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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eLife Sciences Publications Ltd
2017-10-01
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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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issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T01:47:31Z |
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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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