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

Author

Listed:
  • Fushun Wang

    (Sichuan Normal University
    University of Rochester)

  • Wei Wang

    (Sichuan Normal University
    Boston University)

  • Simeng Gu

    (Sichuan Normal University
    Jiangsu University Medical School)

  • Dan Qi

    (Baylor Scott & White Health)

  • Nathan A. Smith

    (University of Rochester
    George Washington University School of Medicine and Health Sciences
    Center for Neuroscience Research, Children’s National Research Institute, Children’s National Hospital)

  • 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
    University of Cincinnati College of Medicine)

  • Lee A. Shapiro

    (Texas A&M University)

  • S. Stephen Yi

    (The University of Texas at Austin
    The University of Texas at Austin
    The University of Texas at Austin)

  • Erxi Wu

    (Baylor Scott & White Health
    The University of Texas at Austin
    Texas A & M University Health Science Center)

  • Jason H. Huang

    (Baylor Scott & White Health
    Texas A & M University Health Science Center
    Baylor College of Medicine)

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.

Suggested Citation

  • 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 & , 2023. "Distinct astrocytic modulatory roles in sensory transmission during sleep, wakefulness, and arousal states in freely moving mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37974-z
    DOI: 10.1038/s41467-023-37974-z
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    References listed on IDEAS

    as
    1. Zhiguo Ma & Tobias Stork & Dwight E. Bergles & Marc R. Freeman, 2016. "Neuromodulators signal through astrocytes to alter neural circuit activity and behaviour," Nature, Nature, vol. 539(7629), pages 428-432, November.
    2. Laura Bojarskaite & Daniel M. Bjørnstad & Klas H. Pettersen & Céline Cunen & Gudmund Horn Hermansen & Knut Sindre Åbjørsbråten & Anna R. Chambers & Rolf Sprengel & Koen Vervaeke & Wannan Tang & Rune E, 2020. "Astrocytic Ca2+ signaling is reduced during sleep and is involved in the regulation of slow wave sleep," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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