Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle

Ben Collins; Sara Pierre-Ferrer; Christine Muheim; David Lukacsovich; Yuchen Cai; Andrea Spinnler; Carolina Gutierrez Herrera; Shao'Ang Wen; Jochen Winterer; Mino D C Belle; Hugh D Piggins; Michael Hastings; Andrew Loudon; Jun Yan; Csaba Földy; Antoine Adamantidis; Steven A Brown

doi:10.1016/j.neuron.2020.08.001

Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle

Ben Collins, Sara Pierre-Ferrer, Christine Muheim, David Lukacsovich, Yuchen Cai, Andrea Spinnler, Carolina Gutierrez Herrera, Shao'Ang Wen, Jochen Winterer, Mino D C Belle, Hugh D Piggins, Michael Hastings, Andrew Loudon, Jun Yan, Csaba Földy, Antoine Adamantidis, Steven A Brown

Research output: Contribution to journal › Article › peer-review

Abstract

Although the mammalian rest-activity cycle is controlled by a "master clock" in the suprachiasmatic nucleus (SCN) of the hypothalamus, it is unclear how firing of individual SCN neurons gates individual features of daily activity. Here, we demonstrate that a specific transcriptomically identified population of mouse VIP+ SCN neurons is active at the "wrong" time of day-nighttime-when most SCN neurons are silent. Using chemogenetic and optogenetic strategies, we show that these neurons and their cellular clocks are necessary and sufficient to gate and time nighttime sleep but have no effect upon daytime sleep. We propose that mouse nighttime sleep, analogous to the human siesta, is a "hard-wired" property gated by specific neurons of the master clock to favor subsequent alertness prior to dawn (a circadian "wake maintenance zone"). Thus, the SCN is not simply a 24-h metronome: specific populations sculpt critical features of the sleep-wake cycle.

Original language	English
Pages (from-to)	486-499.e5
Number of pages	19
Journal	Neuron
Volume	108
Issue number	3
Early online date	10 Sept 2020
DOIs	https://doi.org/10.1016/j.neuron.2020.08.001
Publication status	Published - 11 Nov 2020

Keywords

Animals
Circadian Rhythm/physiology
Male
Mice
Sleep/physiology
Suprachiasmatic Nucleus Neurons/physiology
Vasoactive Intestinal Peptide/metabolism

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10.1016/j.neuron.2020.08.001

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Collins, B., Pierre-Ferrer, S., Muheim, C., Lukacsovich, D., Cai, Y., Spinnler, A., Herrera, C. G., Wen, SA., Winterer, J., Belle, M. D. C., Piggins, H. D., Hastings, M., Loudon, A., Yan, J., Földy, C., Adamantidis, A., & Brown, S. A. (2020). Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle. Neuron, 108(3), 486-499.e5. https://doi.org/10.1016/j.neuron.2020.08.001

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abstract = "Although the mammalian rest-activity cycle is controlled by a {"}master clock{"} in the suprachiasmatic nucleus (SCN) of the hypothalamus, it is unclear how firing of individual SCN neurons gates individual features of daily activity. Here, we demonstrate that a specific transcriptomically identified population of mouse VIP+ SCN neurons is active at the {"}wrong{"} time of day-nighttime-when most SCN neurons are silent. Using chemogenetic and optogenetic strategies, we show that these neurons and their cellular clocks are necessary and sufficient to gate and time nighttime sleep but have no effect upon daytime sleep. We propose that mouse nighttime sleep, analogous to the human siesta, is a {"}hard-wired{"} property gated by specific neurons of the master clock to favor subsequent alertness prior to dawn (a circadian {"}wake maintenance zone{"}). Thus, the SCN is not simply a 24-h metronome: specific populations sculpt critical features of the sleep-wake cycle.",

keywords = "Animals, Circadian Rhythm/physiology, Male, Mice, Sleep/physiology, Suprachiasmatic Nucleus Neurons/physiology, Vasoactive Intestinal Peptide/metabolism",

author = "Ben Collins and Sara Pierre-Ferrer and Christine Muheim and David Lukacsovich and Yuchen Cai and Andrea Spinnler and Herrera, {Carolina Gutierrez} and Shao'Ang Wen and Jochen Winterer and Belle, {Mino D C} and Piggins, {Hugh D} and Michael Hastings and Andrew Loudon and Jun Yan and Csaba F{\"o}ldy and Antoine Adamantidis and Brown, {Steven A}",

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doi = "10.1016/j.neuron.2020.08.001",

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Collins, B, Pierre-Ferrer, S, Muheim, C, Lukacsovich, D, Cai, Y, Spinnler, A, Herrera, CG, Wen, SA, Winterer, J, Belle, MDC , Piggins, HD, Hastings, M, Loudon, A, Yan, J, Földy, C, Adamantidis, A & Brown, SA 2020, 'Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle', Neuron, vol. 108, no. 3, pp. 486-499.e5. https://doi.org/10.1016/j.neuron.2020.08.001

TY - JOUR

T1 - Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle

AU - Collins, Ben

AU - Pierre-Ferrer, Sara

AU - Muheim, Christine

AU - Lukacsovich, David

AU - Cai, Yuchen

AU - Spinnler, Andrea

AU - Herrera, Carolina Gutierrez

AU - Wen, Shao'Ang

AU - Winterer, Jochen

AU - Belle, Mino D C

AU - Piggins, Hugh D

AU - Hastings, Michael

AU - Loudon, Andrew

AU - Yan, Jun

AU - Földy, Csaba

AU - Adamantidis, Antoine

AU - Brown, Steven A

PY - 2020/11/11

Y1 - 2020/11/11

N2 - Although the mammalian rest-activity cycle is controlled by a "master clock" in the suprachiasmatic nucleus (SCN) of the hypothalamus, it is unclear how firing of individual SCN neurons gates individual features of daily activity. Here, we demonstrate that a specific transcriptomically identified population of mouse VIP+ SCN neurons is active at the "wrong" time of day-nighttime-when most SCN neurons are silent. Using chemogenetic and optogenetic strategies, we show that these neurons and their cellular clocks are necessary and sufficient to gate and time nighttime sleep but have no effect upon daytime sleep. We propose that mouse nighttime sleep, analogous to the human siesta, is a "hard-wired" property gated by specific neurons of the master clock to favor subsequent alertness prior to dawn (a circadian "wake maintenance zone"). Thus, the SCN is not simply a 24-h metronome: specific populations sculpt critical features of the sleep-wake cycle.

AB - Although the mammalian rest-activity cycle is controlled by a "master clock" in the suprachiasmatic nucleus (SCN) of the hypothalamus, it is unclear how firing of individual SCN neurons gates individual features of daily activity. Here, we demonstrate that a specific transcriptomically identified population of mouse VIP+ SCN neurons is active at the "wrong" time of day-nighttime-when most SCN neurons are silent. Using chemogenetic and optogenetic strategies, we show that these neurons and their cellular clocks are necessary and sufficient to gate and time nighttime sleep but have no effect upon daytime sleep. We propose that mouse nighttime sleep, analogous to the human siesta, is a "hard-wired" property gated by specific neurons of the master clock to favor subsequent alertness prior to dawn (a circadian "wake maintenance zone"). Thus, the SCN is not simply a 24-h metronome: specific populations sculpt critical features of the sleep-wake cycle.

KW - Animals

KW - Circadian Rhythm/physiology

KW - Male

KW - Mice

KW - Sleep/physiology

KW - Suprachiasmatic Nucleus Neurons/physiology

KW - Vasoactive Intestinal Peptide/metabolism

U2 - 10.1016/j.neuron.2020.08.001

DO - 10.1016/j.neuron.2020.08.001

M3 - Article

C2 - 32916091

SN - 0896-6273

VL - 108

SP - 486-499.e5

JO - Neuron

JF - Neuron

IS - 3

ER -

Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle

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Keywords

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