Oleg I. Lyamin

Cetacean sleep: An unusual form of mammalian sleep

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.

Unihemispheric slow wave sleep and the state of the eyes in a white whale

We recorded electroencephalogram (EEG) and simultaneously documented the state of both eyelids during sleep and wakefulness in a sub-adult male white whale over a 4-day-period. We showed that the white whale was the fifth species of Cetaceans, which exhibits unihemispheric slow wave sleep. We found that the eye contralateral to the sleeping hemisphere in this whale was usually closed (right eye, 52% of the total sleep time in the contralateral hemisphere; left eye, 40%) or in an intermediate state (31 and 46%, respectively) while the ipsilateral eye was typically open (89 and 80%). Episodes of bilateral eye closure in this whale occupied less than 2% of the observation time and were usually recorded during waking (49% of the bilateral eye closure time) or low amplitude sleep (48%) and rarely in high amplitude sleep (3%). In spite of the evident overall relationship between the sleeping hemisphere and eye state, EEG and eye position in this whale could be independent over short time periods (less than 1 min). Therefore, eye state alone may not accurately reflect sleep state in Cetaceans. Our data support the idea that unihemispheric sleep allows Cetaceans to monitor the environment.

Cortical Acetylcholine Release Is Lateralized during Asymmetrical Slow-Wave Sleep in Northern Fur Seals

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 ∼300% during AW, and ∼200% 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.

Behavioral aspects of sleep in bottlenose dolphin mothers and their calves

Adult dolphins are capable of sleeping with one eye open and exhibiting slow wave activity in the electroencephalogram (EEG) of one hemisphere at a time. The aim of this study was to examine the postpartum sleep behavior of bottlenose dolphin calves and their mothers. The behavior of three dolphin mother-calf pairs was monitored from birth to 13 months postpartum. Dolphin mothers and their calves exhibited a complete disappearance of rest at the surface for a minimum of 2 months postpartum, swimming in echelon formation on average in 97-100% of the observation time. Calves surfaced to breathe more often than their mothers between the postpartum age of 2 and 8 weeks. During the first postpartum month two dolphin mothers surfaced with both eyes open on average in 93 and 98% of the time while in their calves both eyes were open in 90 and 60% of the cases. In calves, the eye directed toward the mother was open more often (on average in 95% of all observations in calf 1 and 99% in calf 2) than the eye directed to the opposite side (82% in calf 1 and 60% in calf 2). Our data indicate that dolphin mothers and calves are highly active and vigilant during the initial period of the calfs life, continuously monitoring their position relative to each other by sight during wakefulness and sleep. We hypothesize that episodes of EEG slow wave activity at this time are likely to be brief, fragmenting EEG defined sleep into short episodes.

Electroencephalogram asymmetry and spectral power during sleep in the northern fur seal

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 the asymmetry index [AI = (L − R)/(L + R), where 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 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.

Muscle jerks during behavioral sleep in a beluga whale (Delphinapterus leucas L.)

We conducted video recording of the behavior of one captive adult male beluga (or white) whale over eight nights aiming to quantify muscle jerks and to evaluate their relationship to the sleep-waking cycle. Presumably, the whale was asleep during a significant portion of the time it spent lying on the bottom of the pool. Individual sleep episodes lasted between 20 and 492 s and on average occupied 66.7+/-2.6% of the nighttime (n=8). Muscle jerks were quantified in the last three nights, during which an average of 144+/-24 jerks were documented per night. Forty-six percent of all jerks occurred within 10 s of each other. Series of jerks lasted 2-21 s (on average 4.8+/-0.5 s, n=97) and in total occupied 0.3-0.7% of the rest time (0.2-0.5% of total nighttime). Jerks occurred more frequently at the end of rest episodes. A significant portion of rest episodes with jerks (62%) followed each other. These series of episodes with jerks alternated with periods when jerks were not recorded over 8-37 min. We conclude that some jerks meet the behavioral criteria of paradoxical [or rapid eye movement (REM)] sleep (PS). On the other hand, definitive conclusions about the presence and duration of this sleep stage in cetaceans cannot be reached without further combined electropolygraphic studies and visual observations.

Sleep in the harp seal (Pagophilus groenlandica). Peculiarities of sleep in pups during the first month of their lives

SUMMARY  Two white‐coated (ten day‐old) and two grey‐spotted (one month‐old) pups of the harp seal were implanted with electrodes for recording the electrocorticograms of the two hemispheres, electrocardiogram, electrooculogram and electromyogram of the neck muscles. In all individuals ECoG slow waves always developed synchronously in both hemispheres. When white and grey pups were recorded on the snow, the amount of active wakefulness was, respectively, 21.1% (s.e. 11.8%) and 29.9% (s.e. 0.2%) of total recording time, quiet wakefulness = 27.1% (s.e. 4.4%) and 38.2% (s.e. 6.6%), drowsiness = 7.7% (s.e. 0.5%) and 2.07% (s.e. 0.9%), light slow‐wave sleep (SWS) = 15.1% (s.e. 3.2%) and 13.0% (s.e. 2.4%), deep SWS = 21.2% (s.e. 2.4%) and 13.8% (s.e. 3.8%), paradoxical sleep (PS) = 8.0% (s.e. 1.4%) and 7.4% (s.e. 1.1%). PS always followed SWS and was fragmented. Respiration was very rare and irregular in PS and a considerable part of PS episodes occurred within a single respiratory pause. During SWS all pups displayed respiratory pauses of up to three minutes, alternating with hyperventilation periods. Heart rate was lowest in PS. Peculiarities of sleep and the pace of sleep pattern development during the first month in seals may be adaptive to the cold environment and ice field drifting in their habitat.

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.

Sleep behaviour: Sleep in continuously active dolphins; Activity and sleep in dolphins (Reply)

All terrestrial mammals studied so far do maximal amounts of sleeping at birth, with sleep time gradually decreasing to adult levels. This has led to the concept that sleep, with its characteristic immobility and unresponsiveness, is necessary for brain and body development. We reported that dolphins and killer whales have a very unusual developmental pattern: neonates are maximally and continuously active at birth, and this activity diminishes over a period of months to the adult level; in the postpartum period, mothers also abruptly cease the characteristic ‘hanging’ that constitutes the typical sleep behaviour in bottlenose dolphins and killer whales. We did not claim that all sleep was abolished in the postpartum period. Rather, we reported that immobility was absent and that typical sleep posture increases with age, a pattern opposite to that seen in all land mammals studied so far. Sekiguchi et al. and Gnone et al. challenge our conclusions.