A role for the thalamus in danger discrimination during sleep

Abstract

Sleep is associated with a sensory disconnection from the environment despite a high vulnerability to danger and predation. Yet, sensory stimuli-evoked responses persist in the brain of flies1, rodents2,3, primates4,5, and humans6,7 during sleep. Whether discrimination between sensory stimuli occurs in the mammalian brain during sleep remains unclear. Here, we showed that neutral auditory stimuli evoked electrical responses propagate in parallel auditory and non-auditory pathway, some of which awaken sleeping mice. We used a convolutional neural network and identified neural activities of centro-medial thalamic (CMT) neurons as the most discriminant hub for auditory-evoked sleep-to-wake transitions among all recorded structures. Importantly, we found that prior associative learning of danger (conditioned stimulus, CS+) and neutral (CS-) auditory cues resulted in increased awakening events upon CS+ exposure during NREM, but not REM, sleep. These sleep-to-wake transitions were blocked by optogenetic silencing of CMT neurons during CS exposure in sleeping mice. Altogether, these results suggest a central role of the CMT neurons in the residual processing of behaviorally-relevant information in the sleeping brain.