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Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action

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...

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Autores principales: Fujimoto, Atsushi, Hori, Yukiko, Nagai, Yuji, Kikuchi, Erika, Oyama, Kei, Suhara, Tetsuya, Minamimoto, Takafumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6407294/
https://www.ncbi.nlm.nih.gov/pubmed/30626695
http://dx.doi.org/10.1523/JNEUROSCI.2399-18.2018
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author Fujimoto, Atsushi
Hori, Yukiko
Nagai, Yuji
Kikuchi, Erika
Oyama, Kei
Suhara, Tetsuya
Minamimoto, Takafumi
author_facet Fujimoto, Atsushi
Hori, Yukiko
Nagai, Yuji
Kikuchi, Erika
Oyama, Kei
Suhara, Tetsuya
Minamimoto, Takafumi
author_sort Fujimoto, Atsushi
collection PubMed
description 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 implicated 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 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 highlight the central role of VP in the motivational control of goal-directed action.
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spelling pubmed-64072942019-03-08 Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action Fujimoto, Atsushi Hori, Yukiko Nagai, Yuji Kikuchi, Erika Oyama, Kei Suhara, Tetsuya Minamimoto, Takafumi J Neurosci Research Articles 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 implicated 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 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 highlight the central role of VP in the motivational control of goal-directed action. Society for Neuroscience 2019-03-06 /pmc/articles/PMC6407294/ /pubmed/30626695 http://dx.doi.org/10.1523/JNEUROSCI.2399-18.2018 Text en Copyright © 2019 Fujimoto et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Fujimoto, Atsushi
Hori, Yukiko
Nagai, Yuji
Kikuchi, Erika
Oyama, Kei
Suhara, Tetsuya
Minamimoto, Takafumi
Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action
title Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action
title_full Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action
title_fullStr Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action
title_full_unstemmed Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action
title_short Signaling Incentive and Drive in the Primate Ventral Pallidum for Motivational Control of Goal-Directed Action
title_sort signaling incentive and drive in the primate ventral pallidum for motivational control of goal-directed action
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6407294/
https://www.ncbi.nlm.nih.gov/pubmed/30626695
http://dx.doi.org/10.1523/JNEUROSCI.2399-18.2018
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