A distributed auditory network mediated by pontine central gray underlies ultra-fast awakening in response to alerting sounds.

alert arousal ascending auditory pathway auditory processing auditory thalamus awakening brainstem pons sensory response sleep/wake cycle

Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
07 Sep 2024
Historique:
received: 11 03 2024
revised: 12 07 2024
accepted: 13 08 2024
medline: 13 9 2024
pubmed: 13 9 2024
entrez: 12 9 2024
Statut: aheadofprint

Résumé

Sleeping animals can be woken up rapidly by external threat signals, which is an essential defense mechanism for survival. However, neuronal circuits underlying the fast transmission of sensory signals for this process remain unclear. Here, we report in mice that alerting sound can induce rapid awakening within hundreds of milliseconds and that glutamatergic neurons in the pontine central gray (PCG) play an important role in this process. These neurons exhibit higher sensitivity to auditory stimuli in sleep than wakefulness. Suppressing these neurons results in reduced sound-induced awakening and increased sleep in intrinsic sleep/wake cycles, whereas their activation induces ultra-fast awakening from sleep and accelerates awakening from anesthesia. Additionally, the sound-induced awakening can be attributed to the propagation of auditory signals from the PCG to multiple arousal-related regions, including the mediodorsal thalamus, lateral hypothalamus, and ventral tegmental area. Thus, the PCG serves as an essential distribution center to orchestrate a global auditory network to promote rapid awakening.

Identifiants

pubmed: 39265569
pii: S0960-9822(24)01132-1
doi: 10.1016/j.cub.2024.08.020
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Jinxing Wei (J)

Zilkha Neurogenetic Institute, Center for Neural Circuits and Sensory Processing Disorders, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.

Cuiyu Xiao (C)

Zilkha Neurogenetic Institute, Center for Neural Circuits and Sensory Processing Disorders, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.

Guang-Wei Zhang (GW)

Zilkha Neurogenetic Institute, Center for Neural Circuits and Sensory Processing Disorders, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA; Department of Physiology and Neuroscience, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.

Li Shen (L)

Zilkha Neurogenetic Institute, Center for Neural Circuits and Sensory Processing Disorders, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.

Huizhong W Tao (HW)

Zilkha Neurogenetic Institute, Center for Neural Circuits and Sensory Processing Disorders, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA; Department of Physiology and Neuroscience, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA. Electronic address: htao@usc.edu.

Li I Zhang (LI)

Zilkha Neurogenetic Institute, Center for Neural Circuits and Sensory Processing Disorders, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA; Department of Physiology and Neuroscience, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA. Electronic address: liizhang@usc.edu.

Classifications MeSH