Association between reward‐related activation in the ventral striatum and trait reward sensitivity is moderated by dopamine transporter genotype

Hahn, Tim; Heinzel, Sebastian; Dresler, Thomas; Plichta, Michael M.; Renner, Tobias; Markulin, Falko; Jakob, Peter M.; Lesch, Klaus‐Peter; Fallgatter, Andreas J.

doi:10.1002/hbm.21127

Cited by 73 publications

(69 citation statements)

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“…Thus, the proportion of hits is highly consistent with the target value selected based on previous reports (Knutson et al, 2001a,b;Kuhl et al, 2010;Hahn et al, 2011). There was no correlation between the winnings in the MID task and the self-reported % Wins in the Opportunity condition across subjects (r ϭ Ϫ0.23, p ϭ 0.244).…”

Section: Behavioral Datasupporting

confidence: 88%

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Response to Anticipated Reward in the Nucleus Accumbens Predicts Behavior in an Independent Test of Honesty

Abe

Greene

2014

Journal of Neuroscience

118

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This study examines the cognitive and neural determinants of honesty and dishonesty. Human subjects undergoing fMRI completed a monetary incentive delay task eliciting responses to anticipated reward in the nucleus accumbens. Subjects next performed an incentivized prediction task, giving them real and repeated opportunities for dishonest gain. Subjects attempted to predict the outcomes of random computerized coin-flips and were financially rewarded for accuracy. In some trials, subjects were rewarded based on selfreported accuracy, allowing them to gain money dishonestly by lying. Dishonest behavior was indexed by improbably high levels of self-reported accuracy. Nucleus accumbens response in the first task, involving only honest rewards, accounted for ϳ25% of the variance in dishonest behavior in the prediction task. Individuals showing relatively strong nucleus accumbens responses to anticipated reward also exhibited increased dorsolateral prefrontal activity (bilateral) in response to opportunities for dishonest gain. These results address two hypotheses concerning (dis)honesty. According to the "Will" hypothesis, honesty results from the active deployment of self-control. According to the "Grace" hypothesis, honesty flows more automatically. The present results suggest a reconciliation between these two hypotheses while explaining (dis)honesty in terms of more basic neural mechanisms: relatively weak responses to anticipated rewards make people morally "Graceful," but individuals who respond more strongly may resist temptation by force of Will.

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Section: Behavioral Datasupporting

confidence: 88%

“…To approximately equate MID task performance across subjects, we used an adaptive algorithm that dynamically adjusted the duration of the target presentation as a function of subject performance (Kuhl et al, 2010;Hahn et al, 2011). Five independent "trains" were used, representing the five different reward or loss values.…”

Section: Methodsmentioning

confidence: 99%

Response to Anticipated Reward in the Nucleus Accumbens Predicts Behavior in an Independent Test of Honesty

Abe

Greene

2014

Journal of Neuroscience

118

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“…One could consider altered baseline dopamine levels in the striatum in ADHD (38) as a possible explanation, since positive correlations between striatal dopamine and ventral striatal activity exist in healthy subjects (39). In addition, the influence of other ADHD candidate genes such as the dopamine transporter gene (DAT1/ SLC6A3) (40), which is also associated with altered dopaminergic synthesis-or perhaps an altered connectivity between the prefrontal cortex and striatum (41)-might play a role. Thus, one might hypothesize that the reduced ventral striatal activity is a compensatory mechanism to alleviate the effects of reduced prefrontal control.…”

Section: 3mentioning

confidence: 99%

Nitric Oxide Synthase Genotype Modulation of Impulsivity and Ventral Striatal Activity in Adult ADHD Patients and Healthy Comparison Subjects

Hoogman¹,

Aarts²,

Zwiers³

et al. 2011

AJP

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(5), as evidenced by steeper temporal discounting rates, altered decision making, and an aversion to delay of gratification in reward-related tests (6-9). Temporal discounting is the patient's preference to receive smaller rewards sooner rather than larger rewards later and is postulated to be an intermediate phenotype for impulsivity. Neuroimaging studies have shown engagement of alternative brain regions in decision making in ADHD patients (10). A prominent feature is hypoactivation of the ventral striatum, a brain area with an important role in reward processing (11,12), during reward anticipation (13,14). Ventral striatal activity is also associated with impulsivity, a hallmark of ADHD (12,13). Recently, the NOS1 gene was identified as a candidate gene for ADHD and other impulsivity disorders (15). A variant in this gene was also among the top findings of a genome-wide association study in ADHD (3). NOS1 encodes nitric oxide synthase 1. Nitric oxide, the product of this enzyme's activity, acts as the second messenger downstream of the N-methyl-d-aspartate receptor and interacts with both the dopaminergic and serotonergic systems in the human brain. Nitric oxide inhibits monoamine transporters, thereby modulating the dopamine and noradrenalin concentration in the extracellular space (16). In addi-(A m J P sy c h ia try 2 0 1 1 ; 1 6 8 :1 0 9 9 -1 1 0 6 ) N itric O x id e S y n th a se G e n o ty p e M o d u la tio n o f Im p u lsiv ity a n d Ve n tra l S tria ta l A c tiv ity in A d u lt A D H D P a tie n ts a n d H e a lth y C o m p a riso n S u b je c ts O b je c tiv e : Attention deficit hyperactivity disorder (AD HD ) is a highly heritable disorder. The NO S1 gene encoding nitric oxide synthase is a candidate gene for AD HD and has been previously linked w ith im pulsivity. In the present study, the authors investigated the effect of a functional variable num ber of tandem repeats (VNTR ) polym orphism in NO S1 (NO S1 exon 1f-VNTR ) on the processing of rew ards, one of the cognitive deficits in AD HD. M e th o d :A sam ple of 136 participants, consisting of 87 adult AD HD patients and 49 healthy com parison subjects, completed a rew ard-related im pulsivity task. A total of 104 participants also underw ent functional m agnetic resonance im aging during a rew ard anticipation task. The effect of the NO S1 exon 1f-VNTR genotype on rew ard-related im pulsivity and rew ard-related ventral striatal activity w as exam ined.R e s u lts : AD HD patients had higher impulsivity scores and low er ventral striatal activity than healthy com parison subjects. The association betw een the short allele and increased im pulsivity w as confirm ed. How ever, independent of disease status, hom ozygous carriers of the short allele of NO S1, the AD HD risk genotype, dem onstrated higher ventral striatal activity than carriers of the other NO S1 VNTR genotypes.C o n c lu s io n s : The authors suggest that the NO S1 genotype influences im pulsivity and its relation w ith AD HD is m ediated through effects on this behavioral tr...

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“…This circuit includes the ventral striatum (VS) as a pivotal structure that is innervated by mesostriatal dopamine and linked to the anterior cingulate cortex (ACC), supplementary motor area (SMA), insula, and thalamus (THAL; Knutson et al, 2001a,b;Kirsch et al, 2003;Knutson and Cooper, 2005;Liu et al, 2011). Anticipatory VS activation has been shown to be a reliable fMRI assay within and across subjects (Plichta et al, 2012), sensitive to genetic variants (Kirsch et al, 2006;Forbes et al, 2009;Hahn et al, 2011) and linked to impulsivity and (an)hedonic states in clinical and nonclinical populations (Kirsch et al, 2006;Scheres et al, 2007;Hahn et al, 2009;Plichta et al, 2009;Forbes et al, 2010;Juckel et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Simultaneous EEG and fMRI Reveals a Causally Connected Subcortical-Cortical Network during Reward Anticipation

et al. 2013

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Electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) have been used to study the neural correlates of reward anticipation, but the interrelation of EEG and fMRI measures remains unknown. The goal of the present study was to investigate this relationship in response to a well established reward anticipation paradigm using simultaneous EEG-fMRI recording in healthy human subjects. Analysis of causal interactions between the thalamus (THAL), ventral-striatum (VS), and supplementary motor area (SMA), using both mediator analysis and dynamic causal modeling, revealed that (1) THAL fMRI blood oxygenation level-dependent (BOLD) activity is mediating intermodal correlations between the EEG contingent negative variation (CNV) signal and the fMRI BOLD signal in SMA and VS, (2) the underlying causal connectivity network consists of top-down regulation from SMA to VS and SMA to THAL along with an excitatory information flow through a THAL3 VS3 SMA route during reward anticipation, and (3) the EEG CNV signal is best predicted by a combination of THAL fMRI BOLD response and strength of top-down regulation from SMA to VS and SMA to THAL. Collectively, these findings represent a likely neurobiological mechanism mapping a primarily subcortical process, i.e., reward anticipation, onto a cortical signature.

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Association between reward‐related activation in the ventral striatum and trait reward sensitivity is moderated by dopamine transporter genotype

Cited by 73 publications

References 50 publications

Response to Anticipated Reward in the Nucleus Accumbens Predicts Behavior in an Independent Test of Honesty

Response to Anticipated Reward in the Nucleus Accumbens Predicts Behavior in an Independent Test of Honesty

Nitric Oxide Synthase Genotype Modulation of Impulsivity and Ventral Striatal Activity in Adult ADHD Patients and Healthy Comparison Subjects

Simultaneous EEG and fMRI Reveals a Causally Connected Subcortical-Cortical Network during Reward Anticipation

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