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Signaling incentive and drive in the primate ventral pallidum for motivational control of goal-directed action

View ORCID ProfileAtsushi Fujimoto, Yukiko Hori, Yuji Nagai, Erika Kikuchi, Kei Oyama, Tetsuya Suhara, Takafumi Minamimoto
doi: https://doi.org/10.1101/420851
Atsushi Fujimoto
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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  • ORCID record for Atsushi Fujimoto
Yukiko Hori
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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Yuji Nagai
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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Erika Kikuchi
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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Kei Oyama
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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Tetsuya Suhara
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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Takafumi Minamimoto
1Department of Functional Brain Imaging, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan, 263-8555
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  • For correspondence: minamimoto.takafumi@qst.go.jp
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Abstract

Processing incentive and drive is essential for control of goal-directed behavior. The limbic part of the basal ganglia has been emphasized in these processes, yet the exact neuronal mechanism has remained elusive. In this study, we examined the neuronal activity of the ventral pallidum (VP) and its upstream area, the rostromedial caudate (rmCD), while two male macaque monkeys performed an instrumental lever-release task, in which a visual cue indicated the forthcoming reward size. We found that the activity of some neurons in VP and rmCD reflected the expected reward-size transiently following the cue. Reward-size coding appeared earlier and stronger in VP than in rmCD. We also found that the activity in these areas was modulated by the satiation level of monkeys, which also occurred more frequently in VP than in rmCD. The information regarding reward-size and satiation-level was independently signaled in the neuronal populations of these areas. The data thus highlighted the neuronal coding of key variables for goal-directed behavior in VP. Furthermore, pharmacological inactivation of VP induced more severe deficit of goal-directed behavior than inactivation of rmCD, which was indicated by abnormal error repetition and diminished satiation effect on the performance. These results suggest that VP encodes incentive value and internal drive, and plays a pivotal role in the control of motivation to promote goal-directed behavior.

Significance Statement The limbic part of the basal ganglia has been emphasized in the motivational control of goal-directed action. Here, we investigated how the ventral pallidum (VP) and the rostromedial caudate (rmCD) encode incentive value and internal drive, and control goal-directed behavior. Neuronal recording and subsequent pharmacological inactivation revealed that the VP had stronger coding of reward size and satiation level than rmCD. Reward size and satiation level were independently encoded in the neuronal population of these areas. Furthermore, VP inactivation impaired goal-directed behavior more severely than rmCD inactivation. These results highlighted the central role of VP in the motivational control of goal-directed action.

Acknowledgments

We thank J. Kamei, Y. Matsuda, R. Yamaguchi, Y. Sugii and R. Suma for their technical assistance, and Dr. I. Monosov for his invaluable technical advice and discussion. This work was supported by JSPS KAKENHI [JP15H05917] (to T. M.), [JP15H06872, JP17K13275] (to A. F.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT), and by the Strategic Research Program for Brain Sciences from the Japan Agency for Medical Research and Development (AMED) JP18dm0107146 (to T. M.).

Author Contributions

A. F. and T. M. designed the research; A. F., Y. H., Y. N. and E. K. performed the research; A. F. analyzed the data; all authors wrote the manuscript.

Footnotes

  • Conflict of Interest: The authors declare no competing financial interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 18, 2018.
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Signaling incentive and drive in the primate ventral pallidum for motivational control of goal-directed action
Atsushi Fujimoto, Yukiko Hori, Yuji Nagai, Erika Kikuchi, Kei Oyama, Tetsuya Suhara, Takafumi Minamimoto
bioRxiv 420851; doi: https://doi.org/10.1101/420851
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Signaling incentive and drive in the primate ventral pallidum for motivational control of goal-directed action
Atsushi Fujimoto, Yukiko Hori, Yuji Nagai, Erika Kikuchi, Kei Oyama, Tetsuya Suhara, Takafumi Minamimoto
bioRxiv 420851; doi: https://doi.org/10.1101/420851

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