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Hippocampal astrocytes modulate anxiety-like behavior

Author

Listed:
  • Woo-Hyun Cho

    (Seoul National University School of Dentistry)

  • Kyungchul Noh

    (Seoul National University School of Dentistry)

  • Byung Hun Lee

    (Seoul National University)

  • Ellane Barcelon

    (Seoul National University School of Dentistry)

  • Sang Beom Jun

    (Ewha Womans University
    Ewha Womans University
    Ewha Womans University)

  • Hye Yoon Park

    (Seoul National University
    University of Minnesota)

  • Sung Joong Lee

    (Seoul National University School of Dentistry)

Abstract

Astrocytes can affect animal behavior by regulating tripartite synaptic transmission, yet their influence on affective behavior remains largely unclear. Here we showed that hippocampal astrocyte calcium activity reflects mouse affective state during virtual elevated plus maze test using two-photon calcium imaging in vivo. Furthermore, optogenetic hippocampal astrocyte activation elevating intracellular calcium induced anxiolytic behaviors in astrocyte-specific channelrhodopsin 2 (ChR2) transgenic mice (hGFAP-ChR2 mice). As underlying mechanisms, we found ATP released from the activated hippocampal astrocytes increased excitatory synaptic transmission in dentate gyrus (DG) granule cells, which exerted anxiolytic effects. Our data uncover a role of hippocampal astrocytes in modulating mice anxiety-like behaviors by regulating ATP-mediated synaptic homeostasis in hippocampal DG granule cells. Thus, manipulating hippocampal astrocytes activity can be a therapeutic strategy to treat anxiety.

Suggested Citation

  • Woo-Hyun Cho & Kyungchul Noh & Byung Hun Lee & Ellane Barcelon & Sang Beom Jun & Hye Yoon Park & Sung Joong Lee, 2022. "Hippocampal astrocytes modulate anxiety-like behavior," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34201-z
    DOI: 10.1038/s41467-022-34201-z
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    1. J. A. Gomez & J. M. Perkins & G. M. Beaudoin & N. B. Cook & S. A. Quraishi & E. A. Szoeke & K. Thangamani & C. W. Tschumi & M. J. Wanat & A. M. Maroof & M. J. Beckstead & P. A. Rosenberg & C. A. Palad, 2019. "Ventral tegmental area astrocytes orchestrate avoidance and approach behavior," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Christian Henneberger & Thomas Papouin & Stéphane H. R. Oliet & Dmitri A. Rusakov, 2010. "Long-term potentiation depends on release of d-serine from astrocytes," Nature, Nature, vol. 463(7278), pages 232-236, January.
    3. Gertrudis Perea & Aimei Yang & Edward S. Boyden & Mriganka Sur, 2014. "Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo," Nature Communications, Nature, vol. 5(1), pages 1-12, May.
    4. Giselle Cheung & Danijela Bataveljic & Josien Visser & Naresh Kumar & Julien Moulard & Glenn Dallérac & Daria Mozheiko & Astrid Rollenhagen & Pascal Ezan & Cédric Mongin & Oana Chever & Alexis-Pierre , 2022. "Physiological synaptic activity and recognition memory require astroglial glutamine," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Thomas Hainmueller & Marlene Bartos, 2018. "Parallel emergence of stable and dynamic memory engrams in the hippocampus," Nature, Nature, vol. 558(7709), pages 292-296, June.
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