Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways

Parvalbumin (PV) expressing GABAergic interneurons provide large source of GABA to spiny projection neurons (SPNs) in the striatum. However, the roles of PV+ interneurons in the regulation of SPNs in the ventral striatum and emotional states are largely unknown. Here, we investigated whether stimula...

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Main Authors: Xi Chen, Zhiyuan Liu, Chaonan Ma, Lan Ma, Xing Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Behavioral Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnbeh.2019.00110/full
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author Xi Chen
Zhiyuan Liu
Chaonan Ma
Lan Ma
Xing Liu
author_facet Xi Chen
Zhiyuan Liu
Chaonan Ma
Lan Ma
Xing Liu
author_sort Xi Chen
collection DOAJ
description Parvalbumin (PV) expressing GABAergic interneurons provide large source of GABA to spiny projection neurons (SPNs) in the striatum. However, the roles of PV+ interneurons in the regulation of SPNs in the ventral striatum and emotional states are largely unknown. Here, we investigated whether stimulation of ventral striatal (accumbal) PV+ interneurons would drive emotional valence in mice. We found that during conditioned place preference (CPP) training, activation of accumbal PV+ interneurons evoked place preference while suppressing them resulted in conditioned place aversion (CPA). Activation of PV+ interneurons during place conditioning increased Fos expression in SPNs in the direct pathway (dSPNs) and impaired lithium chloride-induced CPA. Activation of dSPNs and SPNs in the indirect pathway (iSPNs) induced CPP and CPA, respectively; conversely, suppression of dSPNs or iSPNs induced CPA or CPP. In addition, activation or suppression of calretinin-expressing (CR) GABAergic interneurons did not induce place preference or aversion. These data suggest that PV+ interneurons can bidirectionally determine the emotional valence through their regulation of accumbal SPN activities and raise the possibility that manipulation of PV+ interneuron activity may have the potential to alter emotional valence and treat related mental disorders.
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spelling doaj.art-a57d270dc2c14912949ee461a97e5cbd2022-12-22T01:29:35ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532019-05-011310.3389/fnbeh.2019.00110455056Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output PathwaysXi ChenZhiyuan LiuChaonan MaLan MaXing LiuParvalbumin (PV) expressing GABAergic interneurons provide large source of GABA to spiny projection neurons (SPNs) in the striatum. However, the roles of PV+ interneurons in the regulation of SPNs in the ventral striatum and emotional states are largely unknown. Here, we investigated whether stimulation of ventral striatal (accumbal) PV+ interneurons would drive emotional valence in mice. We found that during conditioned place preference (CPP) training, activation of accumbal PV+ interneurons evoked place preference while suppressing them resulted in conditioned place aversion (CPA). Activation of PV+ interneurons during place conditioning increased Fos expression in SPNs in the direct pathway (dSPNs) and impaired lithium chloride-induced CPA. Activation of dSPNs and SPNs in the indirect pathway (iSPNs) induced CPP and CPA, respectively; conversely, suppression of dSPNs or iSPNs induced CPA or CPP. In addition, activation or suppression of calretinin-expressing (CR) GABAergic interneurons did not induce place preference or aversion. These data suggest that PV+ interneurons can bidirectionally determine the emotional valence through their regulation of accumbal SPN activities and raise the possibility that manipulation of PV+ interneuron activity may have the potential to alter emotional valence and treat related mental disorders.https://www.frontiersin.org/article/10.3389/fnbeh.2019.00110/fullparvalbumin interneuronsnucleus accumbenscalretinin interneuronsconditioned place preferenceconditioned place aversion
spellingShingle Xi Chen
Zhiyuan Liu
Chaonan Ma
Lan Ma
Xing Liu
Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways
Frontiers in Behavioral Neuroscience
parvalbumin interneurons
nucleus accumbens
calretinin interneurons
conditioned place preference
conditioned place aversion
title Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways
title_full Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways
title_fullStr Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways
title_full_unstemmed Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways
title_short Parvalbumin Interneurons Determine Emotional Valence Through Modulating Accumbal Output Pathways
title_sort parvalbumin interneurons determine emotional valence through modulating accumbal output pathways
topic parvalbumin interneurons
nucleus accumbens
calretinin interneurons
conditioned place preference
conditioned place aversion
url https://www.frontiersin.org/article/10.3389/fnbeh.2019.00110/full
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AT chaonanma parvalbumininterneuronsdetermineemotionalvalencethroughmodulatingaccumbaloutputpathways
AT lanma parvalbumininterneuronsdetermineemotionalvalencethroughmodulatingaccumbaloutputpathways
AT xingliu parvalbumininterneuronsdetermineemotionalvalencethroughmodulatingaccumbaloutputpathways