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

Kyuhyun Choi, Eugenio Piasini, Edgar Díaz-Hernández, Luigim Vargas Cifuentes, Nathan T. Henderson, Elizabeth N. Holly, Manivannan Subramaniyan, Charles R. Gerfen and Marc V. Fuccillo ()
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Kyuhyun Choi: University of Pennsylvania
Eugenio Piasini: University of Pennsylvania
Edgar Díaz-Hernández: University of Pennsylvania
Luigim Vargas Cifuentes: University of Pennsylvania
Nathan T. Henderson: University of Pennsylvania
Elizabeth N. Holly: University of Pennsylvania
Manivannan Subramaniyan: University of Pennsylvania
Charles R. Gerfen: National Institute of Mental Health (NIMH)
Marc V. Fuccillo: University of Pennsylvania

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41467-023-36795-4

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