Distinct astrocytic modulatory roles in sensory transmission during sleep, wakefulness, and arousal states in freely moving mice

Fushun Wang (), Wei Wang, Simeng Gu, Dan Qi, Nathan A. Smith, Weiguo Peng, Wei Dong, Jiajin Yuan, Binbin Zhao, Ying Mao, Peng Cao, Qing Richard Lu, Lee A. Shapiro (), S. Stephen Yi (), Erxi Wu () and Jason H. Huang ()
Additional contact information
Fushun Wang: Sichuan Normal University
Wei Wang: Sichuan Normal University
Simeng Gu: Sichuan Normal University
Dan Qi: Baylor Scott & White Health
Nathan A. Smith: University of Rochester
Weiguo Peng: Sichuan Normal University
Wei Dong: Southwest Medical University
Jiajin Yuan: University of Rochester
Binbin Zhao: Hubei University of Chinese Medicine
Ying Mao: Fudan University
Peng Cao: Nanjing University of Chinese Medicine
Qing Richard Lu: Brain Tumor Center, Division of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center
Lee A. Shapiro: Texas A&M University
S. Stephen Yi: The University of Texas at Austin
Erxi Wu: Baylor Scott & White Health
Jason H. Huang: Baylor Scott & White Health

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Despite extensive research on astrocytic Ca2+ in synaptic transmission, its contribution to the modulation of sensory transmission during different brain states remains largely unknown. Here, by using two-photon microscopy and whole-cell recordings, we show two distinct astrocytic Ca2+ signals in the murine barrel cortex: a small, long-lasting Ca2+ increase during sleep and a large, widespread but short-lasting Ca2+ spike when aroused. The large Ca2+ wave in aroused mice was inositol trisphosphate (IP3)-dependent, evoked by the locus coeruleus-norepinephrine system, and enhanced sensory input, contributing to reliable sensory transmission. However, the small Ca2+ transient was IP3-independent and contributed to decreased extracellular K+, hyperpolarization of the neurons, and suppression of sensory transmission. These events respond to different pharmacological inputs and contribute to distinct sleep and arousal functions by modulating the efficacy of sensory transmission. Together, our data demonstrate an important function for astrocytes in sleep and arousal states via astrocytic Ca2+ waves.

Date: 2023
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DOI: 10.1038/s41467-023-37974-z

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