IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50505-8.html
   My bibliography  Save this article

Distinct roles of monkey OFC-subcortical pathways in adaptive behavior

Author

Listed:
  • Kei Oyama

    (National Institutes for Quantum Science and Technology
    Japan Science and Technology Agency)

  • Kei Majima

    (Japan Science and Technology Agency
    National Institutes for Quantum Science and Technology)

  • Yuji Nagai

    (National Institutes for Quantum Science and Technology)

  • Yukiko Hori

    (National Institutes for Quantum Science and Technology)

  • Toshiyuki Hirabayashi

    (National Institutes for Quantum Science and Technology)

  • Mark A. G. Eldridge

    (National Institutes of Health)

  • Koki Mimura

    (National Institutes for Quantum Science and Technology
    The Institute of Statistical Mathematics)

  • Naohisa Miyakawa

    (National Institutes for Quantum Science and Technology)

  • Atsushi Fujimoto

    (National Institutes for Quantum Science and Technology)

  • Yuki Hori

    (National Institutes for Quantum Science and Technology)

  • Haruhiko Iwaoki

    (National Institutes for Quantum Science and Technology)

  • Ken-ichi Inoue

    (Kyoto University)

  • Richard C. Saunders

    (National Institutes of Health)

  • Masahiko Takada

    (Kyoto University)

  • Noriaki Yahata

    (National Institutes for Quantum Science and Technology)

  • Makoto Higuchi

    (National Institutes for Quantum Science and Technology)

  • Barry J. Richmond

    (National Institutes of Health)

  • Takafumi Minamimoto

    (National Institutes for Quantum Science and Technology)

Abstract

Primates must adapt to changing environments by optimizing their behavior to make beneficial choices. At the core of adaptive behavior is the orbitofrontal cortex (OFC) of the brain, which updates choice value through direct experience or knowledge-based inference. Here, we identify distinct neural circuitry underlying these two separate abilities. We designed two behavioral tasks in which two male macaque monkeys updated the values of certain items, either by directly experiencing changes in stimulus-reward associations, or by inferring the value of unexperienced items based on the task’s rules. Chemogenetic silencing of bilateral OFC combined with mathematical model-fitting analysis revealed that monkey OFC is involved in updating item value based on both experience and inference. In vivo imaging of chemogenetic receptors by positron emission tomography allowed us to map projections from the OFC to the rostromedial caudate nucleus (rmCD) and the medial part of the mediodorsal thalamus (MDm). Chemogenetic silencing of the OFC-rmCD pathway impaired experience-based value updating, while silencing the OFC-MDm pathway impaired inference-based value updating. Our results thus demonstrate dissociable contributions of distinct OFC projections to different behavioral strategies, and provide new insights into the neural basis of value-based adaptive decision-making in primates.

Suggested Citation

  • Kei Oyama & Kei Majima & Yuji Nagai & Yukiko Hori & Toshiyuki Hirabayashi & Mark A. G. Eldridge & Koki Mimura & Naohisa Miyakawa & Atsushi Fujimoto & Yuki Hori & Haruhiko Iwaoki & Ken-ichi Inoue & Ric, 2024. "Distinct roles of monkey OFC-subcortical pathways in adaptive behavior," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50505-8
    DOI: 10.1038/s41467-024-50505-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50505-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50505-8?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. Arghya Mukherjee & Norman H. Lam & Ralf D. Wimmer & Michael M. Halassa, 2021. "Thalamic circuits for independent control of prefrontal signal and noise," Nature, Nature, vol. 600(7887), pages 100-104, December.
    2. Ji-An Li & Daoyi Dong & Zhengde Wei & Ying Liu & Yu Pan & Franco Nori & Xiaochu Zhang, 2020. "Quantum reinforcement learning during human decision-making," Nature Human Behaviour, Nature, vol. 4(3), pages 294-307, March.
    3. Dongjae Kim & Geon Yeong Park & John P. O′Doherty & Sang Wan Lee, 2019. "Task complexity interacts with state-space uncertainty in the arbitration between model-based and model-free learning," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. Kei Kimura & Yuji Nagai & Gaku Hatanaka & Yang Fang & Soshi Tanabe & Andi Zheng & Maki Fujiwara & Mayuko Nakano & Yukiko Hori & Ryosuke F. Takeuchi & Mikio Inagaki & Takafumi Minamimoto & Ichiro Fujit, 2023. "A mosaic adeno-associated virus vector as a versatile tool that exhibits high levels of transgene expression and neuron specificity in primate brain," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Léon Tremblay & Wolfram Schultz, 1999. "Relative reward preference in primate orbitofrontal cortex," Nature, Nature, vol. 398(6729), pages 704-708, April.
    6. Camillo Padoa-Schioppa & John A. Assad, 2006. "Neurons in the orbitofrontal cortex encode economic value," Nature, Nature, vol. 441(7090), pages 223-226, May.
    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. Wan-Yu Shih & Hsiang-Yu Yu & Cheng-Chia Lee & Chien-Chen Chou & Chien Chen & Paul W. Glimcher & Shih-Wei Wu, 2023. "Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    2. Ryan Webb & Paul W. Glimcher & Kenway Louie, 2021. "The Normalization of Consumer Valuations: Context-Dependent Preferences from Neurobiological Constraints," Management Science, INFORMS, vol. 67(1), pages 93-125, January.
    3. Simone Ferrari-Toniolo & Leo Chi U. Seak & Wolfram Schultz, 2022. "Risky choice: Probability weighting explains independence axiom violations in monkeys," Journal of Risk and Uncertainty, Springer, vol. 65(3), pages 319-351, December.
    4. Leo Chi U Seak & Simone Ferrari-Toniolo & Ritesh Jain & Kirby Nielsen & Wolfram Schultz, 2023. "Systematic comparison of risky choices in humans and monkeys," Working Papers 202316, University of Liverpool, Department of Economics.
    5. Paul M Bays & Ben A Dowding, 2017. "Fidelity of the representation of value in decision-making," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-16, March.
    6. Rolls, Edmund T., 2019. "Emotion and reasoning in human decision-making," Economics Discussion Papers 2019-8, Kiel Institute for the World Economy (IfW Kiel).
    7. Rolls, Edmund T., 2019. "Emotion and reasoning in human decision-making," Economics - The Open-Access, Open-Assessment E-Journal (2007-2020), Kiel Institute for the World Economy (IfW Kiel), vol. 13, pages 1-31.
    8. Alcocer, Christian Diego & Jeitschko, Thomas D. & Shupp, Robert, 2020. "Naive and sophisticated mixing: Experimental evidence," Journal of Economic Behavior & Organization, Elsevier, vol. 170(C), pages 157-173.
    9. Laurette Dubé & Antoine Bechara & Ulf Böckenholt & Asim Ansari & Alain Dagher & Mark Daniel & Wayne DeSarbo & Lesley Fellows & Ross Hammond & Terry Huang & Scott Huettel & Yan Kestens & Bärbel Knäuper, 2009. "Towards a brain-to-society systems model of individual choice," Marketing Letters, Springer, vol. 20(1), pages 105-106, March.
    10. Alvino, Letizia & Constantinides, Efthymios & Franco, Massimo, 2018. "Towards a better understanding of consumer behavior : Marginal utility as a parameter in neuromarketing research," Other publications TiSEM b3e61951-9032-4cb4-b075-1, Tilburg University, School of Economics and Management.
    11. Letizia Alvino & Efthymios Constantinides & Massimo Franco, 2018. "Towards a Better Understanding of Consumer Behavior: Marginal Utility as a Parameter in Neuromarketing Research," International Journal of Marketing Studies, Canadian Center of Science and Education, vol. 10(1), pages 90-106, March.
    12. Payzan-LeNestour, Elise & Woodford, Michael, 2022. "Outlier blindness: A neurobiological foundation for neglect of financial risk," Journal of Financial Economics, Elsevier, vol. 143(3), pages 1316-1343.
    13. Louis-Emmanuel Martinet & Denis Sheynikhovich & Karim Benchenane & Angelo Arleo, 2011. "Spatial Learning and Action Planning in a Prefrontal Cortical Network Model," PLOS Computational Biology, Public Library of Science, vol. 7(5), pages 1-21, May.
    14. Wenyi Zhang & Yang Xie & Tianming Yang, 2022. "Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    15. Dickhaut, John & Smith, Vernon & Xin, Baohua & Rustichini, Aldo, 2013. "Human economic choice as costly information processing," Journal of Economic Behavior & Organization, Elsevier, vol. 94(C), pages 206-221.
    16. Bruno B Averbeck & Moonsang Seo, 2008. "The Statistical Neuroanatomy of Frontal Networks in the Macaque," PLOS Computational Biology, Public Library of Science, vol. 4(4), pages 1-11, April.
    17. Brocas, Isabelle & Carrillo, Juan D., 2012. "From perception to action: An economic model of brain processes," Games and Economic Behavior, Elsevier, vol. 75(1), pages 81-103.
    18. Ian Krajbich & Todd Hare & Björn Bartling & Yosuke Morishima & Ernst Fehr, 2015. "A Common Mechanism Underlying Food Choice and Social Decisions," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-24, October.
    19. Andrew E. Clark & Paul Frijters & Michael A. Shields, 2008. "Relative Income, Happiness, and Utility: An Explanation for the Easterlin Paradox and Other Puzzles," Journal of Economic Literature, American Economic Association, vol. 46(1), pages 95-144, March.
    20. Andrew E. Clark & Paul Frijters & Michael A. Shields, 2006. "Income and happiness: Evidence, explanations and economic implications," PSE Working Papers halshs-00590436, HAL.

    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:15:y:2024:i:1:d:10.1038_s41467-024-50505-8. 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.