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

Abstract 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...

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Main Authors: Filip Grill, Lars Nyberg, Anna Rieckmann
Format: Article
Language:English
Published: Wiley 2021-02-01
Series:Brain and Behavior
Subjects:
Online Access:https://doi.org/10.1002/brb3.1987
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spelling doaj-74e510b40ccc45a880118b8dfbc5d26e2021-02-14T15:29:27ZengWileyBrain and Behavior2162-32792021-02-01112n/an/a10.1002/brb3.1987Neural correlates of reward processing: Functional dissociation of two components within the ventral striatumFilip Grill0Lars Nyberg1Anna Rieckmann2Department of Radiation Sciences Umeå Center for Functional Brain Imaging Umeå University Umeå SwedenDepartment of Radiation Sciences Umeå Center for Functional Brain Imaging Umeå University Umeå SwedenDepartment of Radiation Sciences Umeå Center for Functional Brain Imaging Umeå University Umeå SwedenAbstract 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.https://doi.org/10.1002/brb3.1987fMRIfunctional connectivityrewardventral striatum
collection DOAJ
language English
format Article
sources DOAJ
author Filip Grill
Lars Nyberg
Anna Rieckmann
spellingShingle Filip Grill
Lars Nyberg
Anna Rieckmann
Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
Brain and Behavior
fMRI
functional connectivity
reward
ventral striatum
author_facet Filip Grill
Lars Nyberg
Anna Rieckmann
author_sort Filip Grill
title 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_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_sort neural correlates of reward processing: functional dissociation of two components within the ventral striatum
publisher Wiley
series Brain and Behavior
issn 2162-3279
publishDate 2021-02-01
description Abstract 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.
topic fMRI
functional connectivity
reward
ventral striatum
url https://doi.org/10.1002/brb3.1987
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