Distinct temporal integration of noradrenaline signaling by astrocytic second messengers during vigilance

Yuki Oe (), Xiaowen Wang, Tommaso Patriarchi, Ayumu Konno, Katsuya Ozawa, Kazuko Yahagi, Hirokazu Hirai, Takashi Tsuboi, Tetsuya Kitaguchi, Lin Tian, Thomas J. McHugh and Hajime Hirase ()
Additional contact information
Yuki Oe: RIKEN Center for Brain Science
Xiaowen Wang: RIKEN Center for Brain Science
Tommaso Patriarchi: University of California
Ayumu Konno: Gunma University Initiative for Advanced Research
Katsuya Ozawa: RIKEN Center for Brain Science
Kazuko Yahagi: RIKEN Center for Brain Science
Hirokazu Hirai: Gunma University Initiative for Advanced Research
Takashi Tsuboi: The University of Tokyo, 3-8-1 Komaba
Tetsuya Kitaguchi: Institute of Innovative Research, Tokyo Institute of Technology, 4259 Nagatsuta-cho, Midori-ku
Lin Tian: University of California
Thomas J. McHugh: RIKEN Center for Brain Science
Hajime Hirase: RIKEN Center for Brain Science

Nature Communications, 2020, vol. 11, issue 1, 1-15

Abstract: Abstract Astrocytes may function as mediators of the impact of noradrenaline on neuronal function. Activation of glial α1-adrenergic receptors triggers rapid astrocytic Ca2+ elevation and facilitates synaptic plasticity, while activation of β-adrenergic receptors elevates cAMP levels and modulates memory consolidation. However, the dynamics of these processes in behaving mice remain unexplored, as do the interactions between the distinct second messenger pathways. Here we simultaneously monitored astrocytic Ca2+ and cAMP and demonstrate that astrocytic second messengers are regulated in a temporally distinct manner. In behaving mice, we found that while an abrupt facial air puff triggered transient increases in noradrenaline release and large cytosolic astrocytic Ca2+ elevations, cAMP changes were not detectable. By contrast, repeated aversive stimuli that lead to prolonged periods of vigilance were accompanied by robust noradrenergic axonal activity and gradual sustained cAMP increases. Our findings suggest distinct astrocytic signaling pathways can integrate noradrenergic activity during vigilance states to mediate distinct functions supporting memory.

Date: 2020
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DOI: 10.1038/s41467-020-14378-x

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