Incentive-elicited mesolimbic activation and externalizing symptomatology in adolescents.
BACKGROUND
Opponent-process theories of externalizing disorders (ExD) attribute them to some combination of overactive reward processing systems and/or underactive behavior inhibition systems. Reward processing has been indexed by recruitment of incentive-motivational neurocircuitry of the ventral striatum (VS), including nucleus accumbens (NAcc).


METHODS
We used functional magnetic resonance imaging (fMRI) with an incentive task to determine whether externalizing symptomatology in adolescence is correlated with an enhanced VS recruitment by cues for rewards, or by deliveries of rewards. Twelve community-recruited adolescents with externalizing disorders (AED) and 12 age/gender-matched controls responded to targets to win or avoid losing $0, $0.20, $1, $5, or an unknown amount (ranging from $0.20 to $5).


RESULTS
Cues to respond for rewards activated the NAcc (relative to cues for no incentive), in both subject groups similarly, with greatest NAcc recruitment by cues for the largest reward. Loss-anticipatory NAcc signal increase was detected in a volume-of-interest analysis - but this increase occurred only in trials when subjects hit the target. Relative to controls, AED showed significantly elevated NAcc activation by a linear contrast between reward notification versus notification of failure to win reward. In a post hoc reanalysis, VS and pregenual anterior cingulate activation by the reward versus non-reward outcome contrast also directly correlated with Child Behavior Checklist (CBCL) Externalizing total scores (across all subjects) in lieu of a binary diagnosis. Finally, both groups showed right insula activation by loss notifications (contrasted with avoided losses).


CONCLUSIONS
Externalizing behavior, whether assessed dimensionally with a questionnaire, or in the form of a diagnostic categorization, is associated with an exaggerated limbic response to outcomes of reward-directed behavior. This could be a neurobiological signature of the behavioral sensitivity to laboratory reward delivery that is characteristic of children with externalizing symptomatology. Of interest is future research on incentive-motivational processing in more severe, clinically referred AED.
Bjork
James M
JM
Division of Clinical Neuroscience and Behavioral Research, National Institute on Drug Abuse, National Institutes of Health (NIH), Bethesda, MD 20892, USA. jbjork@mail.nih.gov
Chen
Gang
G
Smith
Ashley R
AR
Hommer
Daniel W
DW
D000293:Adolescent; D001143:Arousal / Q000502:physiology*; D001289:Attention Deficit Disorder with Hyperactivity / Q000175:diagnosis / Q000503:physiopathology / Q000523:psychology; D019958:Attention Deficit and Disruptive Behavior Disorders / Q000175:diagnosis / Q000503:physiopathology / Q000523:psychology; D001479:Basal Ganglia / Q000503:physiopathology; D001931:Brain Mapping; D002540:Cerebral Cortex / Q000503:physiopathology; D002653:Child Behavior Disorders / Q000175:diagnosis / Q000503:physiopathology* / Q000523:psychology; D019955:Conduct Disorder / Q000175:diagnosis / Q000503:physiopathology* / Q000523:psychology; D003463:Cues; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D007266:Inhibition, Psychological; D007389:Internal-External Control; D007721:Knowledge of Results, Psychological; D008032:Limbic System / Q000503:physiopathology*; D008279:Magnetic Resonance Imaging; D008297:Male; D008636:Mesencephalon / Q000503:physiopathology*; D009042:Motivation; D009415:Nerve Net / Q000503:physiopathology*; D009714:Nucleus Accumbens / Q000503:physiopathology; D010100:Oxygen / Q000097:blood*; D010364:Pattern Recognition, Visual / Q000502:physiology; D011597:Psychomotor Performance / Q000502:physiology; D011930:Reaction Time / Q000502:physiology; D011999:Recruitment, Neurophysiological / Q000502:physiology*
D010100:Oxygen