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.

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.

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.

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.

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.

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.

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.

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.

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.