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

Abstract

Daily torpor is an energy-saving process that evolved as an extension of non-rapid eye movement (NREM) sleep mechanisms. In many heterothermic species there is a relation between torpor expression and the repartition of the different behavioral states of sleep. Despite the presence of sleep during this period of hypothermia, torpor induces an accumulation of sleep debt which results in a rebound of sleep in mammals. We aimed to investigate the expression of sleep-wake rhythms and delta waves during daily torpor at various ambient temperatures in a non-human primate model, the gray mouse lemur (Microcebus murinus). Cortical activity was measured with telemetric electroencephalography (EEG) recordings in the prefrontal cortex (PFC) during the torpor episode and the next 24 h following hypothermia. Gray mouse lemurs were divided into two groups: the first group was subjected to normal ambient temperatures (25°C) whereas the second group was placed at lower ambient temperatures (10°C). Contrary to normal ambient temperatures, sleep-wake rhythms were maintained during torpor until body temperature (Tb) of the animals reached 21°C. Below this temperature, NREM and REM sleep strongly decreased or were absent whereas the EEG became isoelectric. The different states of sleep were proportional to Tbmin during prior torpor in contrast to active phases. Delta waves increased after torpor but low Tb did not induce greater delta power compared to higher temperatures. Our results showed that Tb was a determining factor for the quality and quantity of sleep. Low Tb might be inconsistent with the recovery function of sleep. Heterothermy caused a sleep debt thus there was a rebound of sleep at the beginning of euthermia to compensate for the lack of sleep.

Mouse lemur, a new animal model to investigate cardiac pacemaker activity in primates

“…We do not have an immediate explanation for this heart rate variations, but its prolonged dynamic suggests that it could be a physiological phenomenon with more complex causes than the classical vagal modulation 5 . We hypothesize that this slow heart rate decrease could be related to the mechanism that allows M. murinus to enter into a torpor state, to save energy when the outside temperature drops 29 30 .…”

“…In captivity, it is bred because, unlike rodents and similarly to humans, it spontaneously develops age-related neurodegeneration like Alzheimer disease 24 25 26 27 28 . Moreover, it presents unique and ancestral features for primates, like the ability to enter into a torpor state to save energy when the outside temperature drops 29 30 .…”

Re-examining extreme sleep duration in bats: implications for sleep phylogeny, ecology and function

“…Gray mouse lemurs (Royo et al, 2019), European ground squirrels (Strijkstra et al, 1999) and laboratory mice (Huang et al, 2021) have been shown to enter torpor through a state of electrophysiological euthermic NREM. Electrophysiological REM has also been detected during shallow torpor at relatively high ambient temperatures (Royo et al, 2019), although this state is usually abolished as animals become hypothermic and EEG power decreases (Strijkstra et al, 1999;Huang et al, 2021). It is therefore possible for torpor and sleep to coincide using the commonly accepted criteria for these states.…”

“…As in other animals, the relationship between sleep and torpor in bats is unknown (Ruczynski et al, 2014). Using currently accepted criteria, it is possible for these states to coincide (Strijkstra et al, 1999;Royo et al, 2019;Huang et al, 2021, see Box 2). If sleep and torpor did coincide in Brebbia and Pyne's recordings, this may render their findings incompatible with sleep recordings from other animals for two reasons.…”

“…Below 19 • C an isoelectric EEG lacking sleep rhythms suggests a deepening of torpor, which the authors recognised as a "unique state of consciousness...at hypothermic extreme" (Brebbia and Pyne, 1972). Although the sleep EEG was described as "typically mammalian" above 26 • C and little brown bats usually defend a homeothermic above 32 • C (Stones, 1964), the possibility that bats were in torpor can not be ruled out at these temperatures either given that normal sleep rhythms are present during high temperature torpor bouts in other animals and that bats have been reported to be torpid above 30 • C in the wild (Royo et al, 2019;Amichai et al, 2013).…”