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Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice

Fronto-striatal circuits have been implicated in cognitive control of behavioral output for social and appetitive rewards. The functional diversity of prefrontal cortical populations is strongly dependent on their synaptic targets, with control of motor output mediated by connectivity to dorsal stri...

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Autores principales: Choi, Kyuhyun, Piasini, Eugenio, Díaz-Hernández, Edgar, Cifuentes, Luigim Vargas, Henderson, Nathan T., Holly, Elizabeth N., Subramaniyan, Manivannan, Gerfen, Charles R., Fuccillo, Marc V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10079960/
https://www.ncbi.nlm.nih.gov/pubmed/37024449
http://dx.doi.org/10.1038/s41467-023-36795-4
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author Choi, Kyuhyun
Piasini, Eugenio
Díaz-Hernández, Edgar
Cifuentes, Luigim Vargas
Henderson, Nathan T.
Holly, Elizabeth N.
Subramaniyan, Manivannan
Gerfen, Charles R.
Fuccillo, Marc V.
author_facet Choi, Kyuhyun
Piasini, Eugenio
Díaz-Hernández, Edgar
Cifuentes, Luigim Vargas
Henderson, Nathan T.
Holly, Elizabeth N.
Subramaniyan, Manivannan
Gerfen, Charles R.
Fuccillo, Marc V.
author_sort Choi, Kyuhyun
collection PubMed
description Fronto-striatal circuits have been implicated in cognitive control of behavioral output for social and appetitive rewards. The functional diversity of prefrontal cortical populations is strongly dependent on their synaptic targets, with control of motor output mediated by connectivity to dorsal striatum. Despite evidence for functional diversity along the anterior-posterior striatal axis, it is unclear how distinct fronto-striatal sub-circuits support value-based choice. Here we found segregated prefrontal populations defined by anterior/posterior dorsomedial striatal target. During a feedback-based 2-alternative choice task, single-photon imaging revealed circuit-specific representations of task-relevant information with prelimbic neurons targeting anterior DMS (PL::A-DMS) robustly modulated during choices and negative outcomes, while prelimbic neurons targeting posterior DMS (PL::P-DMS) encoded internal representations of value and positive outcomes contingent on prior choice. Consistent with this distributed coding, optogenetic inhibition of PL::A-DMS circuits strongly impacted choice monitoring and responses to negative outcomes while inhibition of PL::P-DMS impaired task engagement and strategies following positive outcomes. Together our data uncover PL populations engaged in distributed processing for value-based choice.
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spelling pubmed-100799602023-04-08 Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice Choi, Kyuhyun Piasini, Eugenio Díaz-Hernández, Edgar Cifuentes, Luigim Vargas Henderson, Nathan T. Holly, Elizabeth N. Subramaniyan, Manivannan Gerfen, Charles R. Fuccillo, Marc V. Nat Commun Article Fronto-striatal circuits have been implicated in cognitive control of behavioral output for social and appetitive rewards. The functional diversity of prefrontal cortical populations is strongly dependent on their synaptic targets, with control of motor output mediated by connectivity to dorsal striatum. Despite evidence for functional diversity along the anterior-posterior striatal axis, it is unclear how distinct fronto-striatal sub-circuits support value-based choice. Here we found segregated prefrontal populations defined by anterior/posterior dorsomedial striatal target. During a feedback-based 2-alternative choice task, single-photon imaging revealed circuit-specific representations of task-relevant information with prelimbic neurons targeting anterior DMS (PL::A-DMS) robustly modulated during choices and negative outcomes, while prelimbic neurons targeting posterior DMS (PL::P-DMS) encoded internal representations of value and positive outcomes contingent on prior choice. Consistent with this distributed coding, optogenetic inhibition of PL::A-DMS circuits strongly impacted choice monitoring and responses to negative outcomes while inhibition of PL::P-DMS impaired task engagement and strategies following positive outcomes. Together our data uncover PL populations engaged in distributed processing for value-based choice. Nature Publishing Group UK 2023-04-06 /pmc/articles/PMC10079960/ /pubmed/37024449 http://dx.doi.org/10.1038/s41467-023-36795-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Choi, Kyuhyun
Piasini, Eugenio
Díaz-Hernández, Edgar
Cifuentes, Luigim Vargas
Henderson, Nathan T.
Holly, Elizabeth N.
Subramaniyan, Manivannan
Gerfen, Charles R.
Fuccillo, Marc V.
Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
title Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
title_full Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
title_fullStr Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
title_full_unstemmed Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
title_short Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
title_sort distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10079960/
https://www.ncbi.nlm.nih.gov/pubmed/37024449
http://dx.doi.org/10.1038/s41467-023-36795-4
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