Brain activity regulates loose coupling between mitochondrial and cytosolic Ca2+ transients

Yuan Lin, Lin-Lin Li, Wei Nie, Xiaolei Liu, Avital Adler, Chi Xiao, Fujian Lu, Liping Wang, Hua Han, Xianhua Wang, Wen-Biao Gan () and Heping Cheng ()
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Yuan Lin: Peking University
Lin-Lin Li: Chinese Academy of Sciences
Wei Nie: Peking University
Xiaolei Liu: Chinese Academy of Sciences
Avital Adler: New York University School of Medicine
Chi Xiao: Chinese Academy of Sciences
Fujian Lu: Peking University
Liping Wang: Chinese Academy of Sciences
Hua Han: Chinese Academy of Sciences
Xianhua Wang: Peking University
Wen-Biao Gan: New York University School of Medicine
Heping Cheng: Peking University

Nature Communications, 2019, vol. 10, issue 1, 1-13

Abstract: Abstract Mitochondrial calcium ([Ca2+]mito) dynamics plays vital roles in regulating fundamental cellular and organellar functions including bioenergetics. However, neuronal [Ca2+]mito dynamics in vivo and its regulation by brain activity are largely unknown. By performing two-photon Ca2+ imaging in the primary motor (M1) and visual cortexes (V1) of awake behaving mice, we find that discrete [Ca2+]mito transients occur synchronously over somatic and dendritic mitochondrial network, and couple with cytosolic calcium ([Ca2+]cyto) transients in a probabilistic, rather than deterministic manner. The amplitude, duration, and frequency of [Ca2+]cyto transients constitute important determinants of the coupling, and the coupling fidelity is greatly increased during treadmill running (in M1 neurons) and visual stimulation (in V1 neurons). Moreover, Ca2+/calmodulin kinase II is mechanistically involved in modulating the dynamic coupling process. Thus, activity-dependent dynamic [Ca2+]mito-to-[Ca2+]cyto coupling affords an important mechanism whereby [Ca2+]mito decodes brain activity for the regulation of mitochondrial bioenergetics to meet fluctuating neuronal energy demands as well as for neuronal information processing.

Date: 2019
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DOI: 10.1038/s41467-019-13142-0

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