BRAIN-STATE TRANSITIONS DURING BRUMATION

Ectothermic animals can tolerate rapid and profound decreases in body temperature. In reptiles, acute exposure to low temperatures drives the brain into a deeply hypometabolic state, referred to as brumation, within a few hours. However, the cellular state of the brain and the nature of neuronal activity during this transition have remained unclear. In this study, we used the bearded dragon (Pogona vitticeps), a reptile whose circadian rhythms and sleep wake physiology have been well characterized, as a model organism to examine neural and glial responses to acute cooling.
We first assessed changes in arousal threshold and found that behavioral responses to sensory stimuli disappeared at temperatures below 10°C. This indicates that temperatures below 10°C correspond to a behavioral brumation state. We next performed local field potential recordings under controlled temperature conditions. Sleep related neural oscillations were found to be strongly temperature dependent, with the peak frequencies associated with non REM sleep and REM sleep decreasing approximately linearly as temperature declined. Notably, the temperatures at which non REM sleep and REM sleep activity disappeared were distinct.
While neuronal activity transitioned into a quiescent state during brumation,microglia exhibited pronounced activation. Exposure to 4°C for 7 to 12 hours induced marked morphological changes in microglia, and RNA sequencing analysis revealed a shift in transcriptional profiles toward gene programs associated with neuroprotection. Together, these findings demonstrate that under low temperature conditions, neuronal activity is passively suppressed, whereas microglia exhibit changes that may reflect active adaptive responses.