Sleep: Giving it up to get it on.

A new study presents evidence of sex-related sleep reduction in males of two marsupial mice species but not in females. The growing experimental data suggest that seasonal sleep reduction, linked to migrations and reproductive periods, is common among animals.

A 108-h total sleep deprivation did not impair fur seal performance in delayed matching to sample task.

While the majority of studies have concluded that sleep deprivation causes detrimental effects on various cognitive processes, some studies reported conflicting results. We examined the effects of a 108-h total sleep deprivation (TSD) on working memory in the northern fur seal, an animal with unusual sleep phenomenology and long-range annual migrations. The performance of fur seals was evaluated in a two-choice visual delayed matching to sample (DMTS) task, which is commonly used to evaluate working memory. In baseline conditions, the performance of fur seals in a DMTS task based on the percentage of errors was somewhat comparable with that in nonhuman primates at similar delays. We have determined that a 108-h TSD did not affect fur seals' performance in a visual DMTS task as measured by overall percentage of errors and response latencies. On the contrary, all fur seals improved task performance over the study, including the baseline, TSD and recovery conditions. In addition, TSD did not change the direction and strength of the pattern of behavioral lateralization in fur seals. We conclude that a 108-h TSD did not interfere with working memory in a DMTS test in northern fur seals.

Brain activity of diving seals reveals short sleep cycles at depth.

Sleep is a crucial part of the daily activity patterns of mammals. However, in marine species that spend months or entire lifetimes at sea, the location, timing, and duration of sleep may be constrained. To understand how marine mammals satisfy their daily sleep requirements while at sea, we monitored electroencephalographic activity in wild northern elephant seals (Mirounga angustirostris) diving in Monterey Bay, California. Brain-wave patterns showed that seals took short (less than 20 minutes) naps while diving (maximum depth 377 meters; 104 sleeping dives). Linking these patterns to accelerometry and the time-depth profiles of 334 free-ranging seals (514,406 sleeping dives) revealed a North Pacific sleepscape in which seals averaged only 2 hours of sleep per day for 7 months, rivaling the record for the least sleep among all mammals, which is currently held by the African elephant (about 2 hours per day).

Sleep in the lesser mouse-deer (Tragulus kanchil).

The mouse-deer or chevrotains are the smallest of the ungulates and ruminants. They are characterized by a number of traits which are considered plesiomorphic for the Artiodactyla order. The objective of this study was to examine sleep in the lesser mouse-deer (Tragulus kanchil), which is the smallest in this group (body mass < 2.2 kg). Electroencephalogram, nuchal electromyogram, electrooculogram, and body acceleration were recorded in four adult mouse-deer females using a telemetry system in Bu Gia Map National Park in Vietnam. The mouse-deer spent on average 49.7 ± 3.0% of 24 h in non-rapid eye movement (NREM) sleep. REM sleep occupied 1.7 ± 0.3% of 24 h or 3.2 ± 0.5% of total sleep time. The average duration of REM sleep episodes was 2.0 ± 0.2 min, the average maximum was 5.1 ± 1.1 min, and the longest episodes lasted 8 min. NREM sleep occurred in sternal recumbency with the head held above the ground while 64.7 ± 6.4% of REM sleep occurred with the head resting on the ground. The eyes were open throughout most of the NREM sleep period. The mouse-deer displayed polyphasic sleep and crepuscular peaks in activity (04:00-06:00 and 18:00-19:00). The largest amounts of NREM occurred in the morning (06:00-09:00) and the smallest before dusk (at 04:00-06:00). REM sleep occurred throughout most of the daylight hours (08:00-16:00) and in the first half of the night (19:00-02:00). We suggest that the pattern and timing of sleep in the lesser mouse-deer is adapted to the survival of a small herbivorous animal, subject to predation, living in high environmental temperatures in the tropical forest undergrowth.

Sleep in ostrich chicks (Struthio camelus).

It has been reported that adult ostriches displayed the longest episodes of rapid eye movement (REM) sleep (up to 5 min) and more REM sleep (24% of the nighttime) than any other bird species. If the mammalian ontogenetic trend exists in the ostrich, then the amounts of REM and the duration of sleep episodes in young ostriches may be greater than those reported in adults. We investigated sleep in 1.5-3.5 month old ostrich chicks. Recordings were conducted during nighttime (20:00-08:00), the main sleep period in ostriches, which are diurnal. The polygrams were scored in 4-s epochs for waking, non-rapid eye movement (NREM) sleep and REM sleep, as in other bird studies. REM sleep in ostrich chicks occurred during both cortical EEG activation and during slow waves, as was described in adult ostriches. The chicks spent 69.3% ± 1.5% of the night in NREM sleep. REM sleep occupied 14.1% ± 1.8% of the night or 16.8% ± 2.0% of nighttime sleep. Episodes of REM sleep lasted on average 10 ± 1 s and ranged between 4 and 40 s. Therefore, the total amount and duration of REM sleep episodes in ostrich chicks were substantially smaller than reported in adult ostriches while the amounts of NREM sleep did not greatly differ. The developmental profile of REM sleep ontogenesis in the ostrich may be remarkably different from what has been reported in all studied mammals and birds.

Eye state asymmetry during aquatic unihemispheric slow wave sleep in northern fur seals (Callorhinus ursinus).

Unihemispheric slow wave sleep (USWS) is a unique form of sleep in which one brain hemisphere maintains low voltage electrical activity indicative of waking while the opposite exhibits slow wave electrical activity indicative of sleep. USWS is present in several marine mammals and in some species of birds. One proposed biological function of USWS is to enable the animal to monitor the environment to detect predators or conspecifics. While asymmetrical eye state was often observed during behavioral sleep in birds and marine mammals, electrophysiological (electroencephalogram, EEG) correlates between the asymmetry of eye state and EEG of two cortical hemispheres have not been reliably established. This study examined the association between eye state and EEG activity during aquatic sleep in two subadult northern fur seals (Callorhinus ursinus), taking advantage of the simultaneous visibility of both eyes when the seals were in the prone position. We found that during USWS the eye contralateral to the sleeping hemisphere was closed on average 99.4±0.1% of the recording time. The eye contralateral to the waking hemisphere opened briefly for on average 1.9±0.1 sec with a rate of 8.2±1.0 per min. This eye was open on average 24.8±2.5% of the USWS time and it was closed no longer than 3 sec, on average 39.4±5.6% of the time. These data indicate that fur seals sleep in seawater by having intermittent visual monitoring. Our findings document the extent of visual monitoring of both eyes during USWS and support the idea that USWS allows intermittent visual vigilance. Thus, USWS serves two functions in the fur seal, facilitating movement and visual vigilance, which may also be the case in cetaceans.

Fur Seals Suppress REM Sleep for Very Long Periods without Subsequent Rebound.

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.

Sociality Affects REM Sleep Episode Duration Under Controlled Laboratory Conditions in the Rock Hyrax, Procavia capensis.

The rock hyrax, Procavia capensis, is a highly social, diurnal mammal. In the current study several physiologically measurable parameters of sleep, as well as the accompanying behavior, were recorded continuously from five rock hyraxes, for 72 h under solitary (experimental animal alone in the recording chamber), and social conditions (experimental animal with 1 or 2 additional, non-implanted animals in the recording chamber). The results revealed no significant differences between solitary and social conditions for total sleep times, number of episodes, episode duration or slow wave activity (SWA) for all states examined. The only significant difference observed between social and solitary conditions was the average duration of rapid eye movement (REM) sleep episodes. REM sleep episode duration was on average 20 s and 40 s longer under social conditions daily and during the dark period, respectively. It is hypothesized that the increase in REM sleep episode duration under social conditions could possibly be attributed to improved thermoregulation strategies, however considering the limited sample size and design of the current study further investigations are needed to confirm this finding. Whether the conclusions and the observations made in this study can be generalized to all naturally socially sleeping mammals remains an open question.

Sleep in the northern fur seal.

The pattern of sleep in the fur seal, a semiaquatic pinniped, has several striking behavioral and physiological adaptations that allow this species to inhabit both the land and water environment. These features include unihemispheric slow wave sleep (USWS, also being unihemispheric waking), the ability to maintain movement for stabilization of the sleep posture and to briefly open one eye while having a sleep electroencephalogram (EEG) in one hemisphere. In vivo microdialysis studies suggest that acetylcholine release is required for cortical activation during USWS, and that monoamines are not required for USWS. The need to breathe, to maintain efficient thermoregulation, and to avoid predation have shaped the sleep patterns in semiaquatic fur seals as in fully aquatic cetaceans.

Inactivity/sleep in two wild free-roaming African elephant matriarchs - Does large body size make elephants the shortest mammalian sleepers?

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.

Monoamine Release during Unihemispheric Sleep and Unihemispheric Waking in the Fur Seal.

STUDY OBJECTIVES: Our understanding of the role of neurotransmitters in the control of the electroencephalogram (EEG) has been entirely based on studies of animals with bilateral sleep. The study of animals with unihemispheric sleep presents the opportunity of separating the neurochemical substrates of waking and sleep EEG from the systemic, bilateral correlates of sleep and waking states. METHODS: The release of histamine (HI), norepinephrine (NE), and serotonin (5HT) in cortical and subcortical areas (hypothalamus, thalamus and caudate nucleus) was measured in unrestrained northern fur seals (Callorhinus ursinus) using in vivo microdialysis, in combination with, polygraphic recording of EEG, electrooculogram, and neck electromyogram. RESULTS: The pattern of cortical and subcortical HI, NE, and 5HT release in fur seals is similar during bilaterally symmetrical states: highest in active waking, reduced in quiet waking and bilateral slow wave sleep, and lowest in rapid eye movement (REM) sleep. Cortical and subcortical HI, NE, and 5HT release in seals is highly elevated during certain waking stimuli and behaviors, such as being sprayed with water and feeding. However, in contrast to acetylcholine (ACh), which we have previously studied, the release of HI, NE, and 5HT during unihemispheric sleep is not lateralized in the fur seal. CONCLUSIONS: Among the studied neurotransmitters most strongly implicated in waking control, only ACh release is asymmetric in unihemispheric sleep and waking, being greatly increased on the activated side of the brain. COMMENTARY: A commentary on this article appears in this issue on page 491.

Cardiorespiratory Responses to Acoustic Noise in Belugas.

To date, most research on the adverse effects of anthropogenic noise on marine mammals has focused on auditory and behavioral responses. Other responses have received little attention and are often ignored. In this study, the effect of acoustic noise on heart rate was examined in captive belugas. The data suggest that (1) heart rate can be used as a measure of physiological response (including stress) to noise in belugas and other cetaceans, (2) cardiac response is influenced by parameters of noise and adaptation to repeated exposure, and (3) cetacean calves are more vulnerable to the adverse effect of noise than adults.

Symmetrical serotonin release during asymmetrical slow-wave sleep: implications for the neurochemistry of sleep-waking states.

On land, fur seals predominately display bilaterally synchronized electroencephalogram (EEG) activity during slow-wave sleep (SWS), similar to that observed in all terrestrial mammals. In water, however, fur seals exhibit asymmetric slow-wave sleep (ASWS), resembling the unihemispheric slow-wave sleep of odontocetes (toothed whales). The unique sleeping pattern of fur seals allows us to distinguish neuronal mechanisms mediating EEG changes from those mediating behavioral quiescence. In a prior study we found that cortical acetylcholine release is lateralized during ASWS in the northern fur seal, with greater release in the hemisphere displaying low-voltage (waking) EEG activity, linking acetylcholine release to hemispheric EEG activation (Lapierre et al. 2007). In contrast to acetylcholine, we now report that cortical serotonin release is not lateralized during ASWS. Our data demonstrate that bilaterally symmetric levels of serotonin are compatible with interhemispheric EEG asymmetry in the fur seal. We also find greatly elevated levels during eating and hosing the animals with water, suggesting that serotonin is more closely linked to bilateral variables, such as axial motor and autonomic control, than to the lateralized cortical activation manifested in asymmetrical sleep.

Regional differences in cortical electroencephalogram (EEG) slow wave activity and interhemispheric EEG asymmetry in the fur seal.

Slow wave sleep (SWS) in the northern fur seal (Callorhinus ursinus) is characterized by a highly expressed interhemispheric electroencephalogram (EEG) asymmetry, called 'unihemispheric' or 'asymmetrical' SWS. The aim of this study was to examine the regional differences in slow wave activity (SWA; power in the range of 1.2-4.0 Hz) within one hemisphere and differences in the degree of interhemispheric EEG asymmetry within this species. Three seals were implanted with 10 EEG electrodes, positioned bilaterally (five in each hemisphere) over the frontal, occipital and parietal cortex. The expression of interhemispheric SWA asymmetry between symmetrical monopolar recordings was estimated based on the asymmetry index [AI = (L-R)/(L+R), where L and R are the power in the left and right hemispheres, respectively]. Our findings indicate an anterior-posterior gradient in SWA during asymmetrical SWS in fur seals, which is opposite to that described for other mammals, including humans, with a larger SWA recorded in the parietal and occipital cortex. Interhemispheric EEG asymmetry in fur seals was recorded across the entire dorsal cerebral cortex, including sensory (visual and somatosensory), motor and associative (parietal or suprasylvian) cortical areas. The expression of asymmetry was greatest in occipital-lateral and parietal derivations and smallest in frontal-medial derivations. Regardless of regional differences in SWA, the majority (90%) of SWS episodes with interhemispheric EEG asymmetry meet the criteria for 'unihemispheric SWS' (one hemisphere is asleep while the other is awake). The remaining episodes can be described as episodes of bilateral SWS with a local activation in one cerebral hemisphere.

Sleep in the rock hyrax, Procavia capensis.

We investigated sleep in therock hyrax, Procavia capensis, a social mammal that typically lives in colonies on rocky outcrops throughout most parts of Southern Africa. The sleep of 5 wild-captured, adult rock hyraxes was recorded continuously for 72 h using telemetric relay of signals and allowing unimpeded movement. In addition to waking, slow wave sleep (SWS) and an unambiguous rapid eye movement (REM) state, a sleep state termed somnus innominatus (SI), characterized by low-voltage, high-frequency electroencephalogram, an electromyogram that stayed at the same amplitude as the preceding SWS episode and a mostly regular heart rate, were identified. If SI can be considered a form of low-voltage non-REM, the implication would be that the rock hyrax exhibits the lowest amount of REM recorded for any terrestrial mammal studied to date. Conversely, if SI is a form of REM sleep, it would lead to the classification of a novel subdivision of this state; however, further investigation would be required. The hyraxes spent on average 15.89 h (66.2%) of the time awake, 6.02 h (25.1%) in SWS, 43 min (3%) in SI and 6 min (0.4%) in REM. The unambiguous REM sleep amounts were on average less than 6 min/day. The most common state transition pathway in these animals was found to be wake → SWS → wake. No significant differences were noted with regard to total sleep time, number of episodes and episode duration for all states between the light and dark periods.Thus, prior classification of the rock hyrax as strongly diurnal does not appear to hold under controlled laboratory conditions.

Sleep and wake in rhythmic versus arrhythmic chronotypes of a microphthalmic species of African mole rat (Fukomys mechowii).

The giant Zambian mole rat (Fukomys mechowii) is a subterranean Afrotropical rodent noted for its regressed visual system and unusual patterns of circadian rhythmicity--within this species some individuals exhibit distinct regular circadian patterns of locomotor activity while others have arrhythmic circadian patterns. The current study was aimed at understanding whether differences in circadian chronotypes in this species affect the patterns and proportions of the different phases of the sleep-wake cycle. Physiological parameters of sleep (electroencephalogram and electromyogram) and behaviour (video recording) were recorded continuously for 72 h from 6 mole rats (3 rhythmic and 3 arrhythmic) using a telemetric system and a low-light CCTV camera connected to a DVD recorder. The results indicate that the arrhythmic individuals spend more time in waking with a longer average duration of a waking episode, less time in non-rapid eye movement (NREM) with a shorter average duration of an NREM episode though a greater NREM sleep intensity, and similar sleep cycle lengths. The time spent in rapid eye movement (REM) and the average duration of an REM episode were similar between the chronotypes.

Behavioral sleep in the walrus.

In this study we examined behavioral sleep in the walrus, the only living species of the family Odobenidae. The behavior of four 1.5-2-year-old captive walruses was videotaped continuously for 7-17 days and scored in 1-min epochs. When walruses had access to water and land, behavioral sleep, the combined amount of quiet and rapid eye movement (REM) sleep, occupied on average 17+/-4% of 24 h (n=4) with the majority of sleep occurring on land. All walruses alternated periods of almost continuous swimming lasting for 40-84 h with periods of rest on land lasting for 2-19 h. When in water they were predominantly awake (88-99% of the time). On land walruses were asleep on average 40-74% of the time. The total sleep time varied between 0 and 60% of 24h with the daily amount of REM sleep ranging from 0 to 5% of 24 h. In water, walruses slept while floating at the surface, lying on the bottom or standing and leaning against the pool wall. REM sleep in water occurred in all positions. On land the breathing pattern was regular during quiet sleep (most pauses were <30s) and arrhythmic in REM sleep (apneas lasted up to 160 s). While in water the irregularity of breathing further increased (apneas were >4 min) and all REM sleep episodes occurred during a single apnea. Data indicate that the pattern of sleep and breathing in walruses is similar to the Otariidae seals while on land and the Phocidae seals while in water.

Fur seals display a strong drive for bilateral slow-wave sleep while on land.

Fur seals (pinnipeds of the family Otariidae) display two fundamentally different patterns of sleep: bilaterally symmetrical slow-wave sleep (BSWS) as seen in terrestrial mammals and slow-wave sleep (SWS) with a striking interhemispheric EEG asymmetry (asymmetrical SWS or ASWS) as observed in cetaceans. We examined the effect of preventing fur seals from sleeping in BSWS on their pattern of sleep. Four northern fur seals (Callorhinus ursinus) kept on land were sleep deprived (SD) of BSWS for 3 consecutive days, followed by 1 recovery day. EEG asymmetry was evaluated both visually and by EEG spectral analysis. SD significantly reduced the percentage of high-voltage BSWS (on average to 14% of baseline) and REM sleep (to 60% of baseline) whereas the percentage of low-voltage BSWS was not affected. During the SD period, all seals repeatedly tried to enter BSWS (109-411 attempts per day). SD significantly increased the amount of ASWS in each seal when scored visually (to 116-235% of baseline) and the difference in the EEG slow-wave activity (spectral power in the range of 1.2-4.0 Hz) between the two hemispheres (117-197%) as measured by the asymmetry index. High-voltage BSWS and the amount of SWS in each hemisphere were significantly elevated during the first 4 h of recovery. These data indicate that fur seals display a homeostatic response to the loss of SWS and that alternating SWS in the two hemispheres does not adequately compensate for the absence of BSWS.