Distinct astrocytic modulatory roles in sensory transmission during sleep, wakefulness, and arousal states in freely moving mice

• Published in: Nature communications Vol. 14; no. 1; p. 2186
• Main Authors: Wang, Fushun, Wang, Wei, Gu, Simeng, Qi, Dan, Smith, Nathan A., Peng, Weiguo, Dong, Wei, Yuan, Jiajin, Zhao, Binbin, Mao, Ying, Cao, Peng, Lu, Qing Richard, Shapiro, Lee A., Yi, S. Stephen, Wu, Erxi, Huang, Jason H.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 17-04-2023; Nature Publishing Group; Nature Portfolio
• Subjects: 14/34; 14/63; 631/378/1385/1877; 631/378/1385/519; 631/378/2596/1308; 64/60; 9/26; 9/30; 9/74; 9/97; Animals; Arousal; Arousal - physiology; Astrocytes; Astrocytes - physiology; Brain; Calcium ions; Calcium Signaling - physiology; Calcium signalling; Cortex (barrel); Humanities and Social Sciences; Hyperpolarization; Inositol trisphosphate; Inositols; Locus coeruleus; Mice; Modulation; multidisciplinary; Norepinephrine; Science; Science (multidisciplinary); Sensory neurons; Sleep; Sleep and wakefulness; Somatosensory cortex; Synaptic transmission; Wakefulness
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-37974-z

Despite extensive research on astrocytic Ca
2+
in synaptic transmission, its contribution to the modulation of sensory transmission during different brain states remains largely unknown. Here, by using two-photon microscopy and whole-cell recordings, we show two distinct astrocytic Ca
2+
signals in the murine barrel cortex: a small, long-lasting Ca
2+
increase during sleep and a large, widespread but short-lasting Ca
2+
spike when aroused. The large Ca
2+
wave in aroused mice was inositol trisphosphate (IP3)-dependent, evoked by the locus coeruleus-norepinephrine system, and enhanced sensory input, contributing to reliable sensory transmission. However, the small Ca
2+
transient was IP3-independent and contributed to decreased extracellular K
+
, hyperpolarization of the neurons, and suppression of sensory transmission. These events respond to different pharmacological inputs and contribute to distinct sleep and arousal functions by modulating the efficacy of sensory transmission. Together, our data demonstrate an important function for astrocytes in sleep and arousal states via astrocytic Ca
2+
waves.
The contribution of astrocytic Ca
2+
signaling to the modulation of sensory transmission in different brain states remains largely unknown. Here, the authors show two types of Ca
2+
signals in the mouse barrel cortex with distinct function in sensory transmission during sleep and arousal states.