Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder

Background: Many patients with attention-deficit/hyperactivity disorder (ADHD) display aberrant reward-related behavior. Task-based fMRI studies have related atypical reward processing in ADHD to altered BOLD activity in regions underlying reward processing such as ventral striatum and orbitofrontal...

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Main Authors: Marianne Oldehinkel, Christian F. Beckmann, Barbara Franke, Catharina A. Hartman, Pieter J. Hoekstra, Jaap Oosterlaan, Dirk Heslenfeld, Jan K. Buitelaar, Maarten Mennes
Format: Article
Language:English
Published: Elsevier 2016-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158216301875
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spelling doaj-df7750a97fd4451d88a24986d8fb81772020-11-24T23:13:39ZengElsevierNeuroImage: Clinical2213-15822016-01-0112C79680510.1016/j.nicl.2016.10.006Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorderMarianne Oldehinkel0Christian F. Beckmann1Barbara Franke2Catharina A. Hartman3Pieter J. Hoekstra4Jaap Oosterlaan5Dirk Heslenfeld6Jan K. Buitelaar7Maarten Mennes8Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The NetherlandsDepartment of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The NetherlandsDonders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The NetherlandsUniversity of Groningen, University Medical Center Groningen, Department of Psychiatry, Groningen, The NetherlandsUniversity of Groningen, University Medical Center Groningen, Department of Psychiatry, Groningen, The NetherlandsVrije Universiteit Amsterdam, Clinical Neuropsychology Section, Amsterdam, The NetherlandsVrije Universiteit Amsterdam, Clinical Neuropsychology Section, Amsterdam, The NetherlandsDepartment of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, The NetherlandsDonders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The NetherlandsBackground: Many patients with attention-deficit/hyperactivity disorder (ADHD) display aberrant reward-related behavior. Task-based fMRI studies have related atypical reward processing in ADHD to altered BOLD activity in regions underlying reward processing such as ventral striatum and orbitofrontal cortex. However, it remains unclear whether the observed effects are region-specific or related to changes in functional connectivity of networks supporting reward processing. Here we use resting-state fMRI to comprehensively delineate the functional connectivity architecture underlying aberrant reward processing in ADHD. Methods: We assessed resting-state functional connectivity of four networks that support reward processing. These networks showed high spatial overlap with the default mode, fronto-parietal, lateral visual, and salience networks, yet only activity within the salience network was effectively sensitive to reward value. We parcelled these networks into their functional cortical and subcortical subregions and obtained functional connectivity matrices by computing Pearson correlations between the regional time series. We compared functional connectivity within each of the four networks between participants with ADHD and controls, and related functional connectivity to dimensional ADHD symptom scores across all participants (N = 444; age range: 8.5–30.5; mean age: 17.7). Results: We did not observe significant ADHD-related alterations in functional connectivity of the salience network, which included key reward regions. Instead, levels of inattention symptoms modulated functional connectivity of the default-mode and fronto-parietal networks, which supported general task processing. Conclusions: The present study does not corroborate previous childhood evidence for functional connectivity alterations between key reward processing regions in adolescents and young adults with ADHD. Our findings could point to developmental normalization or indicate that reward-processing deficits result from functional connectivity alterations in general task-related networks.http://www.sciencedirect.com/science/article/pii/S2213158216301875ADHDRewardResting-state fMRIFunctional parcellationFunctional connectivityDefault mode networkFronto-parietal network
collection DOAJ
language English
format Article
sources DOAJ
author Marianne Oldehinkel
Christian F. Beckmann
Barbara Franke
Catharina A. Hartman
Pieter J. Hoekstra
Jaap Oosterlaan
Dirk Heslenfeld
Jan K. Buitelaar
Maarten Mennes
spellingShingle Marianne Oldehinkel
Christian F. Beckmann
Barbara Franke
Catharina A. Hartman
Pieter J. Hoekstra
Jaap Oosterlaan
Dirk Heslenfeld
Jan K. Buitelaar
Maarten Mennes
Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
NeuroImage: Clinical
ADHD
Reward
Resting-state fMRI
Functional parcellation
Functional connectivity
Default mode network
Fronto-parietal network
author_facet Marianne Oldehinkel
Christian F. Beckmann
Barbara Franke
Catharina A. Hartman
Pieter J. Hoekstra
Jaap Oosterlaan
Dirk Heslenfeld
Jan K. Buitelaar
Maarten Mennes
author_sort Marianne Oldehinkel
title Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
title_short Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
title_full Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
title_fullStr Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
title_full_unstemmed Functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
title_sort functional connectivity in cortico-subcortical brain networks underlying reward processing in attention-deficit/hyperactivity disorder
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2016-01-01
description Background: Many patients with attention-deficit/hyperactivity disorder (ADHD) display aberrant reward-related behavior. Task-based fMRI studies have related atypical reward processing in ADHD to altered BOLD activity in regions underlying reward processing such as ventral striatum and orbitofrontal cortex. However, it remains unclear whether the observed effects are region-specific or related to changes in functional connectivity of networks supporting reward processing. Here we use resting-state fMRI to comprehensively delineate the functional connectivity architecture underlying aberrant reward processing in ADHD. Methods: We assessed resting-state functional connectivity of four networks that support reward processing. These networks showed high spatial overlap with the default mode, fronto-parietal, lateral visual, and salience networks, yet only activity within the salience network was effectively sensitive to reward value. We parcelled these networks into their functional cortical and subcortical subregions and obtained functional connectivity matrices by computing Pearson correlations between the regional time series. We compared functional connectivity within each of the four networks between participants with ADHD and controls, and related functional connectivity to dimensional ADHD symptom scores across all participants (N = 444; age range: 8.5–30.5; mean age: 17.7). Results: We did not observe significant ADHD-related alterations in functional connectivity of the salience network, which included key reward regions. Instead, levels of inattention symptoms modulated functional connectivity of the default-mode and fronto-parietal networks, which supported general task processing. Conclusions: The present study does not corroborate previous childhood evidence for functional connectivity alterations between key reward processing regions in adolescents and young adults with ADHD. Our findings could point to developmental normalization or indicate that reward-processing deficits result from functional connectivity alterations in general task-related networks.
topic ADHD
Reward
Resting-state fMRI
Functional parcellation
Functional connectivity
Default mode network
Fronto-parietal network
url http://www.sciencedirect.com/science/article/pii/S2213158216301875
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