Risky Decisions and Their Consequences: Neural Processing by Boys with Antisocial Substance Disorder

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Issue Date
2010-09-22Author
Crowley, Thomas J.
Dalwani, Manish S.
Mikulich-Gilbertson, Susan K.
Du, Yiping P.
Lejuez, Carl W.
Raymond, Kristen M.
Banich, Marie T.
Publisher
Public Library of Science
Type
Article
Article Version
Scholarly/refereed, publisher version
Rights
© 2010 Crowley et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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BACKGROUND: Adolescents with conduct and substance problems (‘‘Antisocial Substance Disorder’’ (ASD)) repeatedly engage in risky antisocial and drug-using behaviors. We hypothesized that, during processing of risky
decisions and resulting rewards and punishments, brain activation would differ between abstinent ASD boys and comparison boys. METHODOLOGY/PRINCIPLE FINDINGS: We compared 20 abstinent adolescent male patients in treatment for ASD with 20 community controls, examining rapid event-related blood-oxygen-level-dependent (BOLD) responses during functional magnetic resonance imaging. In 90 decision trials participants chose to make either a cautious response that earned one cent, or a risky response that would either gain 5 cents or lose 10 cents; odds of losing increased as the game progressed. We also examined those times when subjects experienced wins, or separately losses, from their risky choices. We contrasted decision trials against very similar comparison trials requiring no decisions, using whole-brain
BOLD-response analyses of group differences, corrected for multiple comparisons. During
decision-making ASD boys showed hypoactivation in numerous brain regions robustly activated by controls, including orbitofrontal and dorsolateral prefrontal cortices, anterior cingulate, basal ganglia, insula, mygdala, hippocampus, and cerebellum. While experiencing wins, ASD boys had significantly less activity than controls in anterior cingulate, temporal regions, and cerebellum, with more activity nowhere. During losses ASD boys had significantly more activity than controls in
orbitofrontal cortex, dorsolateral prefrontal cortex, brain stem, and cerebellum, with less activity nowhere.CONCLUSIONS/SIGNIFICANCE: Adolescent boys with ASD had extensive neural hypoactivity during risky decision-making, coupled with decreased activity during reward and increased activity during loss. These neural patterns may underlie the dangerous, excessive, sustained risk-taking of such boys. The findings suggest that the dysphoria, reward insensitivity, and suppressed neural activity observed among older addicted persons also characterize youths early in the development of substance use disorders.
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Citation
Crowley TJ, Dalwani MS, Mikulich-Gilbertson SK, Du YP, Lejuez CW, Raymond KM, et al. (2010) Risky Decisions and Their Consequences: Neural Processing by Boys with Antisocial Substance Disorder. PLoS ONE 5(9): e12835. doi:10.1371/journal.pone.0012835
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