Nucleus accumbens controls wakefulness by a subpopulation of neurons expressing dopamine D1 receptors

Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D 1 receptor (D 1 R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arou...

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Published inNature communications Vol. 9; no. 1; pp. 1 - 17
Main Authors Luo, Yan-Jia, Li, Ya-Dong, Wang, Lu, Yang, Su-Rong, Yuan, Xiang-Shan, Wang, Juan, Cherasse, Yoan, Lazarus, Michael, Chen, Jiang-Fan, Qu, Wei-Min, Huang, Zhi-Li
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 20.04.2018
Nature Publishing Group
Nature Portfolio
Subjects
13/1
13/51
14/19
14/28
14/34
14/63
38/88
631/378/1385/1877
631/378/3920
64/110
9/26
9/74
Animal behavior
Arousal
Dopamine
Dopamine D1 receptors
Electron microscopy
Eye movements
Food intake
Humanities and Social Sciences
Hypothalamus
Hypothalamus (lateral)
Immunohistochemistry
Mesencephalon
multidisciplinary
Neurons
NREM sleep
Nuclei
Nucleus accumbens
Orexins
Photoactivation
Photometry
Receptors
REM sleep
Rodents
Science
Science (multidisciplinary)
Sleep
Sleep and wakefulness
Wakefulness
Online AccessGet full text

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Abstract Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D 1 receptor (D 1 R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arousal-dependent increases in population activity of NAc D 1 R neurons. Optogenetic activation of NAc D 1 R neurons induces immediate transitions from non-rapid eye movement sleep to wakefulness, and chemogenetic stimulation prolongs arousal, with decreased food intake. Patch-clamp, tracing, immunohistochemistry, and electron microscopy reveal that NAc D 1 R neurons project to the midbrain and lateral hypothalamus, and might disinhibit midbrain dopamine neurons and lateral hypothalamus orexin neurons. Photoactivation of terminals in the midbrain and lateral hypothalamus is sufficient to induce wakefulness. Silencing of NAc D 1 R neurons suppresses arousal, with increased nest-building behaviors. Collectively, our data indicate that NAc D 1 R neuron circuits are essential for the induction and maintenance of wakefulness. The nucleus accumbens regulates many behaviours that depend on arousal. Here the authors show that dopamine D 1 receptor neurons in the nucleus accumbens can directly regulate wakefulness.
AbstractList Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D 1 receptor (D 1 R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arousal-dependent increases in population activity of NAc D 1 R neurons. Optogenetic activation of NAc D 1 R neurons induces immediate transitions from non-rapid eye movement sleep to wakefulness, and chemogenetic stimulation prolongs arousal, with decreased food intake. Patch-clamp, tracing, immunohistochemistry, and electron microscopy reveal that NAc D 1 R neurons project to the midbrain and lateral hypothalamus, and might disinhibit midbrain dopamine neurons and lateral hypothalamus orexin neurons. Photoactivation of terminals in the midbrain and lateral hypothalamus is sufficient to induce wakefulness. Silencing of NAc D 1 R neurons suppresses arousal, with increased nest-building behaviors. Collectively, our data indicate that NAc D 1 R neuron circuits are essential for the induction and maintenance of wakefulness.
Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D 1 receptor (D 1 R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arousal-dependent increases in population activity of NAc D 1 R neurons. Optogenetic activation of NAc D 1 R neurons induces immediate transitions from non-rapid eye movement sleep to wakefulness, and chemogenetic stimulation prolongs arousal, with decreased food intake. Patch-clamp, tracing, immunohistochemistry, and electron microscopy reveal that NAc D 1 R neurons project to the midbrain and lateral hypothalamus, and might disinhibit midbrain dopamine neurons and lateral hypothalamus orexin neurons. Photoactivation of terminals in the midbrain and lateral hypothalamus is sufficient to induce wakefulness. Silencing of NAc D 1 R neurons suppresses arousal, with increased nest-building behaviors. Collectively, our data indicate that NAc D 1 R neuron circuits are essential for the induction and maintenance of wakefulness. The nucleus accumbens regulates many behaviours that depend on arousal. Here the authors show that dopamine D 1 receptor neurons in the nucleus accumbens can directly regulate wakefulness.
Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D1 receptor (D1R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arousal-dependent increases in population activity of NAc D1R neurons. Optogenetic activation of NAc D1R neurons induces immediate transitions from non-rapid eye movement sleep to wakefulness, and chemogenetic stimulation prolongs arousal, with decreased food intake. Patch-clamp, tracing, immunohistochemistry, and electron microscopy reveal that NAc D1R neurons project to the midbrain and lateral hypothalamus, and might disinhibit midbrain dopamine neurons and lateral hypothalamus orexin neurons. Photoactivation of terminals in the midbrain and lateral hypothalamus is sufficient to induce wakefulness. Silencing of NAc D1R neurons suppresses arousal, with increased nest-building behaviors. Collectively, our data indicate that NAc D1R neuron circuits are essential for the induction and maintenance of wakefulness.Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D1 receptor (D1R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arousal-dependent increases in population activity of NAc D1R neurons. Optogenetic activation of NAc D1R neurons induces immediate transitions from non-rapid eye movement sleep to wakefulness, and chemogenetic stimulation prolongs arousal, with decreased food intake. Patch-clamp, tracing, immunohistochemistry, and electron microscopy reveal that NAc D1R neurons project to the midbrain and lateral hypothalamus, and might disinhibit midbrain dopamine neurons and lateral hypothalamus orexin neurons. Photoactivation of terminals in the midbrain and lateral hypothalamus is sufficient to induce wakefulness. Silencing of NAc D1R neurons suppresses arousal, with increased nest-building behaviors. Collectively, our data indicate that NAc D1R neuron circuits are essential for the induction and maintenance of wakefulness.
The nucleus accumbens regulates many behaviours that depend on arousal. Here the authors show that dopamine D1 receptor neurons in the nucleus accumbens can directly regulate wakefulness.
Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that NAc dopamine D1 receptor (D1R)-expressing neurons are essential for behavioral arousal. Using in vivo fiber photometry in mice, we find arousal-dependent increases in population activity of NAc D1R neurons. Optogenetic activation of NAc D1R neurons induces immediate transitions from non-rapid eye movement sleep to wakefulness, and chemogenetic stimulation prolongs arousal, with decreased food intake. Patch-clamp, tracing, immunohistochemistry, and electron microscopy reveal that NAc D1R neurons project to the midbrain and lateral hypothalamus, and might disinhibit midbrain dopamine neurons and lateral hypothalamus orexin neurons. Photoactivation of terminals in the midbrain and lateral hypothalamus is sufficient to induce wakefulness. Silencing of NAc D1R neurons suppresses arousal, with increased nest-building behaviors. Collectively, our data indicate that NAc D1R neuron circuits are essential for the induction and maintenance of wakefulness.
ArticleNumber 1576
Author Li, Ya-Dong
Qu, Wei-Min
Huang, Zhi-Li
Yuan, Xiang-Shan
Luo, Yan-Jia
Wang, Lu
Yang, Su-Rong
Cherasse, Yoan
Wang, Juan
Lazarus, Michael
Chen, Jiang-Fan
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– sequence: 6
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  surname: Wang
  fullname: Wang, Juan
  organization: Department of Pharmacology, State Key Laboratory of Medical Neurobiology, School of Basic Medical Sciences; Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University
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  email: quweimin@fudan.edu.cn
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Snippet Nucleus accumbens (NAc) is involved in behaviors that depend on heightened wakefulness, but its impact on arousal remains unclear. Here, we demonstrate that...
The nucleus accumbens regulates many behaviours that depend on arousal. Here the authors show that dopamine D1 receptor neurons in the nucleus accumbens can...
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Animal behavior
Arousal
Dopamine
Dopamine D1 receptors
Electron microscopy
Eye movements
Food intake
Humanities and Social Sciences
Hypothalamus
Hypothalamus (lateral)
Immunohistochemistry
Mesencephalon
multidisciplinary
Neurons
NREM sleep
Nuclei
Nucleus accumbens
Orexins
Photoactivation
Photometry
Receptors
REM sleep
Rodents
Science
Science (multidisciplinary)
Sleep
Sleep and wakefulness
Wakefulness
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Title Nucleus accumbens controls wakefulness by a subpopulation of neurons expressing dopamine D1 receptors
URI https://link.springer.com/article/10.1038/s41467-018-03889-3
https://www.proquest.com/docview/2028131994
https://www.proquest.com/docview/2028955640
https://pubmed.ncbi.nlm.nih.gov/PMC5910424
https://doaj.org/article/a5e620d4d6f24425b57ee8f9091bbfbb
Volume 9
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