A role for the thalamus in danger evoked awakening during sleep

Ida Luisa Boccalaro, Mattia Aime, Florence Marcelle Aellen, Thomas Rusterholz, Micaela Borsa, Ivan Bozic, Andrea Sattin, Tommaso Fellin, Carolina Gutierrez Herrera, Athina Tzovara and Antoine Adamantidis ()
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Ida Luisa Boccalaro: University of Bern
Mattia Aime: University of Bern
Florence Marcelle Aellen: University of Bern
Thomas Rusterholz: University of Bern
Micaela Borsa: University of Bern
Ivan Bozic: University of Bern
Andrea Sattin: Istituto Italiano di Tecnologia
Tommaso Fellin: Istituto Italiano di Tecnologia
Carolina Gutierrez Herrera: University of Bern
Athina Tzovara: University of Bern
Antoine Adamantidis: University of Bern

Nature Communications, 2025, vol. 16, issue 1, 1-15

Abstract: Abstract Sleep involves a relative disconnection from the environment, yet sensory stimuli can still trigger awakenings. The mechanism underlying sensory vigilance and stimulus discrimination during sleep remains unclear. Here, we showed that neutral auditory stimuli evoked responses across parallel auditory and non-auditory pathways, including the auditory cortex and thalamus, the hippocampus and centro-medial thalamus (CMT). Using a convolutional neural network, we identified CMT activity as the most discriminant hub for auditory-evoked sleep-to-wake transitions among all recorded structures. Furthermore, we found that prior associative learning of auditory cues with danger (conditioned stimulus, CS+) resulted in increased awakening 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 functioning as one of the major hubs for awakening in response to danger.

Date: 2025
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DOI: 10.1038/s41467-025-62265-0

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