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Neural correlates of reward processing: Functional dissociation of two components within the ventral striatum
Umeå University, Faculty of Medicine, Department of Radiation Sciences, Diagnostic Radiology. Umeå University, Faculty of Medicine, Umeå Centre for Functional Brain Imaging (UFBI).ORCID iD: 0000-0003-2081-3562
Umeå University, Faculty of Medicine, Department of Radiation Sciences, Diagnostic Radiology. Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Umeå University, Faculty of Medicine, Umeå Centre for Functional Brain Imaging (UFBI).ORCID iD: 0000-0002-3367-1746
Umeå University, Faculty of Medicine, Department of Radiation Sciences, Diagnostic Radiology. Umeå University, Faculty of Medicine, Umeå Centre for Functional Brain Imaging (UFBI). Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).ORCID iD: 0000-0002-5389-1578
2021 (English)In: Brain and Behavior, E-ISSN 2162-3279, Vol. 11, no 2, article id e01987Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
John Wiley & Sons, 2021. Vol. 11, no 2, article id e01987
Keywords [en]
fMRI, functional connectivity, reward, ventral striatum
National Category
Neurosciences
Identifiers
URN: urn:nbn:se:umu:diva-178340DOI: 10.1002/brb3.1987ISI: 000596747300001PubMedID: 33300306Scopus ID: 2-s2.0-85097315292OAI: oai:DiVA.org:umu-178340DiVA, id: diva2:1516206
Funder
Swedish Research Council, 2015-03080Knut and Alice Wallenberg Foundation, 2015.0277Available from: 2021-01-11 Created: 2021-01-11 Last updated: 2024-09-04Bibliographically approved
In thesis
1. Dopamine and the affective-cognitive gradient in the human striatum studied with multimodal brain imaging
Open this publication in new window or tab >>Dopamine and the affective-cognitive gradient in the human striatum studied with multimodal brain imaging
2022 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Both dopamine and the dopamine rich brain area, striatum, have been linked to behaviors related to incentives, motor action, and associative processing. Most of the cortex sends projections to the striatum, these connections have been described as a gradient organization representing a repertoire of functional behaviors. Although considerable research efforts have been made on the functions of dopamine, it is still unclear how and when it is released in the striatum in humans and what role it has for everyday behavior.

The overarching aim of this thesis is to contribute to our understanding of the role of striatal dopamine release during human behaviors relating to incentive, motor, and associative processing. Using a combination of multimodal brain imaging (positron emission tomography and functional magnetic resonance imaging) as well as cognitive modelling this thesis investigates: how a reproducible striatal response to incentives can be divided into behaviorally relevant components relating to affective and cognitive processes, how striatal dopamine release during motor action represent several component processes of behavior, and also provides evidence that striatal dopamine is released during reward prediction errors in humans. The results are consistent with an affective-cognitive gradient in the striatum and suggest that dopamine release into the striatal gradient might facilitate the integration of component processes into complex representations of behavior. The results of this thesis are based on healthy young individuals, however, aberrant dopamine signaling is a hallmark of several psychiatric and neurological diseases making it crucial to further understand the healthy dopamine system.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, 2022. p. 76
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2189
Keywords
dopamine, striatum, incentive, motor, associative, reinforcement learning, reward prediction error, positron emission tomography, functional magnetic resonance imaging, PET/MR, cognitive modelling
National Category
Neurosciences
Identifiers
urn:nbn:se:umu:diva-194740 (URN)978-91-7855-824-7 (ISBN)978-91-7855-823-0 (ISBN)
Public defence
2022-06-10, Hörsal Betula, Målpunkt L, Norrlands universitetssjukhus, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2022-05-20 Created: 2022-05-16 Last updated: 2022-05-17Bibliographically approved

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Grill, FilipNyberg, LarsRieckmann, Anna

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