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

Abstract

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.

Dynamics of sleep oscillations is coupled to brain temperature on multiple scales

“…) and even fur seal (Lyamin et al . ) (though some monkey studies reported just the opposite (Reite & Pegram, ; Hayward & Baker, )). It is debated whether this effect is aimed to protect brain function from REM‐associated hypothermia, or simply reflects the increased metabolic activity due to increased unit firing.…”

The microstructure of REM sleep: Why phasic and tonic?

“…For instance, a study in mice reported remarkable differences across phasic and tonic REM states with respect to theta and gamma oscillations in the parietal cortex of the animals [134]. Exploring the distribution of, and neural (i.e., frequency-specific) activity during phasic and tonic REM periods in species exhibiting peculiar forms of sleep due to environmental constraints [8], or in species outside the mammalian order [2,135] could shed more light on the functions and evolutionary origins of REM sleep [136,137].…”

“…Indeed, empirical data indicates that REM-related muscle twitches contribute to the development of the sensorimotor system [6,7]. In addition, REM sleep functions putatively encompass a wide range of neural and cognitive phenomena from basic mechanisms such as the regulation of brain temperature [8], modulation of receptor sensitivity [9], and synaptic plasticity [10], to more complex processes such as procedural [11] and declarative [12] learning, emotional memory processing [13,14], or the development of consciousness [15].…”

Tired and stressed: Examining the need for sleep

“…However, recent work using EEG recordings from the great frigatebird Fregata minor showed that these birds, which can maintain flight for up to 10 days, accomplish in‐flight sleep through both unihemispheric and bihemispheric sleep, but that the duration of this sleep is less than 10% of their normal sleep time on land (Rattenborg et al., ). Interestingly, the fur seal, which lives both on land and in seawater, suppresses slow wave sleep when in the water and shows no subsequent slow wave rebound upon returning to land (Lyamin et al., ). Taken together, these examples indicate that certain ecological conditions can drive context‐dependent sleep suppression; however, it remains unclear if or how these animals might upregulate other processes to compensate for lost sleep.…”