Basal forebrain thermoregulatory mechanism modulates auto-regulated sleep

Abstract

Regulation of body temperature and sleep are two physiological mechanisms that are vital for our survival. Interestingly neural structures implicated in both these functions are common. These areas include the medial preoptic area (POA), the lateral POA, the ventrolateral POA, the median preoptic nucleus, and the medial septum, which form part of the basal forebrain (BF). When given a choice, rats prefer to stay at an ambient temperature of 27°C, though the maximum sleep was observed when they were placed at 30°C. Ambient temperature around 27°C should be considered as the thermoneutral temperature for rats in all sleep studies. At this temperature the diurnal oscillations of sleep and body temperature are properly expressed. The warm sensitive neurons of the POA mediate the increase in sleep at 30°C. Promotion of sleep during the rise in ambient temperature from 27 to 30°C, serve a thermoregulatory function. Autonomous thermoregulatory changes in core body temperature and skin temperature could act as an input signal to modulate neuronal activity in sleep-promoting brain areas. The studies presented here show that the neurons of the BF play a key role in regulating sleep. BF thermoregulatory system is a part of the global homeostatic sleep regulatory mechanism, which is auto-regulated.

Keywords: ambient temperature; basal forebrain; preoptic area; sleep; thermal preference; thermoneutral zone; thermoreceptors; thermoregulation.

Figure 1

Schematic diagram of environmental chamber having three different ambient temperature (18, 30, and 33°C) in the three interconnected compartments.

Figure 2

Sleep-wake stages (bar diagram) and body temperature (line diagram) in 2 h bin at 27 and 30°C ambient temperature. Sleep parameters and body temperature recording for 6 h (11:00–17:00 hours) at 27 and 30°C was preceded by 2 h baseline recording (9:00–11:00 hours) at 27°C. X-axis shows the time of the day. Y-axis shows percentage time (mean ± SD) of recordings (bar diagram) in sleep-wakefulness and body temperature (line diagram). *p < 0.05, **p < 0.01, shows significance of change in each 2 h (11:00–13:00, 13:00–15:00, and 15:00–17:00 hours) compared to baseline (9:00–11:00 hours) data. ▴p < 0.05, shows significance of change in three 2 h bin (11:00–13:00, 13:00–15:00, and 15:00–17:00 hours) at 30°C compared to time matched bin of 27°C.

Figure 3

Rapid eye movement sleep and slow wave sleep (% mean ± SD) at different ambient temperature in rats before and after destruction of (A) peripheral and central warm receptors, (B) only peripheral warm receptors, and (C) only preoptic warm sensitive neurons. *p < 0.05, significance of change at different ambient temperature compared with 27°C. †p < 0.05, significance of change at different ambient temperature compared with 18°C ⁺p < 0.05, ‡p < 0.01, significance of change between before and after destruction.