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.
In both human and nonhuman primates (NHP), the medial prefrontal region, defined as the supplementary eye field (SEF), can indirectly influence behavior selection through modulation of the primary selection process in the oculomotor structures. To perform this oculomotor control, SEF integrates multiple cognitive signals such as attention, memory, reward, and error. As changes in pupil responses can assess these cognitive efforts, a better understanding of the precise dynamics by which pupil diameter and medial prefrontal cortex activity interact requires thorough investigations before, during, and after changes in pupil diameter. We tested whether SEF activity is related to pupil dynamics during a mixed pro/antisaccade oculomotor task in 2 macaque monkeys. We used functional ultrasound (fUS) imaging to examine temporal changes in brain activity at the 0.1-s time scale and 0.1-mm spatial resolution concerning behavioral performance and pupil dynamics. By combining the pupil signals and real-time imaging of NHP during cognitive tasks, we were able to infer localized cerebral blood volume (CBV) responses within a restricted part of the dorsomedial prefrontal cortex, referred to as the SEF, an area in which antisaccade preparation activity is also recorded. Inversely, SEF neurovascular activity measured by fUS imaging was found to be a robust predictor of specific variations in pupil diameter over short and long-time scales. Furthermore, we directly manipulated pupil diameter and CBV in the SEF using reward modulations. These results bring a novel understanding of the physiological links between pupil and SEF, but it also raises questions about the role of anterior cingulate cortex (ACC), as CBV variations in the ACC seems to be negligible compared to CBV variations in the SEF.
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