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Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive

The external part of the globus pallidus (GPe) is a core nucleus of the basal ganglia (BG) whose activity is disrupted under conditions of low dopamine release, as in Parkinson's disease. Current models assume decreased dopamine release in the dorsal striatum results in deactivation of dorsal G...

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Autores principales: Fiore, Vincenzo G., Nolte, Tobias, Rigoli, Francesco, Smittenaar, Peter, Gu, Xiaosi, Dolan, Raymond J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Academic Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5929903/
https://www.ncbi.nlm.nih.gov/pubmed/29481966
http://dx.doi.org/10.1016/j.neuroimage.2018.02.048
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author Fiore, Vincenzo G.
Nolte, Tobias
Rigoli, Francesco
Smittenaar, Peter
Gu, Xiaosi
Dolan, Raymond J.
author_facet Fiore, Vincenzo G.
Nolte, Tobias
Rigoli, Francesco
Smittenaar, Peter
Gu, Xiaosi
Dolan, Raymond J.
author_sort Fiore, Vincenzo G.
collection PubMed
description The external part of the globus pallidus (GPe) is a core nucleus of the basal ganglia (BG) whose activity is disrupted under conditions of low dopamine release, as in Parkinson's disease. Current models assume decreased dopamine release in the dorsal striatum results in deactivation of dorsal GPe, which in turn affects motor expression via a regulatory effect on other nuclei of the BG. However, recent studies in healthy and pathological animal models have reported neural dynamics that do not match with this view of the GPe as a relay in the BG circuit. Thus, the computational role of the GPe in the BG is still to be determined. We previously proposed a neural model that revisits the functions of the nuclei of the BG, and this model predicts that GPe encodes values which are amplified under a condition of low striatal dopaminergic drive. To test this prediction, we used an fMRI paradigm involving a within-subject placebo-controlled design, using the dopamine antagonist risperidone, wherein healthy volunteers performed a motor selection and maintenance task under low and high reward conditions. ROI-based fMRI analysis revealed an interaction between reward and dopamine drive manipulations, with increased BOLD activity in GPe in a high compared to low reward condition, and under risperidone compared to placebo. These results confirm the core prediction of our computational model, and provide a new perspective on neural dynamics in the BG and their effects on motor selection and cognitive disorders.
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spelling pubmed-59299032018-06-01 Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive Fiore, Vincenzo G. Nolte, Tobias Rigoli, Francesco Smittenaar, Peter Gu, Xiaosi Dolan, Raymond J. Neuroimage Article The external part of the globus pallidus (GPe) is a core nucleus of the basal ganglia (BG) whose activity is disrupted under conditions of low dopamine release, as in Parkinson's disease. Current models assume decreased dopamine release in the dorsal striatum results in deactivation of dorsal GPe, which in turn affects motor expression via a regulatory effect on other nuclei of the BG. However, recent studies in healthy and pathological animal models have reported neural dynamics that do not match with this view of the GPe as a relay in the BG circuit. Thus, the computational role of the GPe in the BG is still to be determined. We previously proposed a neural model that revisits the functions of the nuclei of the BG, and this model predicts that GPe encodes values which are amplified under a condition of low striatal dopaminergic drive. To test this prediction, we used an fMRI paradigm involving a within-subject placebo-controlled design, using the dopamine antagonist risperidone, wherein healthy volunteers performed a motor selection and maintenance task under low and high reward conditions. ROI-based fMRI analysis revealed an interaction between reward and dopamine drive manipulations, with increased BOLD activity in GPe in a high compared to low reward condition, and under risperidone compared to placebo. These results confirm the core prediction of our computational model, and provide a new perspective on neural dynamics in the BG and their effects on motor selection and cognitive disorders. Academic Press 2018-06 /pmc/articles/PMC5929903/ /pubmed/29481966 http://dx.doi.org/10.1016/j.neuroimage.2018.02.048 Text en © 2018 The Authors http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Fiore, Vincenzo G.
Nolte, Tobias
Rigoli, Francesco
Smittenaar, Peter
Gu, Xiaosi
Dolan, Raymond J.
Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive
title Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive
title_full Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive
title_fullStr Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive
title_full_unstemmed Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive
title_short Value encoding in the globus pallidus: fMRI reveals an interaction effect between reward and dopamine drive
title_sort value encoding in the globus pallidus: fmri reveals an interaction effect between reward and dopamine drive
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5929903/
https://www.ncbi.nlm.nih.gov/pubmed/29481966
http://dx.doi.org/10.1016/j.neuroimage.2018.02.048
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