Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus

Dysfunction of the striatum is frequently associated with sleep disturbances. However, its role in sleep-wake regulation has been paid little attention even though the striatum densely expresses adenosine A2A receptors (A2ARs), which are essential for adenosine-induced sleep. Here we showed that che...

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Main Authors: Xiang-Shan Yuan, Lu Wang, Hui Dong, Wei-Min Qu, Su-Rong Yang, Yoan Cherasse, Michael Lazarus, Serge N Schiffmann, Alban de Kerchove d'Exaerde, Rui-Xi Li, Zhi-Li Huang
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-10-01
Series:eLife
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Online Access:https://elifesciences.org/articles/29055
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author Xiang-Shan Yuan
Lu Wang
Hui Dong
Wei-Min Qu
Su-Rong Yang
Yoan Cherasse
Michael Lazarus
Serge N Schiffmann
Alban de Kerchove d'Exaerde
Rui-Xi Li
Zhi-Li Huang
author_facet Xiang-Shan Yuan
Lu Wang
Hui Dong
Wei-Min Qu
Su-Rong Yang
Yoan Cherasse
Michael Lazarus
Serge N Schiffmann
Alban de Kerchove d'Exaerde
Rui-Xi Li
Zhi-Li Huang
author_sort Xiang-Shan Yuan
collection DOAJ
description Dysfunction of the striatum is frequently associated with sleep disturbances. However, its role in sleep-wake regulation has been paid little attention even though the striatum densely expresses adenosine A2A receptors (A2ARs), which are essential for adenosine-induced sleep. Here we showed that chemogenetic activation of A2AR neurons in specific subregions of the striatum induced a remarkable increase in non-rapid eye movement (NREM) sleep. Anatomical mapping and immunoelectron microscopy revealed that striatal A2AR neurons innervated the external globus pallidus (GPe) in a topographically organized manner and preferentially formed inhibitory synapses with GPe parvalbumin (PV) neurons. Moreover, lesions of GPe PV neurons abolished the sleep-promoting effect of striatal A2AR neurons. In addition, chemogenetic inhibition of striatal A2AR neurons led to a significant decrease of NREM sleep at active period, but not inactive period of mice. These findings reveal a prominent contribution of striatal A2AR neuron/GPe PV neuron circuit in sleep control.
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spelling doaj.art-b08d72df72dc4b71813577bdc5f9dc2c2022-12-22T03:53:02ZengeLife Sciences Publications LtdeLife2050-084X2017-10-01610.7554/eLife.29055Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidusXiang-Shan Yuan0Lu Wang1Hui Dong2Wei-Min Qu3Su-Rong Yang4Yoan Cherasse5Michael Lazarus6https://orcid.org/0000-0003-3863-4474Serge N Schiffmann7Alban de Kerchove d'Exaerde8Rui-Xi Li9Zhi-Li Huang10https://orcid.org/0000-0001-9359-1150Department of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, China; Department of Anatomy, Histology and Embryology, School of Basic Medical Science, Fudan University, Shanghai, ChinaDepartment of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, ChinaDepartment of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, ChinaDepartment of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, ChinaDepartment of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, ChinaInternational Institute for Integrative Sleep Medicine, University of Tsukuba, Tsukuba, JapanInternational Institute for Integrative Sleep Medicine, University of Tsukuba, Tsukuba, JapanLaboratory of Neurophysiology, ULB Neuroscience Institute, Université Libre de Bruxelles, Brussels, BelgiumLaboratory of Neurophysiology, ULB Neuroscience Institute, Université Libre de Bruxelles, Brussels, BelgiumDepartment of Anatomy, Histology and Embryology, School of Basic Medical Science, Fudan University, Shanghai, ChinaDepartment of Pharmacology, School of Basic Medical Science, Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, ChinaDysfunction of the striatum is frequently associated with sleep disturbances. However, its role in sleep-wake regulation has been paid little attention even though the striatum densely expresses adenosine A2A receptors (A2ARs), which are essential for adenosine-induced sleep. Here we showed that chemogenetic activation of A2AR neurons in specific subregions of the striatum induced a remarkable increase in non-rapid eye movement (NREM) sleep. Anatomical mapping and immunoelectron microscopy revealed that striatal A2AR neurons innervated the external globus pallidus (GPe) in a topographically organized manner and preferentially formed inhibitory synapses with GPe parvalbumin (PV) neurons. Moreover, lesions of GPe PV neurons abolished the sleep-promoting effect of striatal A2AR neurons. In addition, chemogenetic inhibition of striatal A2AR neurons led to a significant decrease of NREM sleep at active period, but not inactive period of mice. These findings reveal a prominent contribution of striatal A2AR neuron/GPe PV neuron circuit in sleep control.https://elifesciences.org/articles/29055striatumA2A receptorsleepchemogeneticsoptogenetics
spellingShingle Xiang-Shan Yuan
Lu Wang
Hui Dong
Wei-Min Qu
Su-Rong Yang
Yoan Cherasse
Michael Lazarus
Serge N Schiffmann
Alban de Kerchove d'Exaerde
Rui-Xi Li
Zhi-Li Huang
Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus
eLife
striatum
A2A receptor
sleep
chemogenetics
optogenetics
title Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus
title_full Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus
title_fullStr Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus
title_full_unstemmed Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus
title_short Striatal adenosine A2A receptor neurons control active-period sleep via parvalbumin neurons in external globus pallidus
title_sort striatal adenosine a2a receptor neurons control active period sleep via parvalbumin neurons in external globus pallidus
topic striatum
A2A receptor
sleep
chemogenetics
optogenetics
url https://elifesciences.org/articles/29055
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