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Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons

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  • Zhibing Tan

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine
    Institute of Neuroscience and Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences)

  • Yu Liu

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine)

  • Wang Xi

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine)

  • Hui-fang Lou

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine)

  • Liya Zhu

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine)

  • Zhifei Guo

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine)

  • Lin Mei

    (Medical College of Georgia, Augusta University)

  • Shumin Duan

    (Key Laboratory of Medical Neurobiology of The Ministry of Health of China, Key Laboratory of Neurobiology of Zhejiang Province, Zhejiang University School of Medicine)

Abstract

Astrocyte responds to neuronal activity with calcium waves and modulates synaptic transmission through the release of gliotransmitters. However, little is known about the direct effect of gliotransmitters on the excitability of neuronal networks beyond synapses. Here we show that selective stimulation of astrocytes expressing channelrhodopsin-2 in the CA1 area specifically increases the firing frequency of CCK-positive but not parvalbumin-positive interneurons and decreases the firing rate of pyramidal neurons, phenomena mimicked by exogenously applied ATP. Further evidences indicate that ATP-induced increase and decrease of excitability are caused, respectively, by P2Y1 receptor-mediated inhibition of a two-pore domain potassium channel and A1 receptor-mediated opening of a G-protein-coupled inwardly rectifying potassium channel. Moreover, the activation of ChR2-expressing astrocytes reduces the power of kainate-induced hippocampal ex vivo gamma oscillation. Thus, through distinct receptor subtypes coupled with different K+ channels, astrocyte-derived ATP differentially modulates the excitability of different types of neurons and efficiently controls the activity of neuronal network.

Suggested Citation

  • Zhibing Tan & Yu Liu & Wang Xi & Hui-fang Lou & Liya Zhu & Zhifei Guo & Lin Mei & Shumin Duan, 2017. "Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons," Nature Communications, Nature, vol. 8(1), pages 1-14, April.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms13772
    DOI: 10.1038/ncomms13772
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    Cited by:

    1. Junli Zhao & Jinyi Sun & Yang Zheng & Yanrong Zheng & Yuying Shao & Yulan Li & Fan Fei & Cenglin Xu & Xiuxiu Liu & Shuang Wang & Yeping Ruan & Jinggen Liu & Shumin Duan & Zhong Chen & Yi Wang, 2022. "Activated astrocytes attenuate neocortical seizures in rodent models through driving Na+-K+-ATPase," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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