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A role for the thalamus in danger evoked awakening during sleep

Author

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  • Ida Luisa Boccalaro

    (University of Bern
    University of Bern
    Harvard Medical School)

  • Mattia Aime

    (University of Bern
    University of Bern)

  • Florence Marcelle Aellen

    (University of Bern
    University of Bern)

  • Thomas Rusterholz

    (University of Bern
    University of Bern)

  • Micaela Borsa

    (University of Bern
    University of Bern)

  • Ivan Bozic

    (University of Bern
    University of Bern)

  • Andrea Sattin

    (Istituto Italiano di Tecnologia)

  • Tommaso Fellin

    (Istituto Italiano di Tecnologia)

  • Carolina Gutierrez Herrera

    (University of Bern
    University of Bern)

  • Athina Tzovara

    (University of Bern
    University of Bern)

  • Antoine Adamantidis

    (University of Bern
    University of Bern)

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.

Suggested Citation

  • Ida Luisa Boccalaro & Mattia Aime & Florence Marcelle Aellen & Thomas Rusterholz & Micaela Borsa & Ivan Bozic & Andrea Sattin & Tommaso Fellin & Carolina Gutierrez Herrera & Athina Tzovara & Antoine A, 2025. "A role for the thalamus in danger evoked awakening during sleep," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-62265-0
    DOI: 10.1038/s41467-025-62265-0
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    References listed on IDEAS

    as
    1. Amanda L. Schott & Justin Baik & Shinjae Chung & Franz Weber, 2023. "A medullary hub for controlling REM sleep and pontine waves," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Mojtaba Bandarabadi & Carolina Gutierrez Herrera & Thomas C. Gent & Claudio Bassetti & Kaspar Schindler & Antoine R. Adamantidis, 2020. "A role for spindles in the onset of rapid eye movement sleep," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    3. Mario A. Penzo & Vincent Robert & Jason Tucciarone & Dimitri De Bundel & Minghui Wang & Linda Van Aelst & Martin Darvas & Luis F. Parada & Richard D. Palmiter & Miao He & Z. Josh Huang & Bo Li, 2015. "The paraventricular thalamus controls a central amygdala fear circuit," Nature, Nature, vol. 519(7544), pages 455-459, March.
    4. Fabricio H. Do-Monte & Kelvin Quiñones-Laracuente & Gregory J. Quirk, 2015. "A temporal shift in the circuits mediating retrieval of fear memory," Nature, Nature, vol. 519(7544), pages 460-463, March.
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