Different Effects of Sleep Deprivation and Torpor on EEG Slow-Wave Characteristics in Djungarian Hamsters

Abstract

It has been shown previously in Djungarian hamsters that the initial electroencephalography (EEG) slow-wave activity (power in the 0.5–4.0 Hz band; SWA) in non-rapid eye movement (NREM) sleep following an episode of daily torpor is consistently enhanced, similar to the SWA increase after sleep deprivation (SD). However, it is unknown whether the network mechanisms underlying the SWA increase after torpor and SD are similar. EEG slow waves recorded in the neocortex during sleep reflect synchronized transitions between periods of activity and silence among large neuronal populations. We therefore set out to investigate characteristics of individual cortical EEG slow waves recorded during NREM sleep after 4 h SD and during sleep after emergence from an episode of daily torpor in adult male Djungarian hamsters. We found that during the first hour after both SD and torpor, the SWA increase was associated with an increase in slow-wave incidence and amplitude. However, the slopes of single slow waves during NREM sleep were steeper in the first hour after SD but not after torpor, and, in contrast to sleep after SD, the magnitude of change in slopes after torpor was unrelated to the changes in SWA. Furthermore, slow-wave slopes decreased progressively within the first 2 h after SD, while a progressive increase in slow-wave slopes was apparent during the first 2 h after torpor. The data suggest that prolonged waking and torpor have different effects on cortical network activity underlying slow-wave characteristics, while resulting in a similar homeostatic sleep response of SWA. We suggest that sleep plays an important role in network homeostasis after both waking and torpor, consistent with a recovery function for both states.

Daily Torpor and Sleep in a Non-human Primate, the Gray Mouse Lemur (Microcebus murinus)

“…Contrary to REM sleep, the time spent in NREM sleep increases with the prior heterothermy duration (Strijkstra and Daan, 1997). It is noteworthy that the effects of hypometabolism are similar to those observed after sleep deprivation (Deboer and Tobler, 1994; Vyazovskiy et al, 2017). Indeed, after the emergence from daily torpor, animals show a rebound of sleep, which is explained by the accumulation of a sleep debt, suggesting that torpor and hibernation might be inconsistent with the recovery function of sleep.…”

“…The arousal episodes may be necessary to induce sleep processes. Moreover, previous studies in Djungarian hamsters show that hypometabolism is followed by a period of sleep (Deboer and Tobler, 1994; Vyazovskiy et al, 2017). Contrary to REM sleep, the time spent in NREM sleep increases with the prior heterothermy duration (Strijkstra and Daan, 1997).…”

The Temperature Dependence of Sleep

“…Djungarian hamster ( Phodopus sungorus ), Golden-mantled ground squirrel ( Callospermophilus lateralis ), Fat-tailed dwarf lemur ( Cheirogaleus medius ), Arctic ground squirrel ( Urocitellus parryii ). Data adapted from Frerichs et al (1994); Ruf and Geiser (2015), and Vyazovskiy et al (2017).…”

“…While this sleep debt, as measured by delta power, accumulates during torpor it does so almost three times slower at brain temperature below 27°C, compared with time awake (Deboer and Tobler, 2003). However, comparisons of recovery sleep EEG, following sleep deprivation or torpor, revealed differences in cortical network activity suggesting that torpor is not entirely equivalent to either sleep deprivation or natural sleep (Vyazovskiy et al, 2017). Thus, a critical temperature may exist below which sleep function is impaired.…”

Brain energetics during the sleep–wake cycle

“…Second, rapid eye movement (REM) sleep is as expensive as wakefulness and the suspension of thermoregulation during REM sleep is paradoxically associated with increases in brain metabolic heat production and temperature [ 4 ]. Third, neither torpor/hibernation (for instance, in mammals undergoing daily hypothermia) [ 5 ] nor several anesthetic states [ 6 ] can completely redeem sleep need and recovery, in spite of the loss of consciousness and the accompanying decrease of energy use. Sleep must be related to some essential functions that are adaptive to the organism in the face of their relatively high energy requirements.…”