Sub-minute prediction of brain temperature based on sleep–wake state in the mouse

Abstract

Although brain temperature has neurobiological and clinical importance, it remains unclear which factors contribute to its daily dynamics and to what extent. Using a statistical approach, we previously demonstrated that hourly brain temperature values co-varied strongly with time spent awake (Hoekstra et al., 2019). Here we develop and make available a mathematical tool to simulate and predict cortical temperature in mice based on a 4-s sleep–wake sequence. Our model estimated cortical temperature with remarkable precision and accounted for 91% of the variance based on three factors: sleep–wake sequence, time-of-day (‘circadian’), and a novel ‘prior wake prevalence’ factor, contributing with 74%, 9%, and 43%, respectively (including shared variance). We applied these optimized parameters to an independent cohort of mice and predicted cortical temperature with similar accuracy. This model confirms the profound influence of sleep–wake state on brain temperature, and can be harnessed to differentiate between thermoregulatory and sleep–wake-driven effects in experiments affecting both.

Simultaneous CMOS-Based Imaging of Calcium Signaling of the Central Amygdala and the Dorsal Raphe Nucleus During Nociception in Freely Moving Mice

“…Along with the very minute increase in temperature during LED activation, temperature-related necrosis can be said to have not occurred. The relatively low internal body temperature can be attributed to the sleeping state of the recorded mouse ( Sela et al, 2021 ). With the devices’ viability and novel features, many methodology changes can be explored.…”

“…The relatively low internal body temperature can be attributed to the sleeping state of the recorded mouse (Sela et al, 2021). With the devices' viability and novel features, many methodology changes can be explored.…”

Role of the Preoptic Area in Sleep and Thermoregulation

“…In mice and rats, transitions to sleep are accompanied by a decrease in brain and core body temperature ( Obál et al, 1985 ; Alföldi et al, 1990 ; Franken et al, 1992a , b ; Hoekstra et al, 2019 ; Sela et al, 2021 ) suggesting that the brain state drives fluctuations in the body temperature. The brain and cortical temperature during different vigilance states has been further characterized in many mammalian species such as sheep, Djungarian hamsters, and monkeys ( Baker and Hayward, 1968 ; Hayward and Baker, 1968 ; Deboer et al, 1994 ; Blessing, 2018 ).…”

“…Sustained waking induced by sleep deprivation significantly elevated the cortical temperature in mice suggesting a causal relationship between wakefulness and cortical temperature ( Hoekstra et al, 2019 ). Furthermore, a mathematical model used the sleep-wake sequence to simulate and predict the cortical temperature and found a significant influence of the sleep-wake state on brain temperature ( Sela et al, 2021 ). Sleep fragmentation in mice impairs the reduction in brain temperature during sleep and instead resulted in an increase ( Baud et al, 2013 ).…”

The two‐process model of sleep regulation: Beginnings and outlook†

“…Not only sleep deprivation but also spontaneous periods of wakefulness affected the central and peripheral dynamics of this protein. Using brain temperature at high temporal resolution in a state‐of‐the art follow‐up of an early study (Franken et al, 1992), a model was developed that predicted with high accuracy state‐related and long‐term changes, and provided data on the relative contribution of homeostatic and circadian factors (Sela et al, 2021).…”