Slow-wave sleep is controlled by a subset of nucleus accumbens core neurons in mice

Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep–wake behaviour; however, the precise circuit mechanisms underlying their effe...

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Published inNature communications Vol. 8; no. 8; pp. 734 - 12
Main Authors 裏出 良博, LAZARUS MICHAEL, Oishi Yo, Xu Qi, Wang Lu, Zhang Bin-Jia, Takahashi Koji, Takata Yohko, Luo Yan-Jia, Cherasse Yoan, Schiffmann Serge N., de Kerchove d'Exaerde Alban, Urade Yoshihiro, Qu Wei-Min, Huang Zhi-Li, Lazarus Michael
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group 29.09.2017
Nature Publishing Group UK
Nature Portfolio
Subjects
631/378/1385/1814
631/378/1385/2641
631/378/1385/519
631/378/1662
631/378/3920
Adenosine
Animals
Arousal
Brain
Circadian Rhythm
Circadian rhythms
Cognitive ability
Emotional factors
Female
Humanities and Social Sciences
Inhibition (psychology)
Male
Mice
Mice, Inbred C57BL
Motivation
multidisciplinary
Neurons
Nuclei
Nucleus accumbens
Nucleus Accumbens - physiology
Pallidum (ventral)
Patch-Clamp Techniques
Proto-Oncogene Proteins c-fos - metabolism
Receptor, Adenosine A2A - metabolism
Receptor, Adenosine A2A - physiology
Reinforcement
Rodents
Science
Science (multidisciplinary)
Sleep
Sleep - physiology
Sleep and wakefulness
Stimuli
Online AccessGet full text

Cover

Abstract Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep–wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A2A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation.
AbstractList Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep-wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A2A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation.In addition to circadian and homoeostatic drives, motivational levels influence sleep-wake cycles. Here the authors demonstrate that adenosine receptor-expressing neurons in the nucleus accumbens core that project to the ventral pallidum are inhibited by motivational stimuli and are causally involved in the control of slow-wave sleep.Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep-wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A2A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation.In addition to circadian and homoeostatic drives, motivational levels influence sleep-wake cycles. Here the authors demonstrate that adenosine receptor-expressing neurons in the nucleus accumbens core that project to the ventral pallidum are inhibited by motivational stimuli and are causally involved in the control of slow-wave sleep.
Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep–wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A2A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation.
Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep–wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A 2A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation. In addition to circadian and homoeostatic drives, motivational levels influence sleep−wake cycles. Here the authors demonstrate that adenosine receptor-expressing neurons in the nucleus accumbens core that project to the ventral pallidum are inhibited by motivational stimuli and are causally involved in the control of slow-wave sleep.
In addition to circadian and homoeostatic drives, motivational levels influence sleep−wake cycles. Here the authors demonstrate that adenosine receptor-expressing neurons in the nucleus accumbens core that project to the ventral pallidum are inhibited by motivational stimuli and are causally involved in the control of slow-wave sleep.
Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep-wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation.In addition to circadian and homoeostatic drives, motivational levels influence sleep-wake cycles. Here the authors demonstrate that adenosine receptor-expressing neurons in the nucleus accumbens core that project to the ventral pallidum are inhibited by motivational stimuli and are causally involved in the control of slow-wave sleep.
Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major sleep-regulating factors. Cognitive and emotional factors also influence sleep–wake behaviour; however, the precise circuit mechanisms underlying their effects on sleep control are unknown. Previous studies suggest that adenosine has a role affecting behavioural arousal in the nucleus accumbens (NAc), a brain area critical for reinforcement and reward. Here, we show that chemogenetic or optogenetic activation of excitatory adenosine A 2A receptor-expressing indirect pathway neurons in the core region of the NAc strongly induces slow-wave sleep. Chemogenetic inhibition of the NAc indirect pathway neurons prevents the sleep induction, but does not affect the homoeostatic sleep rebound. In addition, motivational stimuli inhibit the activity of ventral pallidum-projecting NAc indirect pathway neurons and suppress sleep. Our findings reveal a prominent contribution of this indirect pathway to sleep control associated with motivation.
ArticleNumber 734
Author LAZARUS MICHAEL
Cherasse Yoan
Schiffmann Serge N.
Zhang Bin-Jia
Wang Lu
Takata Yohko
Oishi Yo
Takahashi Koji
Huang Zhi-Li
裏出 良博
Xu Qi
Luo Yan-Jia
de Kerchove d'Exaerde Alban
Qu Wei-Min
Urade Yoshihiro
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  fullname: Xu Qi
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  fullname: Zhang Bin-Jia
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  fullname: Takahashi Koji
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https://www.ncbi.nlm.nih.gov/pubmed/28963505$$D View this record in MEDLINE/PubMed
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Snippet Sleep control is ascribed to a two-process model, a widely accepted concept that posits homoeostatic drive and a circadian process as the major...
In addition to circadian and homoeostatic drives, motivational levels influence sleep−wake cycles. Here the authors demonstrate that adenosine...
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SubjectTerms 631/378/1385/1814
631/378/1385/2641
631/378/1385/519
631/378/1662
631/378/3920
Adenosine
Animals
Arousal
Brain
Circadian Rhythm
Circadian rhythms
Cognitive ability
Emotional factors
Female
Humanities and Social Sciences
Inhibition (psychology)
Male
Mice
Mice, Inbred C57BL
Motivation
multidisciplinary
Neurons
Nuclei
Nucleus accumbens
Nucleus Accumbens - physiology
Pallidum (ventral)
Patch-Clamp Techniques
Proto-Oncogene Proteins c-fos - metabolism
Receptor, Adenosine A2A - metabolism
Receptor, Adenosine A2A - physiology
Reinforcement
Rodents
Science
Science (multidisciplinary)
Sleep
Sleep - physiology
Sleep and wakefulness
Stimuli
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Title Slow-wave sleep is controlled by a subset of nucleus accumbens core neurons in mice
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Volume 8
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