Distinct roles of monkey OFC-subcortical pathways in adaptive behavior

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, Richard C. Saunders, Masahiko Takada, Noriaki Yahata, Makoto Higuchi, Barry J. Richmond and Takafumi Minamimoto ()
Additional contact information
Kei Oyama: National Institutes for Quantum Science and Technology
Kei Majima: Japan Science and Technology Agency
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
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

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-50505-8

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