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Distinct roles of monkey OFC-subcortical pathways in adaptive behavior

Lookup NU author(s): Dr Mark EldridgeORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© The Author(s) 2024.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.


Publication metadata

Author(s): Oyama K, Majima K, Nagai Y, Hori Y, Hirabayashi T, Eldridge MAG, Mimura K, Miyakawa N, Fujimoto A, Hori Y, Iwaoki H, Inoue K-I, Saunders RC, Takada M, Yahata N, Higuchi M, Richmond BJ, Minamimoto T

Publication type: Article

Publication status: Published

Journal: Nature Communications

Year: 2024

Volume: 15

Issue: 1

Online publication date: 28/08/2024

Acceptance date: 10/07/2024

Date deposited: 19/02/2025

ISSN (electronic): 2041-1723

Publisher: Nature Research

URL: https://doi.org/10.1038/s41467-024-50505-8

DOI: 10.1038/s41467-024-50505-8

Data Access Statement: The Source data are provided as a Source Data file at https://github. com/minamimoto-lab/2023-Oyama-OFC. Source data are provided with this paper. The Python code used for the analysis is available at https://github. com/minamimoto-lab/2023-Oyama-OFC.

PubMed id: 39198415


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Funding

Funder referenceFunder name
MEXT/JSPS KAKENHI Grant Numbers JP18K15353, JP21K07268, JP22H05521

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