Fur seals have no or little REM sleep when they stay in water

Virtually all land mammals and birds have two sleep states: slow-wave sleep (SWS) and rapid eye movement (REM) sleep []. After deprivation of REM sleep by repeated awakenings, mammals increase REM sleep time [], 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 []. However, separating the effects of REM sleep loss from the stress of repeated awakening is difficult []. The northern fur seal (Callorhinus ursinus) is a semiaquatic mammal []. 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 []. Here we show that when the fur seal stays in seawater, where it spends most of its life [], 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.

In contrast to the near elimination of REM sleep, the total amounts of SWS (USWS plus BSWS) in fur seals in seawater ranged from 45% to 129% of baseline values except for the first day in water (W1) when it was reduced on average to 20% of baseline. The drop in SWS in the seawater was significant only on W1 (p < 0.01 compared to the baseline and other days in seawater, ANOVA, F= 18.961, p = 7.63E−10; see Table S2 ). The time spent in SWS as depicted in Figure 3 D overestimates the amount of SWS that each hemisphere acquired, as SWS was largely unihemispheric in the water ( Figure 3 E). This hemispheric reduction of SWS may explain the increased time spent in SWS on R1. During all days in seawater, the amount of BSWS was significantly smaller than that under baseline conditions, with a decrease from 7.5% of the 24 hr to 0.5% of the 24 hr (p = 1.18E−09, F= 22.868) and the proportion of USWS was significantly greater with an increase from 62.0% to 93.8% of SWS time (p = 2.03E−08, F= 17.540; see Table S2 and Figure 3 E). After a return to baseline conditions on both recovery days, the amount of BSWS more than doubled with respect to the average baseline amounts (p < 0.001; Table S2 ). This represented a reversal of the decreased BSWS in the water. The increase of total SWS over baseline values on R1 (62%; p < 0.001, df = 6) and R2 (43%; p = 0.05) may also have been a partial consequence of the thermoregulatory and activity adjustments produced by the animals’ return to a dry platform after the 10–14 day in-water period. The proportion of USWS dropped back to 69% of baseline values ( Table S2 ).

For all seals combined, the average amount above baseline values on R1 was just 28 ± 17 min of the average 895 ± 147 min lost, or 3% ± 2% of REM sleep lost in seawater ( Table S3 ). The estimated loss of REM sleep in the fourth seal, which stayed in seawater for 14 days, the longest period studied, was 21.5 hr or 1,369% of the daily baseline. However, the amount of REM sleep on R1 and R2 was comparable to its baseline prior to the period in seawater ( Figure 4 B, seal 4). Across seals, the number of REM sleep episodes did not significantly differ from baseline on R1, as was the case with REM sleep amounts. The amount of REM sleep in the seals on R1 did not correlate with the amount of REM sleep lost. On R2, the amounts of REM sleep remained substantially greater than baseline values in only one of the four seals ( Tables S2 and S3 ).

On the first day the seals were returned to baseline conditions (“recovery” day 1, R1), the amounts of REM sleep were not significantly greater than during baseline (Tukey’s post hoc test, df = 6, p > 0.05; see Table S2 ) ( Figure 4 B). On average, REM percent of 24 hr was 38% ± 16% above baseline level on R1 and 18% ± 14% above baseline on R2, with two of the four seals accounting for most of this increase. The amounts of REM sleep in the other two seals on R1 and R2 were within the range of day-to-day variation under baseline conditions.

By the end of the 10day, an accumulated “loss” of the expected amounts of REM sleep under baseline conditions averaged 765 ± 72 min (12.8 hr) or 974% ± 8% of projected daily baseline amounts ( Figure 4 A and Table S3 ). The episodes of REM sleep in seawater were characterized by head jerks, submergence of the head with apneas lasting up to 75 s, heart rate deceleration, and arrhythmia ( Figure 2 B; see also STAR Methods ). Apneas (respiratory pauses longer than 30 s) were not recorded during waking or SWS on land.

(B) Despite their REM sleep loss, only two out of four seals (marked blue and brown) displayed a substantial increase in REM sleep beyond baseline values after return to baseline conditions. In two other seals (labeled light green and dark blue), REM sleep amounts were similar to the daily variation seen under baseline conditions. Average values are shown as mean ± SEM (see also Table S3 ).

(A) During 10–14 days in seawater, the estimated deficit of REM sleep in fur seals reached 995%–1,370% of the daily baseline amount. Different seals are coded by color, and average values are shown as gray bars. The dotted lines connect the last day in seawater (the 10 th , 11 th , or 14 th ) and the first recovery day in each seal.

Throughout the period in seawater, the average daily amount of REM sleep in seals was reduced to 3 min a day versus 80 min under baseline conditions (a 96.4% ± 1.0% reduction; one-way ANOVA, F= 27.506, p = 3.21E−13; see Table S2 ). This is a greater amount and percentage reduction than the average reduction seen even with automated REM-sleep-deprivation techniques in the rat []. In seawater, the number of REM sleep episodes per day decreased to 20% ± 3% of the baseline values (F= 10.754, p = 9.98E−08), and the average duration of REM sleep episodes decreased to 13% ± 1% of baseline (F= 6.508, p = 2.68E−05; see also Figures 2 A, 2B, and 3 A–3C and Table S2 ). No REM sleep was recorded in the seals during the first 3–7 days in seawater. In one of the four seals, REM sleep was recorded on only one of 11 days ( Figure 3 A).

The amount (A), duration (B), and number (C) of REM sleep episodes were substantially decreased in fur seals during the entire period in seawater. (D) shows the percentage of slow-wave sleep (BSWS plus USWS), and (E) shows the percentage of bilateral SWS (BSWS). No significant REM rebound was recorded when the fur seal returned to land. The total amounts of SWS decreased only on the first day in seawater and increased above baseline values when the seals were returned to baseline conditions (D). BSWS was almost completely absent in seawater (E; see also Table S2 ). The colored lines and symbols mark individual seals, and the gray bars indicate the average values. See also Table S4

REM Sleep Is Suppressed When Fur Seals Are in Seawater with Little or No Rebound When Returned to Baseline Conditions

Figure 3 REM Sleep Is Suppressed When Fur Seals Are in Seawater with Little or No Rebound When Returned to Baseline Conditions

We examined the sleep of fur seals when they were in seawater with and without access to a dry platform. These two experimental conditions approximate that of fur seals during the breeding and migratory seasons [] (see Table S1 ). We continuously recorded electroencephalogram (EEG), electromyogram, electrooculogram, and electrocardiogram using a data logger. Slow-wave sleep (SWS) and REM sleep on land occurred when fur seals were lying or sitting ( Figures 1 and 2 ). In agreement with our prior studies [], fur seals on land displayed REM and nonREM sleep. SWS includes both bilateral SWS (BSWS) and unihemispheric SWS (USWS; see Figure 1 E and Table S2 ), the latter resembling the unihemispheric slow-wave pattern seen in dolphins, with unilateral eye opening. After a baseline period of 2 days with access to a dry platform, the platform was removed for 10–14 days. In seawater, the seals slept at the surface predominantly in the lateral position (88% ± 7% of total sleep time, n = 4) with the remaining time in the prone position ( Figures 1 C, 1D, 1F, and 1G). SWS in seawater was predominantly USWS (94% ± 1% of all SWS compared to 61% ± 4% of SWS when on land; see Figures 1 E–1G and Table S2 ). There was a clear association between the lateralization of EEG slow waves in fur seals sleeping in seawater and the asymmetric lateral posture and eye opening [] ( Figure 1 F).

(B) Episodes of REM sleep in seawater were much shorter (on average 23 s, no longer than 2 min) than under baseline conditions on land. The cluster of REM episodes that is presented is among the longest that we observed in water. The short episodes occurred while the head was held above seawater (episodes 1–4) and when the head was submerged (episodes 5 and 6). As described above and in Figure 3 and Tables S2 and S3 , when fur seals were in the water, on many days, there was no REM sleep at all. REM sleep in fur seals was characterized by pronounced heart rate arrhythmia and apneas. High-voltage deflection in the EEG during episodes 1, 3, and 5 are movement artifacts caused by repeated immersion of head.

(A) Episodes of REM sleep in fur seals under baseline conditions were characterized by maximal muscle tone reduction and lasted up to 16 min (on average, 5 min). A representative episode is displayed.

(E–G) Periods of sleep and wakefulness on land and in the lateral and prone positions as shown by EEG of the two cerebral hemispheres and neck electromyogram (EMG). Brown dotted lines indicate left unihemispheric slow-wave sleep (USWS), and blue dotted lines indicate right USWS. The drawings above each panel indicate the predominant fur seal posture during the recording. (E) shows the predominant posture while sleeping on land with relatively little EEG asymmetry. (F) illustrates the most common posture of sleep in the fur seal in water. The initial posture, with the right front flipper moving in the water, is asssoicated with right USWS, and the second posture, with the left front flipper moving in the water, is associated with left USWS. (G) illustrates a prone posture in water, which is less common, as the fur seals begins sleeping in right USWS, then left, then right then left again without changing the position. The photo in (D) and polygrams in (E)–(G) are from [].

(C and D) Sleep in seawater at the surface in the lateral (C) and in a prone (D) position.

Discussion

4 Kushida C.A.

Bergmann B.M.

Rechtschaffen A. Sleep deprivation in the rat: IV. Paradoxical sleep deprivation. 12 Rechtschaffen A.

Bergmann B.M.

Everson C.A.

Kushida C.A.

Gilliland M.A. Sleep deprivation in the rat: X. Integration and discussion of the findings. When returned from their 10–14 days in seawater to baseline conditions (sleeping on a dry platform), the seals were in good condition, as judged by their appearance, activity, interaction with the experimenters, weight, and appetite. We did not undertake any further examination of changes in their health. The condition of fur seals after the extended REM sleep suppression in water is in dramatic contrast to that of rats deprived of REM sleep by the disk-over-water method for a similar period. The REM-sleep-deprived rats show weight loss, skin lesions, hypothermia, and a generally debilitated appearance, leading to death [].

4 Kushida C.A.

Bergmann B.M.

Rechtschaffen A. Sleep deprivation in the rat: IV. Paradoxical sleep deprivation. 12 Rechtschaffen A.

Bergmann B.M.

Everson C.A.

Kushida C.A.

Gilliland M.A. Sleep deprivation in the rat: X. Integration and discussion of the findings. 13 Everson C.A.

Gilliland M.A.

Kushida C.A.

Pilcher J.J.

Fang V.S.

Refetoff S.

Bergmann B.M.

Rechtschaffen A. Sleep deprivation in the rat: IX. Recovery. 4 Kushida C.A.

Bergmann B.M.

Rechtschaffen A. Sleep deprivation in the rat: IV. Paradoxical sleep deprivation. 13 Everson C.A.

Gilliland M.A.

Kushida C.A.

Pilcher J.J.

Fang V.S.

Refetoff S.

Bergmann B.M.

Rechtschaffen A. Sleep deprivation in the rat: IX. Recovery. In further contrast, REM sleep deprivation in the rat produced a significant increase of 560% of baseline REM amounts on recovery day 1 and 180% of baseline amounts on days 2–15 []. This difference in recovery amounts between fur seals and rats occurred despite the much greater loss of REM sleep in the fur seal, since the automated deprivation apparatus used in the rat had to first detect sleep states before each disruption, i.e., a considerable amount of REM sleep occurred during each of the hundreds of detections each day. In these rat studies, as in all conventional REM-sleep-deprivation studies, a considerable disruption of nonREM sleep also occurred [].

14 Siegel J.M. Clues to the functions of mammalian sleep. Prompted by the current findings, we re-analyzed the data we previously reviewed [] for spontaneous REM sleep time versus nonREM sleep time across mammalian species. All land mammals so far examined have bilateral nonREM sleep exclusively. We find that REM sleep time is correlated with nonREM sleep time (r = +0.488, p = 0.000279; see Table S4 ). Thus, REM sleep amounts are a function of bilateral nonREM amounts, even as these nonREM amounts vary across terrestrial mammalian species.

3 Dement W. The effect of dream deprivation. 15 Shiromani P.J.

Lu J.

Wagner D.

Thakkar J.

Greco M.A.

Basheer R.

Thakkar M. Compensatory sleep response to 12 h wakefulness in young and old rats. 16 Lesku J.A.

Rattenborg N.C.

Valcu M.

Vyssotski A.L.

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Heidrich W.

Kempenaers B. Adaptive sleep loss in polygynous pectoral sandpipers. 17 Rattenborg N.C.

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Wikelski M.

Vyssotski A.L. Evidence that birds sleep in mid-flight. 7 Gentry R.L. Behavioral Ecology of the Northern Fur Seal. The assumption has been that animals have a daily need for REM sleep and display a rebound of REM sleep amount and intensity after it has been selectively eliminated or reduced, even if the loss is not fully recovered []. The northern fur seal is a semiaquatic mammal. During the summer breeding season, fur seals alternate between staying on land for a period of several days and foraging in the ocean for periods of up to 2 weeks. During their winter migration, fur seals remain continuously pelagic for up to 10 months []. We have found that REM sleep is eliminated or greatly reduced when fur seals enter seawater. This lasts for a period of at least 2 weeks. We also found that after a return to baseline conditions, REM sleep was substantially increased in only two out of the four fur seals. In addition, the increase of REM sleep was not proportional to REM sleep lost. REM sleep and BSWS amounts are reduced in fur seals in seawater, at a time when the animal requires high levels of alertness, cognitive performance, learning, and motor activity to navigate, locate prey, and avoid predators compared to when the animals are resting in large, safe groups on land and have daily REM sleep.

1 Lesku J.A.

Rattenborg N.C. Avian sleep. 2 Siegel J.M. Rapid eye movement sleep. 18 Parmeggiani P.L.

Zamboni G.

Cianci T.

Calasso M. Absence of thermoregulatory vasomotor responses during fast wave sleep in cats. 8 Lyamin O.I.

Mukhametov L.M.

Siegel J.M. Sleep in the northern fur seal. 11 Lyamin O.I.

Manger P.R.

Ridgway S.H.

Mukhametov L.M.

Siegel J.M. Cetacean sleep: an unusual form of mammalian sleep. 19 Lyamin O.I. Sleep in the harp seal (Pagophilus groenlandica). Comparison of sleep on land and in water. 20 Castellini M.A.

Milsom W.K.

Berger R.J.

Costa D.P.

Jones D.R.

Castellini J.M.

Rea L.D.

Bharma S.

Harris M. Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups. 21 Mitani Y.

Andrews R.D.

Sato K.

Kato A.

Naito Y.

Costa D.P. Three-dimensional resting behaviour of northern elephant seals: drifting like a falling leaf. One can appreciate why suppression of REM sleep and high-voltage bilateral SWS would be adaptive in fur seals when they stay in seawater. It is known that animals sleeping under the risk of predation have smaller amounts of REM sleep []. Muscle tone reduction and elevated arousal thresholds are features of REM sleep and bilateral SWS []. Thus, long episodes of bilateral sleep at the surface of seawater with bilateral eye closure would be potentially dangerous for fur seals. Aspiration of seawater during sleep is also a considerable risk since the nostrils must be held above the waves. Thermoregulation is impaired in REM sleep [], and long episodes in cold water might cause hypothermia []. Phocidae seals (the other group of pinnipeds) deal with some of these issues by holding their breath and hiding in the seawater’s depths during which REM sleep of normal duration may occur []. Phocids, unlike otariids, do not have USWS in seawater or on land.

11 Lyamin O.I.

Manger P.R.

Ridgway S.H.

Mukhametov L.M.

Siegel J.M. Cetacean sleep: an unusual form of mammalian sleep. An absence or nearly complete absence or REM sleep may be a characteristic of unihemispherically sleeping animals. Repeated studies of cetaceans (dolphins and whales) have failed to find evidence for REM sleep in any amount []. Cetaceans solve the problem of breathing and maintaining vigilance in the ocean environment by never showing bilateral high-voltage EEG activity. Rather, they have periods of high-amplitude unihemispheric slow waves, which can occur during swimming, while the other hemisphere shows a waking EEG. We find that fur seals convert their bilateral nonREM sleep on land to a largely unihemispheric pattern in seawater, in parallel with a profound reduction or elimination of REM sleep.

22 Carskadon M.A.

Dement W.C. Normal human sleep. 23 Ursin R. The two stages of slow wave sleep in the cat and their relation to REM sleep. 24 Benington J.H.

Heller H.C. Does the function of REM sleep concern non-REM sleep or waking?. 22 Carskadon M.A.

Dement W.C. Normal human sleep. It has been hypothesized that the function of REM sleep is linked to nonREM sleep []. In land mammals, REM sleep normally follows nonREM periods, and the duration and intensity of phasic events in REM increases throughout the sleep period, being maximal near the time of spontaneous awakening []. We hypothesize that a major function of REM sleep may be the reversal of the metabolic depression and cooling of the brainstem that result from prolonged bilateral nonREM sleep. Novel evidence for this is the correlation of REM sleep amount with nonREM sleep across mammalian species (see Table S4 ). Further work is necessary to determine the strength of this relation across species, the timing and duration of individual REM periods in relation to prior nonREM periods, and the role of circadian and environmental variables in the occurrence of REM sleep.

2 Siegel J.M. Rapid eye movement sleep. 2 Siegel J.M. Rapid eye movement sleep. 25 Jouvet M.

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Sastre J.P. Progressive hypothermia is accompanied by an almost permanent paradoxical sleep in pontine cats. 26 Szymusiak R.

McGinty D. Hypothalamic regulation of sleep and arousal. The brainstem is necessary and sufficient for REM sleep generation []. In a decerebrate cat, in which hypothalamic thermoregulatory systems are removed or disconnected from the brainstem, thermoregulation is abolished and brain temperature drifts toward the controlled environmental temperature. Under these conditions, low brain temperature is associated with greatly increased REM sleep, with REM comprising up to 70% of recording time at a brain temperature of 25°C, an amount of REM never seen in intact cats (or any other mammal). Average baseline REM sleep amounts in intact cats at a brain temperature of 39°C is 13% []. Thus, the brainstem generators of REM sleep are triggered by brain cooling, consistent with a role of the smaller reduction in temperature which occurs in nonREM sleep in triggering the smaller REM durations seen in intact mammals [].

13 Everson C.A.

Gilliland M.A.

Kushida C.A.

Pilcher J.J.

Fang V.S.

Refetoff S.

Bergmann B.M.

Rechtschaffen A. Sleep deprivation in the rat: IX. Recovery. Total sleep deprivation by the disk over water technique in the rat elicits a surprising, and very large, increase in REM sleep, rather than total sleep or nonREM sleep when the deprivation ends []. But this method of deprivation not only decreases sleep, it also decreases body and brain temperature. This is consistent with a triggering of REM sleep to counter the brain hypothermia that occurs with the disk-over-water deprivation technique.

27 Wehr T.A. A brain-warming function for REM sleep. 28 Horner R.L.

Sanford L.D.

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Morrison A.R. Activation of a distinct arousal state immediately after spontaneous awakening from sleep. 29 Parmeggiani P.L. REM sleep related increase in brain temperature: a physiologic problem. 30 Buchsbaum M.S.

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Bunney Jr., W.E. Positron emission tomography with deoxyglucose-F18 imaging of sleep. 31 Schmidt M.H. The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness. 32 Siegel J.M. Sleep in animals: a state of adaptive inactivity. Further studies might be profitably aimed at recording temperature from both cerebral hemispheres and bilaterally in the brainstem of the fur seal in seawater and on land and determining the temperature dependence of REM triggering. Alertness and brain temperature are considerably greater when animals awaken at the end of periods of REM than after nonREM sleep [] as is brain metabolic rate []. The alternation of nonREM and REM sleep allows animals to achieve the energetic savings of nonREM sleep [], without the relatively impaired awakening that occurs in nonREM sleep arousals.