Evaluation of the ability of northern fur seals to perceive and visually discriminate images under the conditions of sleep loss.

This is the first study estimating the ability of sea mammals to perceive and analyze information under the conditions of an almost complete sleep deprivation.

[Sleep in cetaceans].

Over the course of evolution, cetaceans have adapted to sleep in conditions that can be considered extreme for warm-blooded and air breathing animals. Studies of sleep in cetaceans have led to the discovery of an unusual type of sleep called unihemispheric slow wave sleep. The ability of cetaceans to sleep during swimming and to close only one eye at a time are two other features of their sleep, directly related to its unihemispheric nature. Paradoxical sleep in the form it is recorded in all terrestrial mammals is absent in cetaceans. The pattern of sleep in cetaceans allows them to 1) monitor the environment for predators and conspecifics to maintain group coherence, 2) surface regularly for breathing and 3) maintain effective thermoregulation.

Study of sleep in a walrus.

Several behavioral and physiological adaptations have been developed in evolution of Pinnipeds allowing them to sleep both on land and in water. To date sleep has been examined in detail in eared and true seals (the families of Otariidae and Phocidae). The aim of this study was to examine sleep in another semiaquatic mammal - the walrus, which is the only extant representative of the family Odobenidae. Slow wave and paradoxical sleep (SWS and PS) in the examined walrus (2 year old female, weight 130 kg) averaged 19.4 ± 2.0 and 6.9 ± 1.1% of 24-h when on land, and 20.5 ± 0.8% of 24-h and 1.1 ± 0.6% when in water, respectively. The average duration of PS episode was 6.4 ± 0.6 min (maximum 23 min) when on land and 1.8 ± 0.1 min (maximum 3.3 min) when in water. In water, sleep occurred predominantly while the walrus submerged and lay on the bottom of the pool (89% of total sleep time). The walrus usually woke up while emerging to the surface for breathing. Most often EEG slow waves developed synchronously in both cortical hemispheres (90% of SWS time when on land and 97% when in water). Short episodes of interhemispheric EEG asymmetry usually coincided with brief opening of one eye. The pattern of sleep in the walrus was similar to the pattern of sleep in the Otariidae seals while on land (predominantly bilateral SWS, accompanied by regular breathing) and to the pattern of sleep in the Phocidae while in water (sleep during apneas both in depth and at the surface, interrupted by brief arousal when emerging for breathing).

[Rest and activity states in the Commerson's dolphin (Cephalorhynchus commersonii)].

The unihemispheric slow-wave sleep, the ability to sleep during swimming with one open eye and the absence of paradoxical sleep in the form of it is observed in all terrestrial mammals are unique features of sleep in cetaceans. Visual observations supplement electrophysiological studies and allow obtaining novel data about sleep of cetaceans. In the present study we examined behavior of 3 adult Commerson's dolphins Cephalorhynchus commersonii which were housed in the oceanarium Sea-World (San Diego, USA). The behavior of the dolphins can be subdivided into 5 swimming types: 1) active swimming marked by variable speed and irregular trajectory of movement (on average for 3 dolphins 35.1 +/- 2.7% of the 24-h period) was scored as active wakefulness; 2) circular swimming was divided into slow and fast swimming and occupied, on average, 44.4 +/- 3.8 and 9.7 +/- 0.8% of the 24-h period, respectively; while in circular swimming, dolphins swam from 1 to 6 circles on one respiration pause; 3) quiet chaotic swimming (3.9 +/- 1.2%) that occurred at the bottom and was not accompanied by signs of activity; 4) floating, and 5) slow swimming at the surface (4.1 +/- 0.5 and 2.8 +/- 0.4%), respectively; the latter two swimming types were accompanied by frequent respiration (hyperventilation). We suggest that sleep in Commerson's dolphins occurred predominantly during the circular and quiet swimming. From time to time the dolphins slowed down their speeds and even stopped for several seconds. Such episodes appeared to be the deepest sleep episodes. In all dolphins muscle jerks as well erections in the male were observed. Jerks and erections occurred during the circular and quiet chaotic swimming. Similar to other studied small cetaceans, Commerson's dolphins are in a state of almost uninterrupted swimming during 24 h per day and they sleep during swimming. Some muscle jerks that we observed in the dolphins in this study might have been episodes of paradoxical sleep.

Relationship between sleep and eye state in Cetaceans and Pinnipeds.

We recorded EEG from both hemispheres and documented the state of the two eyes in two species of Cetaceans (one beluga and one bottlenose dolphin) and one species of Pinnipeds (two northern fur seals). In the dolphin and beluga we found that episodes of unihemispheric slow wave sleep (USWS) were associated with asymmetry in eye state. During USWS and asymmetrical SWS the eye contralateral to the sleeping hemisphere was mostly closed or in an intermediate state while the eye contralateral to the waking hemisphere was more often open or in an intermediate state. Bilateral eye opening indicated waking in about 80% cases and unilateral eye closure indicated USWS with an accuracy of about 75%. Bilateral eye closure was rare (< 2% of the observation time) and was not necessarily associated with high amplitude SWS. In fur seals, episodes of one eye briefly opening usually occurred in the beginning of sleep episodes and lasted several minutes. Those episodes were frequently associated with lower amplitude EEG slow waves in the contralateral brain hemisphere. During most of their sleep on land, fur seals had both eyes tightly closed. No EEG asymmetry was recorded at this time. Although eye state and EEG stage are correlated in the bottlenose dolphin, beluga and fur seals, short episodes of EEG synchrony (less then 1 min) occur contralateral to an open eye and waking (a more activated EEG) activity can be present contralateral to a closed eye. The available data suggest that two functions of USWS/EEG asymmetry during SWS in Cetaceans and fur seals are multisensory control of the environment and maintenance of motion and postures of sleep. The adaptive advantages of USWS throughout the evolution of Cetaceans and Pinnipeds from terrestrial mammals to present forms could include 1) the avoidance of predators and maintenance of contact with other animals of the same species; 2) continuance of regular breathing; 3) and effective thermoregulation in the water environment.

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.

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.

Rest and activity states in a gray whale.

The behaviour of a female gray whale (Eschrichtius robustus) that had been rescued 14 months previously was recorded continuously on a video-recorder for 9 days at 'Sea World' in San Diego. On average, during the first six recording days, active wakefulness accounted for 37.9 +/- 1.7% of each 24 h; transitional stage for 17.4 +/- 1.4% and rest for 41.2 +/- 1.7%. In the rest stage the whale was lying on the bottom of the pool (13.2 +/- 1.7%) or hanging on the surface (28. 0 +/- 1.7%). During the rest stage, it was immobile most of the time and moved only for respiration. In the rest stage both eyes could be open, one eye could be open while the other was closed or, more rarely, both eyes could be closed. Characteristic jerks of the head, neck and sometimes of the whole body were observed in the whale during the rest stage. Most jerks were single and only 10% of all jerks were serial (occurring within 10 s of a prior jerk). Eyelid movements accompanied 40% of jerks. In two episodes, intense jerks followed each other continuously for 3 and 4 s and were accompanied by eyelid movements. These jerks resembled the twitches characteristic of paradoxical sleep in terrestrial mammals. During these episodes the whale was falling slowly onto its side and subsequently started to swim in the pool.

Sleep in an Amazonian manatee, Trichechus inunguis.

For the first time, sleep was studied in a representative of the order of Sirenia. Slow wave sleep occupied 27%, and paradoxical sleep 1% of the total recording time in the Amazonian manatee. Trichechus inunguis. The circadian rhythmicity of sleep was pronounced. During the sleep period, the manatee woke up for a short time for each respiratory act. Interhemispheric asynchrony of the electrocortical slow wave activity was found.

[Quantitative characteristics of the electrocorticographic sleep stages in bottle-nosed dolphins]. / Kolichestvennaia kharakteristika élektrokortikograficheskikh stadii sna u del'finov-afalin.

Quantitative analysis of the ECoG stages in four bottle-nosed dolphins has demonstrated that unihemispheric slow-wave sleep is the dominant type of their natural sleep. All the variants of the bilateral and unilateral ECoG synchronization comprise 33.4% of the total recording time, with unilateral slow-wave sleep accounting for 28.8%. A single brain hemisphere is in a state of ECoG synchronization for 19% of the total recording time. The maximal amount of sleep is registered during a night and the second half of the day. Unihemispheric sleep episodes tend to appear alternatively in both hemispheres.

Unihemispheric slow-wave sleep in the Amazonian dolphin, Inia geoffrensis.

An electroencephalographic study of sleep in Amazonian dolphins, Inia geoffrensis, revealed that unihemispheric slow-wave sleep is the dominant sleep type in this species, as in the other two dolphin species that were studied earlier.

[Features of sleep in the water by the northern fur seal Callorhinus ursinus]. / Osobennosti sna v vode u severnykh morskikh kotikov.

The peculiarities of sleep in water and on land were investigated in four adult Northern fur seals (Callorhinus ursinus) of both sexes. The electrocorticogram of both hemispheres, the neck electromyogram, the electrooculogram and electrocardiogram were recorded with implanted electrodes. The interhemispheric asymmetry of EEG during slow wave sleep was observed in all the animals sleeping in water and on land. The relative amount of interhemispheric slow wave asymmetry was higher during the sleep in water comparing to that on land. The fur seals maintain their special sleep posture on the water surface by moving only one of their front flippers. The asymmetric EEG in fur seals sleeping in the water may be attributed to the asymmetric motor activity of their flippers.

Interhemispheric asynchrony of the sleep EEG in northern fur seals.

In northern fur seals the two brain hemispheres can generate the EEG slow waves during sleep not only simultaneously, as in all the terrestrial mammals investigated, but also independently as in dolphins.

[Sleep and wakefulness in Callorhinus ursinus]. / Son i bodrstvovanie u severnykh morskikh kotikov.

Sleep and wakefulness of northern fur seals were studied on three subadult bulls carrying the implanted electrodes for recording the electrocorticogram of the two hemispheres, the neck electromiogram, the electrooculogram and the electrocardiogram. The active wakefulness accounted for 32.0 +/- 5.3% of total recording time, the relaxed wakefulness -31.7 +/- 3.1%, the slow wave sleep -30.5 +/- 5.1% and the paradoxical sleep -5.8 +/- 0.9%. The sleep cycle averaged 22,6 +/- 1.2 minutes. Interhemispheric asymmetry of the ECoG slow waves was pronounced in all three animals. Different forms of the asymmetry occupied 15.0 +/- 0.7% of total recording time. Such interhemispheric asymmetry was found in pinnipeds for the first time, in this respect the northern fur seals differ from the Caspean seals but resemble the dolphins.

[Sleep of Caspian seals]. / Son kaspiiskikh tiulenei.

ECoG both hemispheres, EOG, neck EMG, ECG and electrical activity of olfactory bulbs were recorded in 4 free moving adult Caspean seals of both sexes. Their sleep on land and in water was compared. The wakefulness occupied 85,5 +/- 1,5% of total recording time, the slow wave sleep--12,8 +/- 1,4% and paradoxical sleep--1,7 +/- 0,2%. Unlike the dolphins, the Caspean seals possess no unihemispheric slow wave sleep. When the seals sleep on the land or on the water surface and do not change their posture for breathing they may breathe without awakening like the terrestrial mammals. But when the seals emerge or change their posture to get nostrils above the water they wake up briefly for respiration period.

[Electroencephalographic study of sleep in Sea of Azov porpoises]. / Elektroéntsefalograficheskoe issledovanie sna u del'finov-azovok.

ECoG of both hemispheres, EMG of neck muscles, ECG and respiration rate were recorded in 3 free swimming Black Sea porpoises. The sleep characteristics in the porpoises were similar to those in the bottlenose dolphins which have been investigated earlier. Unihemispheric slow sleep was the main type of the porpoise sleep. Paradoxical sleep has not yet been found in them. All ther types of the porpoise sleep occurred during swimming and therefore could not serve to spare energy and to immobilize the animal. The experiments with nembutal and diazepam administration suggest that the functional necessity of the unihemispheric sleep results from the impossibility of maintaining dolphins' respiration during bilateral delta-sleep.