IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36795-4.html
   My bibliography  Save this article

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

Author

Listed:
  • Kyuhyun Choi

    (University of Pennsylvania)

  • Eugenio Piasini

    (University of Pennsylvania
    International School for Advanced Studies (SISSA))

  • Edgar Díaz-Hernández

    (University of Pennsylvania)

  • Luigim Vargas Cifuentes

    (University of Pennsylvania
    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)

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.

Suggested Citation

  • Kyuhyun Choi & Eugenio Piasini & Edgar Díaz-Hernández & Luigim Vargas Cifuentes & Nathan T. Henderson & Elizabeth N. Holly & Manivannan Subramaniyan & Charles R. Gerfen & Marc V. Fuccillo, 2023. "Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36795-4
    DOI: 10.1038/s41467-023-36795-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36795-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36795-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Caroline A. Runyan & Eugenio Piasini & Stefano Panzeri & Christopher D. Harvey, 2017. "Distinct timescales of population coding across cortex," Nature, Nature, vol. 548(7665), pages 92-96, August.
    2. Ben Engelhard & Joel Finkelstein & Julia Cox & Weston Fleming & Hee Jae Jang & Sharon Ornelas & Sue Ann Koay & Stephan Y. Thiberge & Nathaniel D. Daw & David W. Tank & Ilana B. Witten, 2019. "Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons," Nature, Nature, vol. 570(7762), pages 509-513, June.
    3. Marcus Stephenson-Jones & Kai Yu & Sandra Ahrens & Jason M. Tucciarone & Aile N. van Huijstee & Luis A. Mejia & Mario A. Penzo & Lung-Hao Tai & Linda Wilbrecht & Bo Li, 2016. "A basal ganglia circuit for evaluating action outcomes," Nature, Nature, vol. 539(7628), pages 289-293, November.
    4. Denise J. Cai & Daniel Aharoni & Tristan Shuman & Justin Shobe & Jeremy Biane & Weilin Song & Brandon Wei & Michael Veshkini & Mimi La-Vu & Jerry Lou & Sergio E. Flores & Isaac Kim & Yoshitake Sano & , 2016. "A shared neural ensemble links distinct contextual memories encoded close in time," Nature, Nature, vol. 534(7605), pages 115-118, June.
    5. James M. Otis & Vijay M. K. Namboodiri & Ana M. Matan & Elisa S. Voets & Emily P. Mohorn & Oksana Kosyk & Jenna A. McHenry & J. Elliott Robinson & Shanna L. Resendez & Mark A. Rossi & Garret D. Stuber, 2017. "Prefrontal cortex output circuits guide reward seeking through divergent cue encoding," Nature, Nature, vol. 543(7643), pages 103-107, March.
    6. Junya Hirokawa & Alexander Vaughan & Paul Masset & Torben Ott & Adam Kepecs, 2019. "Frontal cortex neuron types categorically encode single decision variables," Nature, Nature, vol. 576(7787), pages 446-451, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Zihao Chen & Yechao Han & Zheng Ma & Xinnian Wang & Surui Xu & Yong Tang & Alexei L. Vyssotski & Bailu Si & Yang Zhan, 2024. "A prefrontal-thalamic circuit encodes social information for social recognition," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Yu-Jun Wang & Gui-Ying Zan & Cenglin Xu & Xue-Ping Li & Xuelian Shu & Song-Yu Yao & Xiao-Shan Xu & Xiaoyun Qiu & Yexiang Chen & Kai Jin & Qi-Xin Zhou & Jia-Yu Ye & Yi Wang & Lin Xu & Zhong Chen & Jing, 2023. "The claustrum-prelimbic cortex circuit through dynorphin/κ-opioid receptor signaling underlies depression-like behaviors associated with social stress etiology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Paul J. Lamothe-Molina & Andreas Franzelin & Lennart Beck & Dong Li & Lea Auksutat & Tim Fieblinger & Laura Laprell & Joachim Alhbeck & Christine E. Gee & Matthias Kneussel & Andreas K. Engel & Claus , 2022. "ΔFosB accumulation in hippocampal granule cells drives cFos pattern separation during spatial learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Zhiwei Xu & Erez Geron & Luis M. Pérez-Cuesta & Yang Bai & Wen-Biao Gan, 2023. "Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Kelsey M. Vollmer & Lisa M. Green & Roger I. Grant & Kion T. Winston & Elizabeth M. Doncheck & Christopher W. Bowen & Jacqueline E. Paniccia & Rachel E. Clarke & Annika Tiller & Preston N. Siegler & B, 2022. "An opioid-gated thalamoaccumbal circuit for the suppression of reward seeking in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Robert N. Fetcho & Baila S. Hall & David J. Estrin & Alexander P. Walsh & Peter J. Schuette & Jesse Kaminsky & Ashna Singh & Jacob Roshgodal & Charlotte C. Bavley & Viraj Nadkarni & Susan Antigua & Th, 2023. "Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    11. Akinobu Suzuki & Sakurako Kosugi & Emi Murayama & Eri Sasakawa & Noriaki Ohkawa & Ayumu Konno & Hirokazu Hirai & Kaoru Inokuchi, 2022. "A cortical cell ensemble in the posterior parietal cortex controls past experience-dependent memory updating," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. John N. J. Reynolds & Riccardo Avvisati & Paul D. Dodson & Simon D. Fisher & Manfred J. Oswald & Jeffery R. Wickens & Yan-Feng Zhang, 2022. "Coincidence of cholinergic pauses, dopaminergic activation and depolarisation of spiny projection neurons drives synaptic plasticity in the striatum," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    13. Henry W. Kietzman & Gracy Trinoskey-Rice & Sarah A. Blumenthal & Jidong D. Guo & Shannon L. Gourley, 2022. "Social incentivization of instrumental choice in mice requires amygdala-prelimbic cortex-nucleus accumbens connectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Shiri Shoob & Nadav Buchbinder & Ortal Shinikamin & Or Gold & Halit Baeloha & Tomer Langberg & Daniel Zarhin & Ilana Shapira & Gabriella Braun & Naomi Habib & Inna Slutsky, 2023. "Deep brain stimulation of thalamic nucleus reuniens promotes neuronal and cognitive resilience in an Alzheimer’s disease mouse model," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Sam Gijsen & Miro Grundei & Robert T Lange & Dirk Ostwald & Felix Blankenburg, 2021. "Neural surprise in somatosensory Bayesian learning," PLOS Computational Biology, Public Library of Science, vol. 17(2), pages 1-36, February.
    17. Nagaraj R. Mahajan & Shreesh P. Mysore, 2022. "Donut-like organization of inhibition underlies categorical neural responses in the midbrain," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Ana M. G. Manea & David J.-N. Maisson & Benjamin Voloh & Anna Zilverstand & Benjamin Hayden & Jan Zimmermann, 2024. "Neural timescales reflect behavioral demands in freely moving rhesus macaques," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Torben Ott & Anna Marlina Stein & Andreas Nieder, 2023. "Dopamine receptor activation regulates reward expectancy signals during cognitive control in primate prefrontal neurons," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    20. Yanjun Sun & Lisa M. Giocomo, 2022. "Neural circuit dynamics of drug-context associative learning in the mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36795-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.