 1975c, Mukhametov and Lyamin, 1997, Goley, 1999, Gnone et al., 2001, Sekiguchi and Kohshima, 2003). All the available descriptions of resting behavior of bottlenose dolphins in the wild are primarily anecdotal (e.g. Klinowska, 1986, Shane et al., 1986, Hanson and
Neuronal groups involved in the control of the sleep–wake cycle
Within the mammalian brain there are several neuronal groups that have been implicated in the control of the sleep–wake cycle, and many of these have been identified anatomically such that they can be recognized with immunohistochemical stains. These neuronal groups are found in two broad regions, the first comprising those neurons in the basal forebrain and hypothalamus, the second comprising those groups located in a cluster at the ponto-medullary junction of the brainstem. Many of these
Evolution of cetacean sleep phenomenology
As described above, cetacean sleep is characterized by unihemispheric slow wave sleep, alternating in approximately 1-h intervals between hemispheres, a very small amount (or complete lack) of REM sleep, the ability to sleep during swimming and with only one eye closed at a time. Even though large cetaceans (both odontocetes and mysticetes) spend a lot of time sleeping while immobile at the surface or under water, it is very likely that all representatives of the order (large and small) have
Summary and conclusions
We hypothesize that three factors – the need to come to the surface to breathe, more efficient monitoring of the environment and thermogenesis – may have been important in the evolution of the observable cetacean sleep phenomenology (sleeping while in motion, USWS, absence of REM sleep, and sleeping with one eye open). The need to come to the surface to breathe is an obvious life-sustaining requirement for any aquatic mammal. This need might make the physiological process of breathing more
Acknowledgments
The work presented here was supported by the National Science Foundation (NSF-0234687), National Institute of Health (NS 42947), the Medical Research Service of the Department of Veterans Affairs, Utrish Dolphinarium Ltd. and the South African National Research Foundation.
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