IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37974-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37974-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37974-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yung-Tian A. Gau & Eric T. Hsu & Richard J. Cha & Rebecca W. Pak & Loren L. Looger & Jin U. Kang & Dwight E. Bergles, 2024. "Multicore fiber optic imaging reveals that astrocyte calcium activity in the mouse cerebral cortex is modulated by internal motivational state," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    2. Nicole Pogodalla & Holger Kranenburg & Simone Rey & Silke Rodrigues & Albert Cardona & Christian Klämbt, 2021. "Drosophila ßHeavy-Spectrin is required in polarized ensheathing glia that form a diffusion-barrier around the neuropil," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    3. Valentina Botero & Bethany A. Stanhope & Elizabeth B. Brown & Eliza C. Grenci & Tamara Boto & Scarlet J. Park & Lanikea B. King & Keith R. Murphy & Kenneth J. Colodner & James A. Walker & Alex C. Keen, 2021. "Neurofibromin regulates metabolic rate via neuronal mechanisms in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Lan Pang & Zhiguo Liu & Jiani Chen & Zhi Dong & Sicong Zhou & Qichao Zhang & Yueqi Lu & Yifeng Sheng & Xuexin Chen & Jianhua Huang, 2022. "Search performance and octopamine neuronal signaling mediate parasitoid induced changes in Drosophila oviposition behavior," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Laura Bojarskaite & Alexandra Vallet & Daniel M. Bjørnstad & Kristin M. Gullestad Binder & Céline Cunen & Kjell Heuser & Miroslav Kuchta & Kent-Andre Mardal & Rune Enger, 2023. "Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37974-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.