Our knowledge of the form of lateralized sleep behavior, known as unihemispheric slow wave sleep (USWS), seen in all members of the order Cetacea examined to date, is described. We trace the discovery of this phenotypically unusual form of mammalian sleep and highlight specific aspects that are different from sleep in terrestrial mammals. We find that for cetaceans sleep is characterized by USWS, a negligible amount or complete absence of rapid eye movement (REM) sleep, and a varying degree of movement during sleep associated with body size, and an asymmetrical eye state. We then compare the anatomy of the mammalian somnogenic system with what is known in cetaceans, highlighting areas where additional knowledge is needed to understand cetacean sleep. Three suggested functions of USWS (facilitation of movement, more efficient sensory processing and control of breathing) are discussed. Lastly, the possible selection pressures leading to this form of sleep are examined, leading us to the suggestion that the selection pressure necessitating the evolution of cetacean sleep was most likely the need to offset heat loss to the water from birth and throughout life. Aspects such as sentinel functions and breathing are likely to be proximate evolutionary phenomenon of this form of sleep.
All mammals previously studied take maximal rest or sleep after birth, with the amount gradually decreasing as they grow to adulthood, and adult fruitflies and rats die if they are forcibly deprived of sleep. It has therefore been assumed that sleep is necessary for development and serves a vital function in adults. But we show here that, unlike terrestrial mammals, killer-whale and bottlenose-dolphin neonates and their mothers show little or no typical sleep behaviour for the first postpartum month, avoiding obstacles and remaining mobile for 24 hours a day. We find that neonates and their mothers gradually increase the amount of time they spend resting to normal adult levels over a period of several months, but never exceed these levels. Our findings indicate either that sleep behaviour may not have the developmental and life-sustaining functions attributed to it, or that alternative mechanisms may have evolved in cetaceans.
The current study provides details of sleep (or inactivity) in two wild, free-roaming African elephant matriarchs studied in their natural habitat with remote monitoring using an actiwatch subcutaneously implanted in the trunk, a standard elephant collar equipped with a GPS system and gyroscope, and a portable weather station. We found that these two elephants were polyphasic sleepers, had an average daily total sleep time of 2 h, mostly between 02:00 and 06:00, and displayed the shortest daily sleep time of any mammal recorded to date. Moreover, these two elephants exhibited both standing and recumbent sleep, but only exhibited recumbent sleep every third or fourth day, potentially limiting their ability to enter REM sleep on a daily basis. In addition, we observed on five occasions that the elephants went without sleep for up to 46 h and traversed around 30 km in 10 h, possibly due to disturbances such as potential predation or poaching events, or a bull elephant in musth. They exhibited no form of sleep rebound following a night without sleep. Environmental conditions, especially ambient air temperature and relative humidity, analysed as wet-bulb globe temperature, reliably predict sleep onset and offset times. The elephants selected novel sleep sites each night and the amount of activity between sleep periods did not affect the amount of sleep. A number of similarities and differences to studies of elephant sleep in captivity are noted, and specific factors shaping sleep architecture in elephants, on various temporal scales, are discussed.
Virtually all land mammals and birds have two sleep states: slow-wave sleep (SWS) and rapid eye movement (REM) sleep [1, 2]. After deprivation of REM sleep by repeated awakenings, mammals increase REM sleep time [3], supporting the idea that REM sleep is homeostatically regulated. Some evidence suggests that periods of REM sleep deprivation for a week or more cause physiological dysfunction and eventual death [4, 5]. However, separating the effects of REM sleep loss from the stress of repeated awakening is difficult [2, 6]. The northern fur seal (Callorhinus ursinus) is a semiaquatic mammal [7]. It can sleep on land and in seawater. The fur seal is unique in showing both the bilateral SWS seen in most mammals and the asymmetric sleep previously reported in cetaceans [8]. Here we show that when the fur seal stays in seawater, where it spends most of its life [7], it goes without or greatly reduces REM sleep for days or weeks. After this nearly complete elimination of REM, it displays minimal or no REM rebound upon returning to baseline conditions. Our data are consistent with the hypothesis that REM sleep may serve to reverse the reduced brain temperature and metabolism effects of bilateral nonREM sleep, a state that is greatly reduced when the fur seal is in the seawater, rather than REM sleep being directly homeostatically regulated. This can explain the absence of REM sleep in the dolphin and other cetaceans and its increasing proportion as the end of the sleep period approaches in humans and other mammals.
SUMMARY The fur seal (Callorhinus ursinus), a member of the Pinniped family, displays a highly expressed electroencephalogram (EEG) asymmetry during slow wave sleep (SWS), which is comparable with the unihemispheric sleep in cetaceans. In this study, we investigated the EEG asymmetry in the fur seal using spectral analysis. Four young (2-3 years old) seals were implanted with EEG electrodes for polygraphic sleep recording.In each animal, EEG spectral power in the frequency range of 1.2-16 Hz was computed in symmetrical cortical recordings over two consecutive nights. The degree of EEG asymmetry was measured by using thewhere L and R are the spectral powers in the left and right hemispheres, respectively]. In fur seals, EEG asymmetry, as measured by the percent of 20-s epochs with absolute AI > 0.3 and >0.6, was expressed in the entire frequency range (1.2-16 Hz). The asymmetry was significantly greater during SWS (25.6-44.2% of all SWS epochs had an absolute AI > 0.3 and 2.1-12.2% of all epochs had AI > 0.6) than during quiet waking (11.0-20.3% and 0-1.9% of all waking epochs, respectively) and REM sleep (4.2-8.9% of all REM sleep epochs and no epochs, respectively). EEG asymmetry was recorded during both low-and high-voltage SWS, and was maximal in the range of 1.2-4 and 12-16 Hz. As shown in this study, the degree of EEG asymmetry and the frequency range in which it is expressed during SWS in fur seals are profoundly different from those of terrestrial mammals and birds.
Fur seals are unique in that they display both bilateral slow-wave sleep (BSWS), as seen in all terrestrial mammals, and slow-wave sleep with interhemispheric electroencephalogram (EEG) asymmetry, resembling the unihemispheric slow waves of cetaceans. Little is known about the underlying mechanisms of this phenomenon, which is also termed asymmetrical slow wave sleep (ASWS). However, we may begin to understand the expression of ASWS by studying the neurotransmitter systems thought to be involved in the generation and maintenance of sleep-wake states in terrestrial mammals. We examined bilaterally the release of cortical acetylcholine (ACh), a neurotransmitter implicated in the regulation of cortical EEG and behavioral arousal, across the sleep-wake cycle in four juvenile northern fur seals (Callorhinus ursinus). In vivo microdialysis and high-performance liquid chromatography coupled with electrochemical detection were used to measure cortical ACh levels during polygraphically defined behavioral states. Cortical ACh release was state-dependent, showing maximal release during active waking (AW), similar levels during quiet waking (QW), and rapid eye movement (REM) sleep, and minimal release during BSWS. When compared with BSWS, cortical ACh levels increased ϳ300% during AW, and ϳ200% during QW and REM sleep. During these bilaterally symmetrical EEG states, ACh was synchronously released from both hemispheres. However, during ASWS, ACh release was lateralized with greater release in the hemisphere displaying lower voltage activity, at levels approximating those seen in QW. These findings demonstrate that cortical ACh release is tightly linked to hemispheric EEG activation.
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