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Neuron. 2018 Sep 19;99(6):1302-1314.e5. doi: 10.1016/j.neuron.2018.08.002. Epub 2018 Aug 23.

Monitoring and Updating of Action Selection for Goal-Directed Behavior through the Striatal Direct and Indirect Pathways.

Author information

1
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan.
2
Department of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University School of Medicine, Fukushima 960-1295, Japan.
3
Division of Cerebral Circuitry, National Institute for Physiological Sciences, and Department of Physiological Sciences, SOKENDAI (The Graduate University for Advanced Studies), Okazaki 444-8787, Japan.
4
Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan.
5
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan; Department of Physiology, Faculty of Health and Sports Science, Juntendo University, Chiba 270-1695 Japan.
6
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan; Center for Information and Neural Networks, National Institute of Information and Communications Technology, Osaka 565-0871, Japan.
7
Division of System Neurophysiology, National Institute for Physiological Sciences, and Department of Physiological Sciences, SOKENDAI (The Graduate University for Advanced Studies), Okazaki 444-8585, Japan.
8
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan; Department of Anatomy and Neurobiology, University of California, Irvine, CA 92697, USA.
9
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan; Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
10
Medical Innovation Center, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan.
11
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan. Electronic address: isomura@lab.tamagawa.ac.jp.
12
Brain Science Institute, Tamagawa University, Machida, Tokyo 194-8610, Japan. Electronic address: mkimura@lab.tamagawa.ac.jp.

Abstract

The basal ganglia play key roles in adaptive behaviors guided by reward and punishment. However, despite accumulating knowledge, few studies have tested how heterogeneous signals in the basal ganglia are organized and coordinated for goal-directed behavior. In this study, we investigated neuronal signals of the direct and indirect pathways of the basal ganglia as rats performed a lever push/pull task for a probabilistic reward. In the dorsomedial striatum, we found that optogenetically and electrophysiologically identified direct pathway neurons encoded reward outcomes, whereas indirect pathway neurons encoded no-reward outcome and next-action selection. Outcome coding occurred in association with the chosen action. In support of pathway-specific neuronal coding, light activation induced a bias on repeat selection of the same action in the direct pathway, but on switch selection in the indirect pathway. Our data reveal the mechanisms underlying monitoring and updating of action selection for goal-directed behavior through basal ganglia circuits.

KEYWORDS:

action selection; antidromic activation; basal ganglia; decision making; direct and indirect pathway; dorsomedial striatum; optogenetics; outcome; punishment; reward

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