Abstract

IntroductionRewarding 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.MethodsWe 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.ResultsThe 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.ConclusionWe 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.

Highlights

  • Rewarding and punishing stimuli elicit blood oxygenation level dependent (BOLD) responses in the affective division of the striatum

  • In human fMRI studies, the ventral striatum (VS) shows a differential response between rewarding and punishing stimuli, where rewards are associated with an increased blood oxygenation level dependent (BOLD) response when compared to punishments

  • Even though disinhibition and activation cannot be disentangled with fMRI, it is noteworthy in this context that the inferior VS response to rewards was driven by a less negative BOLD signal as compared to an implicit baseline, maybe suggesting a less inhibited state, whereas the superior VS response was driven by a difference in positive BOLD signal

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Summary

Introduction

Rewarding and punishing stimuli elicit BOLD responses in the affective division of the striatum. 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. An inferior ventral striatal component and hippocampus are part of an intrinsically coupled network that responds to reward-based processing during gambling. A gradient-like organization of cortico-striatal connections has been shown in nonhuman primates (Haber & Knutson, 2010) and identified by resting-state functional connectivity in humans (Marquand et al, 2017). A canonical reward response covers a portion of an affective-cognitive gradient possibly combining aspects of behavior related to affective as well as associative processing (Haber, 2003; Haber et al, 2000; Haber & Knutson, 2010, for review)

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