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Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum

INTRODUCTION: Rewarding and punishing stimuli elicit BOLD responses in the affective division of the striatum. The responses typically traverse from the affective to the associative division of the striatum, suggesting an involvement of associative processes during the modulation of stimuli valance....

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Autores principales: Grill, Filip, Nyberg, Lars, Rieckmann, Anna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7882172/
https://www.ncbi.nlm.nih.gov/pubmed/33300306
http://dx.doi.org/10.1002/brb3.1987
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author Grill, Filip
Nyberg, Lars
Rieckmann, Anna
author_facet Grill, Filip
Nyberg, Lars
Rieckmann, Anna
author_sort Grill, Filip
collection PubMed
description INTRODUCTION: Rewarding and punishing stimuli elicit BOLD responses in the affective division of the striatum. The responses typically traverse from the affective to the associative division of the striatum, suggesting an involvement of associative processes during the modulation of stimuli valance. In this study, we hypothesized that fMRI responses to rewards versus punishments in a guessing card game can be disassociated into two functional component processes that reflect the convergence of limbic and associative functional networks in the ventral striatum. METHODS: We used fMRI data of 175 (92 female) subjects from the human connectome project´s gambling task, working memory task, and resting‐state scans. A reward > punish contrast identified a ventral striatum cluster from which voxelwise GLM parameter estimates were entered into a k‐means clustering algorithm. The k‐means analysis supported separating the cluster into two spatially distinct components. These components were used as seeds to investigate their functional connectivity profile. GLM parameter estimates were extracted and compared from the task contrasts reward > punish and 2‐back > 0‐back from two ROIs in the ventral striatum and one ROI in hippocampus. RESULTS: The analyses converged to show that a superior striatal component, coupled with the ventral attention and frontal control networks, was responsive to both a modulation of cognitive control in working memory and to rewards, whereas the most inferior part of the ventral striatum, coupled with the limbic and default mode networks including the hippocampus, was selectively responsive to rewards. CONCLUSION: We show that the fMRI response to rewards in the ventral striatum reflects a mixture of component processes of reward. An inferior ventral striatal component and hippocampus are part of an intrinsically coupled network that responds to reward‐based processing during gambling. The more superior ventral striatal component is intrinsically coupled to networks involved with executive functioning and responded to both reward and cognitive control demands.
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spelling pubmed-78821722021-02-19 Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum Grill, Filip Nyberg, Lars Rieckmann, Anna Brain Behav Original Research INTRODUCTION: Rewarding and punishing stimuli elicit BOLD responses in the affective division of the striatum. The responses typically traverse from the affective to the associative division of the striatum, suggesting an involvement of associative processes during the modulation of stimuli valance. In this study, we hypothesized that fMRI responses to rewards versus punishments in a guessing card game can be disassociated into two functional component processes that reflect the convergence of limbic and associative functional networks in the ventral striatum. METHODS: We used fMRI data of 175 (92 female) subjects from the human connectome project´s gambling task, working memory task, and resting‐state scans. A reward > punish contrast identified a ventral striatum cluster from which voxelwise GLM parameter estimates were entered into a k‐means clustering algorithm. The k‐means analysis supported separating the cluster into two spatially distinct components. These components were used as seeds to investigate their functional connectivity profile. GLM parameter estimates were extracted and compared from the task contrasts reward > punish and 2‐back > 0‐back from two ROIs in the ventral striatum and one ROI in hippocampus. RESULTS: The analyses converged to show that a superior striatal component, coupled with the ventral attention and frontal control networks, was responsive to both a modulation of cognitive control in working memory and to rewards, whereas the most inferior part of the ventral striatum, coupled with the limbic and default mode networks including the hippocampus, was selectively responsive to rewards. CONCLUSION: We show that the fMRI response to rewards in the ventral striatum reflects a mixture of component processes of reward. An inferior ventral striatal component and hippocampus are part of an intrinsically coupled network that responds to reward‐based processing during gambling. The more superior ventral striatal component is intrinsically coupled to networks involved with executive functioning and responded to both reward and cognitive control demands. John Wiley and Sons Inc. 2020-12-09 /pmc/articles/PMC7882172/ /pubmed/33300306 http://dx.doi.org/10.1002/brb3.1987 Text en © 2020 The Authors. Brain and Behavior published by Wiley Periodicals LLC This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Grill, Filip
Nyberg, Lars
Rieckmann, Anna
Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
title Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
title_full Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
title_fullStr Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
title_full_unstemmed Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
title_short Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
title_sort neural correlates of reward processing: functional dissociation of two components within the ventral striatum
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7882172/
https://www.ncbi.nlm.nih.gov/pubmed/33300306
http://dx.doi.org/10.1002/brb3.1987
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