Ventral Striatal Hyporesponsiveness During Reward Anticipation in Attention-Deficit/Hyperactivity Disorder
Abstract
Background Although abnormalities in reward processing have been proposed to underlie attention-deficit/hyperactivity disorder (ADHD), this link has not been tested explicitly with neural probes.Methods This hypothesis was tested by using fMRI to compare neural activity within the striatum in individuals with ADHD and healthy controls during a reward-anticipation task that has been shown previously to produce reliable increases in ventral striatum activity in healthy adults and healthy adolescents. Eleven adolescents with ADHD (5 off medication and 6 medication-naïve) and 11 healthy controls (ages 12-17 y) were included. Groups were matched for age, gender, and intelligence quotient.Results We found reduced ventral striatal activation in adolescents with ADHD during reward anticipation, relative to healthy controls. Moreover, ventral striatal activation was negatively correlated with parent-rated hyperactive/impulsive symptoms across the entire sample.Conclusions These findings provide neural evidence that symptoms of ADHD, and impulsivity or hyperactivity in particular, may involve diminished reward anticipation, in addition to commonly observed executive dysfunction.
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Amygdala hyperactivation has also been reported in ADHD during the processing of delayed rewards.
“Amygdala hyperactivation has also been reported in ADHD during the processing of delayed rewards, perhaps consistent with the delay aversion found in some behavioral studies (38, 99-101).”
From Emotion Dysregulation in Attention Deficit Hyperactivity Disorder (2014) · cites this paper as [100]
The study's data are in contrast with reports of decreased responsiveness of the VS in anticipation of reward in adults with ADHD and with one study with adolescents with ADHD.
“However, they are in contrast with reports of decreased responsiveness of the VS in anticipation of reward in adults with ADHD,15 as well as with one study with adolescents with ADHD.16”
From Increased neural responses to reward in adolescents and young adults with attention-deficit/hyperactivity disorder and their unaffected siblings (2015) · cites this paper as [16]
Ventral striatum responses during reward anticipation for adolescents with ADHD were lower than for control participants, but no differences were observed during reward receipt.
“VS responses during reward anticipation for adolescents with ADHD were observed to be lower than for control participants, but no differences were observed during reward receipt.16”
From Increased neural responses to reward in adolescents and young adults with attention-deficit/hyperactivity disorder and their unaffected siblings (2015) · cites this paper as [16]
Children with ADHD have reduced NAc activity when anticipating monetary rewards, seen particularly in drug-naive children, carriers of the DAT nine-repeat allele, and in response to seeking gains rather than avoiding losses.
“Children with ADHD have reduced NAc activity when anticipating monetary rewards [18,486,487], which is seen particularly in drug-naive children [490], in carriers of the DAT nine-repeat allele [491], and in response to seeking gains rather than avoiding losses [492].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [486]
fMRI studies in ADHD have shown decreased ventral striatum activation during monetary-reward anticipation, atypical orbitofrontal activation during monetary-reward outcome, and decreased DCN and amygdala activation during delayed reward outcome.
“These studies have shown decreased ventral striatum activation during monetary-reward anticipation [484-487], atypical orbitofrontal activation during monetary-reward outcome [487,488], and decreased DCN and amygdala activation during delayed reward outcome [485,489].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [486]
Recent studies suggest underactivation in the ventral striatum in ADHD following the signaling of future rewards.
“To date the role of structural and/or functional alterations within this circuit in ADHD remain under-researched although recent studies suggest underactivation in the ventral striatum in ADHD following the signaling of future rewards (Scheres et al., 2007) and over-activation of the amygdala as delay to rewards increase (Plichta et al., 2009).”
From Context-dependent Dynamic Processes in Attention Deficit/Hyperactivity Disorder: Differentiating Common and Unique Effects of State Regulation Deficits and Delay Aversion (2010) · cites this paper as Scheres et al., 2007
Functional MRI studies in ADHD have found decreased nucleus accumbens activation during reward anticipation.
“In addition, functional MRI studies in ADHD have found decreased NAcc activation during reward anticipation (Plichta et al., 2009; Scheres et al., 2007).”
From Reward circuit connectivity relates to delay discounting in children with attention-deficit/hyperactivity disorder (2013) · cites this paper as Scheres et al., 2007
Task-based fMRI studies have found atypical activation of the nucleus accumbens in ADHD during reward tasks.
“task-based fMRI studies have found atypical activation of this region while the participants performed a reward task.”
From Reward circuit connectivity relates to delay discounting in children with attention-deficit/hyperactivity disorder (2013) · cites this paper as Scheres et al., 2007
fMRI studies report decreased activation of the ventral striatum for both immediate and delayed rewards in adult and adolescent participants with ADHD compared with controls.
“Consistent with this, recent fMRI studies report decreased activation of the ventral striatum for both immediate and delayed rewards and in adult and adolescent participants with ADHD compared with controls (Plichta et al., 2009; Scheres et al., 2007).”
From Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity (2014) · cites this paper as Scheres et al., 2007
A parsimonious account of the current results and reward anticipation studies, if replicated, is that children with ADHD process the anticipation of monetary incentives or delay exposure differently from controls.
“A parsimonious account of the results of this study and that of the reward anticipation studies, if replicated (e.g.(Scheres et al., 2007) is that children with ADHD differentially process the anticipation of monetary incentives or delay exposure than control children.”
From Brain activation to cues predicting inescapable delay in adolescent Attention Deficit/Hyperactivity Disorder: An fMRI pilot study (2012) · cites this paper as Scheres et al., 2007
Recent studies have indicated deficits in the dopamine reward circuitry in ADHD, as predicted by developmental neurobiological models of the disorder.
“Recent studies have further indicated deficits in the dopamine reward circuitry,3–5 as predicted by developmental neurobiological models of the disorder.6–8”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [3]
Only a single study has focused on adolescents with ADHD (n=11), reporting decreased activation in the ventral striatum in the ADHD group compared to controls following cues predicting monetary gains, but not following cues predicting loss-avoidance, or in the outcome phase.
“To date, only a single study has focused on adolescents with ADHD (n=11), reporting decreased activation in the VS in the ADHD group (compared to controls) following cues predicting monetary gains, but not following cues predicting loss-avoidance, or in the outcome phase.3”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [3]
The relatively small sample size (n=11) and inclusion of both genders and mixed ADHD subtypes in the prior study make direct comparisons difficult.
“Yet the relatively small sample size in that study (n=11)3 and the inclusion of both genders and mixed ADHD subtypes (factors that have been associated with reward-related activation and impulsivity16,45) make direct comparisons difficult.”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [3]
Our findings agree with prior lack of group differences in neural activation to loss-avoidance anticipation but contradict prior reduced VS activation during gain anticipation.
“Our findings, while in agreement with the reported lack of significant group differences in neural activation to loss-avoidance anticipation, apparently contradict the demonstration of reduced activation in the VS during gain anticipation.3”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [3]
The single previous study that examined outcome-related activation in adolescents with ADHD focused solely on the VS and did not find group differences.
“Although in agreement with previous evidence from adults with ADHD,4 the single previous study that examined outcome-related activation in adolescents with ADHD had focused solely on the VS and did not find group differences.3”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [3]
MILT differed from MID-type paradigms in that conditioned cues predicted successful outcomes with greater certainty (~80% vs ~66%).
“MILT differed from MID-type paradigms used in earlier ADHD research in two ways: first, the conditioned cues predicted successful outcomes with greater certainty (∼80%, compared to ∼66%3,4).”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [3]
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- Authors
- Scheres, A., Milham, M. P., Knutson, B., & Castellanos, F. X.
- Affiliations
- University of Arizona (US)
- NYU Langone Health (US)
- Stanford University (US)
- Corresponding author
- Scheres, Anouk
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2007-03
- Volume
- 61
- Issue
- 5
- Pages
- 720-724
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2031254430
- Cited by
- 499
- References
- 30
- Citations by year
- 2026: 11 · 2025: 7 · 2024: 8 · 2023: 16 · 2022: 5 · 2021: 19 · 2020: 19 · 2019: 25 · 2018: 23 · 2017: 24 · 2016: 37 · 2015: 29 · 2014: 36 · 2013: 37 · 2012: 42
- FWCI
- 18.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- National Institute of Mental Health (MH0660393)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- attention deficit hyperactivity disorder, ventral striatum, reward anticipation, reward processing, hyperactivity/impulsivity, adolescents, executive dysfunction
- MeSH terms
- Adolescent, Attention Deficit Disorder with Hyperactivity, Basal Ganglia, Brain Mapping, Child, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Oxygen, Reaction Time, Reward, Case-Control Studies
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