Abstract

During hibernation, critical physiological processes are downregulated and thermogenically induced arousals are presumably needed periodically to fulfil those physiological demands. Among the processes incompatible with a hypome tabolic state is sleep. However, one hibernating primate, the dwarf lemur Cheirogaleus medius, experiences rapid eye movement (REM)-like states during hibernation, whenever passively reaching temperatures above 30°C, as occurs when it hibernates in poorly insulated tree hollows under tropical conditions. Here, we report electroencephalographic (EEG) recordings, temperature data and metabolic rates from two related species (C. crossleyi and C. sibreei), inhabiting high-altitude rainforests and hibernating underground, conditions that mirror, to some extent, those experienced by temperate hibernators. We compared the physiology of hibernation and spontaneous arousals in these animals to C. medius, as well as the much more distantly related non-primate hibernators, such as Arctic, golden-mantled and European ground squirrels. We observed a number of commonalities with non-primate temperate hibernators including: (i) monotonous ultra-low voltage EEG during torpor bouts in these relatively cold-weather hibernators, (ii) the absence of sleep during torpor bouts, (iii) the occurrence of spontaneous arousals out of torpor, during which sleep regularly occurred, (iv) relatively high early EEG non-REM during the arousal, and (v) a gradual transition to the torpid EEG state from non-REM sleep. Unlike C. medius, our study species did not display sleep-like states during torpor bouts, but instead exclusively exhibited them during arousals. During these short euthermic periods, non-REM as well as REM sleep-like stages were observed. Differences observed between these two species and their close relative, C. medius, for which data have been published, presumably reflect differences in hibernaculum temperature.

Highlights

  • When neither food nor water is sufficient, mammals must either migrate or severely depress their metabolic processes to survive

  • This study provides the first analysis of EEG data during hibernation, including bouts of torpor and the subsequent spontaneous arousals in a primate hibernator

  • The findings suggest that sleep does not occur during torpor bouts in these two lemur species, which are exposed to relatively cold temperatures, in contrast with the western species, C. medius

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Summary

Introduction

When neither food nor water is sufficient, mammals must either migrate or severely depress their metabolic processes to survive. One recently emerged hypothesis proposes that the ability to reduce metabolism (and hide underground) is deeply rooted in mammalian phylogeny, and was critical for the survival of small mammals after the cataclysmic Cretaceous/Tertiary (K-T) extinction events—a period characterized by intense thermal radiation [8,9]. This would place the origins of hibernation in ‘tropical’ environments rather than the cold habitats we tend to associate hibernation with today

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