Astrocytic chloride is brain state dependent and modulates inhibitory neurotransmission in mice

Verena Untiet (), Felix R. M. Beinlich, Peter Kusk, Ning Kang, Antonio Ladrón- de-Guevara, Wei Song, Celia Kjaerby, Mie Andersen, Natalie Hauglund, Zuzanna Bojarowska, Björn Sigurdsson, Saiyue Deng, Hajime Hirase, Nicolas C. Petersen, Alexei Verkhratsky () and Maiken Nedergaard ()
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Verena Untiet: University of Copenhagen
Felix R. M. Beinlich: University of Copenhagen
Peter Kusk: University of Copenhagen
Ning Kang: University of Rochester Medical Center
Antonio Ladrón- de-Guevara: University of Rochester Medical Center
Wei Song: University of Rochester Medical Center
Celia Kjaerby: University of Copenhagen
Mie Andersen: University of Copenhagen
Natalie Hauglund: University of Copenhagen
Zuzanna Bojarowska: University of Copenhagen
Björn Sigurdsson: University of Copenhagen
Saiyue Deng: Huazhong University of Science and Technology
Hajime Hirase: University of Copenhagen
Nicolas C. Petersen: University of Copenhagen
Alexei Verkhratsky: University of Copenhagen
Maiken Nedergaard: University of Copenhagen

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

Abstract: Abstract Information transfer within neuronal circuits depends on the balance and recurrent activity of excitatory and inhibitory neurotransmission. Chloride (Cl−) is the major central nervous system (CNS) anion mediating inhibitory neurotransmission. Astrocytes are key homoeostatic glial cells populating the CNS, although the role of these cells in regulating excitatory-inhibitory balance remains unexplored. Here we show that astrocytes act as a dynamic Cl− reservoir regulating Cl− homoeostasis in the CNS. We found that intracellular chloride concentration ([Cl−]i) in astrocytes is high and stable during sleep. In awake mice astrocytic [Cl−]i is lower and exhibits large fluctuation in response to both sensory input and motor activity. Optogenetic manipulation of astrocytic [Cl−]i directly modulates neuronal activity during locomotion or whisker stimulation. Astrocytes thus serve as a dynamic source of extracellular Cl− available for GABAergic transmission in awake mice, which represents a mechanism for modulation of the inhibitory tone during sustained neuronal activity.

Date: 2023
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DOI: 10.1038/s41467-023-37433-9

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