Single caudate neurons encode temporally discounted value for formulating motivation for action

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Abstract

The term ‘temporal discounting’ describes both choice preferences and motivation for delayed rewards. Here we show that neuronal activity in the dorsal part of the primate caudate head (dCDh) signals the temporally discounted value needed to compute the motivation for delayed rewards. Macaque monkeys performed an instrumental task, in which visual cues indicated the forthcoming size and delay duration before reward. Single dCDh neurons represented the temporally discounted value without reflecting changes in the animal’s physiological state. Bilateral pharmacological or chemogenetic inactivation of dCDh markedly distorted the normal task performance based on the integration of reward size and delay, but did not affect the task performance for different reward sizes without delay. These results suggest that dCDh is involved in encoding the integrated multidimensional information critical for motivation.

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We provide source data to reproduce the main results of the paper presented in Figures 1, 5, 7 and 8.

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Yukiko Hori

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1023-9587
Koki Mimura

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

Competing interests
The authors declare that no competing interests exist.
Yuji Nagai

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7005-0749
Atsushi Fujimoto

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1621-2003
Kei Oyama

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

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The authors declare that no competing interests exist.
Erika Kikuchi

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

Competing interests
The authors declare that no competing interests exist.
Ken-ichi Inoue

Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Japan

Competing interests
The authors declare that no competing interests exist.
Masahiko Takada

Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Japan

Competing interests
The authors declare that no competing interests exist.
Tetsuya Suhara

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

Competing interests
The authors declare that no competing interests exist.
Barry J Richmond

Laboratory of Neuropsychology, NIMH/NIH/DHHS, Bethesda, MD 20814, USA, Bethesda, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8234-1540
Takafumi Minamimoto

Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan

For correspondence
minamimoto.takafumi@qst.go.jp

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4305-0174

Funding

Japan Society for the Promotion of Science (JP18H04037,JP20H05955)

Takafumi Minamimoto

Japan Agency for Medical Research and Development (JP20dm0107146)

Takafumi Minamimoto

Japan Agency for Medical Research and Development (JP20dm0207077)

Masahiko Takada

Japan Agency for Medical Research and Development (JP20dm0307021)

Ken-ichi Inoue

National Institute of Mental Health (Annual Report ZIAMH-2619)

Barry J Richmond

Primate Research Institute, Kyoto University (2020-A-6)

Takafumi Minamimoto

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All surgical and experimental procedures were approved by the National Institutes for Quantum and Radiological Science and Technology (11-1038-11) and by the Animal Care and Use Committee of the National Institute of Mental Health (Annual Report ZIAMH002619), and were in accordance with the Institute of Laboratory Animal Research Guide for the Care and Use of Laboratory Animals.

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.