Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses

Summary: Drinking behavior in rodents is characterized by stereotyped, rhythmic licking movement, which is regulated by the basal ganglia. It is unclear how direct and indirect pathways control the lick bout and individual spout contact. We find that inactivating D1 and D2 receptor-expressing medium...

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Main Authors: Zhaorong Chen, Zhi-Yu Zhang, Wen Zhang, Taorong Xie, Yaping Li, Xiao-Hong Xu, Haishan Yao
Format: Article
Language:English
Published: Elsevier 2021-10-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124721013115
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author Zhaorong Chen
Zhi-Yu Zhang
Wen Zhang
Taorong Xie
Yaping Li
Xiao-Hong Xu
Haishan Yao
author_facet Zhaorong Chen
Zhi-Yu Zhang
Wen Zhang
Taorong Xie
Yaping Li
Xiao-Hong Xu
Haishan Yao
author_sort Zhaorong Chen
collection DOAJ
description Summary: Drinking behavior in rodents is characterized by stereotyped, rhythmic licking movement, which is regulated by the basal ganglia. It is unclear how direct and indirect pathways control the lick bout and individual spout contact. We find that inactivating D1 and D2 receptor-expressing medium spiny neurons (MSNs) in the ventrolateral striatum (VLS) oppositely alters the number of licks in a bout. D1- and D2-MSNs exhibit different patterns of lick-sequence-related activity and different phases of oscillation time-locked to the lick cycle. On the timescale of a lick cycle, transient inactivation of D1-MSNs during tongue protrusion reduces spout contact probability, whereas transiently inactivating D2-MSNs has no effect. On the timescale of a lick bout, inactivation of D1-MSNs (D2-MSNs) causes rate increase (decrease) in a subset of basal ganglia output neurons that decrease firing during licking. Our results reveal the distinct roles of D1- and D2-MSNs in regulating licking at both coarse and fine timescales.
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spelling doaj.art-3ddf2c28ea024e35a214d5e39a0e4a902022-12-21T23:08:45ZengElsevierCell Reports2211-12472021-10-01373109847Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responsesZhaorong Chen0Zhi-Yu Zhang1Wen Zhang2Taorong Xie3Yaping Li4Xiao-Hong Xu5Haishan Yao6Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology, Shanghai 201210, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China; Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology, Shanghai 201210, China; Corresponding authorSummary: Drinking behavior in rodents is characterized by stereotyped, rhythmic licking movement, which is regulated by the basal ganglia. It is unclear how direct and indirect pathways control the lick bout and individual spout contact. We find that inactivating D1 and D2 receptor-expressing medium spiny neurons (MSNs) in the ventrolateral striatum (VLS) oppositely alters the number of licks in a bout. D1- and D2-MSNs exhibit different patterns of lick-sequence-related activity and different phases of oscillation time-locked to the lick cycle. On the timescale of a lick cycle, transient inactivation of D1-MSNs during tongue protrusion reduces spout contact probability, whereas transiently inactivating D2-MSNs has no effect. On the timescale of a lick bout, inactivation of D1-MSNs (D2-MSNs) causes rate increase (decrease) in a subset of basal ganglia output neurons that decrease firing during licking. Our results reveal the distinct roles of D1- and D2-MSNs in regulating licking at both coarse and fine timescales.http://www.sciencedirect.com/science/article/pii/S2211124721013115ventrolateral striatumlickingmedium spiny neuronsoscillatory activitysubstantia nigra pars reticulata
spellingShingle Zhaorong Chen
Zhi-Yu Zhang
Wen Zhang
Taorong Xie
Yaping Li
Xiao-Hong Xu
Haishan Yao
Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
Cell Reports
ventrolateral striatum
licking
medium spiny neurons
oscillatory activity
substantia nigra pars reticulata
title Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
title_full Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
title_fullStr Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
title_full_unstemmed Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
title_short Direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
title_sort direct and indirect pathway neurons in ventrolateral striatum differentially regulate licking movement and nigral responses
topic ventrolateral striatum
licking
medium spiny neurons
oscillatory activity
substantia nigra pars reticulata
url http://www.sciencedirect.com/science/article/pii/S2211124721013115
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AT wenzhang directandindirectpathwayneuronsinventrolateralstriatumdifferentiallyregulatelickingmovementandnigralresponses
AT taorongxie directandindirectpathwayneuronsinventrolateralstriatumdifferentiallyregulatelickingmovementandnigralresponses
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AT xiaohongxu directandindirectpathwayneuronsinventrolateralstriatumdifferentiallyregulatelickingmovementandnigralresponses
AT haishanyao directandindirectpathwayneuronsinventrolateralstriatumdifferentiallyregulatelickingmovementandnigralresponses