Incentive-elicited mesolimbic activation and externalizing symptomatology in adolescents.

Division of Clinical Neuroscience and Behavioral Research, National Institute on Drug Abuse, National Institutes of Health (NIH), Bethesda, MD 20892, USA.
Journal of Child Psychology and Psychiatry (Impact Factor: 5.42). 12/2009; 51(7):827-37. DOI: 10.1111/j.1469-7610.2009.02201.x
Source: PubMed

ABSTRACT 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).
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).
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).
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.

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    ABSTRACT: Background Children with early-onset Disruptive Behavior Disorders (DBD), especially those with callous-unemotional traits, are at risk of developing persistent and severe adult antisocial behavior. One possible underlying mechanism for persistence is deficient reward and loss sensitivity, i.e. deficient incentive processing. However, little is known about the relation between deficient incentive processing and persistence of antisocial behavior into adulthood, or its relation with callous-unemotional and other psychopathic traits. In this study, we investigate the relationship between the neural correlates of incentive processing and both DBD persistence and psychopathic traits. Methods In a sample of 128 adolescents (mean age 17.7) with a history of criminal offending before age 12, functional Magnetic Resonance Imaging was performed during a Monetary Incentive Delay task designed to assess neural responses during incentive processing. Neural activation during incentive processing was then associated with DBD persistence and psychopathic traits, measured with the Youth Psychopathic traits Inventory (YPI). Results Compared to both healthy controls and youths who had desisted from DBD, persistent DBD subjects showed lower neural responses in the ventral striatum during reward outcomes and higher neural responses in the amygdala during loss outcomes. Callous-unemotional traits were related to lower neural responses in the amygdala during reward outcomes, while other psychopathic traits were not related to incentive processing. Conclusions In the current study, aberrant incentive processing is related to persistence of childhood antisocial behavior into late adolescence and to callous-unemotional traits. This mechanism may underlie treatment-resistance in a subgroup of antisocial youth and provide a target for intervention.
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    ABSTRACT: Functional magnetic resonance imaging (fMRI) has illuminated the development of human brain function. Some of this work in typically-developing youth has ostensibly captured neural underpinnings of adolescent behavior which is characterized by risk-seeking propensity, according to psychometric questionnaires and a wealth of anecdote. Notably, cross-sectional comparisons have revealed age-dependent differences between adolescents and other age groups in regional brain responsiveness to prospective or experienced rewards (usually greater in adolescents) or penalties (usually diminished in adolescents). These differences have been interpreted as reflecting an imbalance between motivational drive and behavioral control mechanisms, especially in mid-adolescence, thus promoting greater risk-taking. While intriguing, we caution here that researchers should be more circumspect in attributing clinically significant adolescent risky behavior to age-group differences in task-elicited fMRI responses from neurotypical subjects. This is because actual mortality and morbidity from behavioral causes (e.g. substance abuse, violence) by mid-adolescence is heavily concentrated in individuals who are not neurotypical, who rather have shown a lifelong history of behavioral disinhibition that frequently meets criteria for a disruptive behavior disorder, such as conduct disorder, oppositional-defiant disorder, or attention-deficit hyperactivity disorder. These young people are at extreme risk of poor psychosocial outcomes, and should be a focus of future neurodevelopmental research.
    Developmental Cognitive Neuroscience 08/2014; 11. DOI:10.1016/j.dcn.2014.07.008 · 3.71 Impact Factor


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May 27, 2014