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Cited by 142Neural and Behavioral Psychology StudiesSubstance Abuse Treatment and OutcomesPsychopathy, Forensic Psychiatry, Sexual Offending

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

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Crowley, Thomas J., Dalwani, Manish S., Mikulich-Gilbertson, Susan K., Du, Yiping P., Lejuez, Carl W., Raymond, Kristen M., Banich, Marie T.·2010·PLoS ONE
DOI 10.1371/journal.pone.0012835PMC PMC2943904
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Abstract

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/PRINCIPAL 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, amygdala, 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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Figure 1 Schematic illustration of dysphoria induced by repeated intoxication-withdrawal cycles. Each intoxication leads to a subjective “high”, with enhanced response to reward due to reduced reward thresholds in medial forebrain bundle. Each acute withdrawal event results in subjective dysphoria with reduced response to reward due to elevated reward thresholds. Frequent cycle repetitions gradually suppress subjective “highs”, deepening dysphoria by further raising reward thresholds. Increasingly, the drug is used to escape dysphoria and achieve normal mood. During abstinence, mood recovers very slowly. (Based on Koob and Volkow [33]).
Figure 1 Schematic illustration of dysphoria induced by repeated intoxication-withdrawal cycles. Each intoxication leads to a subjective “high”, with enhanced response to reward due to reduced reward thresholds in medial forebrain bundle. Each acute withdrawal event results in subjective dysphoria with reduced response to reward due to elevated reward thresholds. Frequent cycle repetitions gradually suppress subjective “highs”, deepening dysphoria by further raising reward thresholds. Increasingly, the drug is used to escape dysphoria and achieve normal mood. During abstinence, mood recovers very slowly. (Based on Koob and Volkow [33]).CC BY · PubMed Central
Figure 2 Colorado Balloon Game. A. Decision-Balloon screen, yellow light illuminated. Counter initially $5. B. Events during presentation of 90 paired trials, each Decision Balloon (DecBa) followed by a Directed Balloon (DirBa). Top: timing (seconds). Colored circles represent stoplight lights. DecBa begins (B, upper): yellow light illuminated 4 sec, subject decides to press left (L) or right (R) button. Green light (0.5 sec), subject executes response. Red light, consequence appears (3.5 sec). Risky right press consequence, either: (a) “smiley face”, expanding balloon, puffing sounds, counter adds 5 cents, or (b) “pop” sound, shrinking balloon, “frowney face”, counter loses 10 cents. Cautious left press consequence: +1 cent on counter, dull “thud” sound, unchanged balloon. Then, “jittered” fixation. DirBa's (B, lower) are identical to their paired DecBa's except: only half of initial yellow light illuminates, signaling (i) start of a DirBa and (ii) button to press during green light (e.g., right illumination – press right) – the same button chosen during preceding paired DecBa. Green-light press on directed button: +2 cents on counter. Then balloon repeats the consequence (puff up, pop, or no change) of previous paired DecBa; subject was told that DirBa consequences would not affect earnings. Finally, jittered fixation screen. C. During DecBa, declining proportion of right presses programmed to win as game progresses. Mostly pressing left later in game saves earnings. D. Visual Analog Scales (VAS). After sessions subjects rated their opinions about the stated questions on 100mm lines. Marked positions represent all-subject means; groups did not differ significantly. Upper VAS: subjects' understanding of decision-making source for DecBa vs. DirBa. Lower VAS: Different emotional responses to puff-ups or pops of DecBa, vs. DirBa. E. Mean numbers, DecBa selections.
Figure 2 Colorado Balloon Game. A. Decision-Balloon screen, yellow light illuminated. Counter initially $5. B. Events during presentation of 90 paired trials, each Decision Balloon (DecBa) followed by a Directed Balloon (DirBa). Top: timing (seconds). Colored circles represent stoplight lights. DecBa begins (B, upper): yellow light illuminated 4 sec, subject decides to press left (L) or right (R) button. Green light (0.5 sec), subject executes response. Red light, consequence appears (3.5 sec). Risky right press consequence, either: (a) “smiley face”, expanding balloon, puffing sounds, counter adds 5 cents, or (b) “pop” sound, shrinking balloon, “frowney face”, counter loses 10 cents. Cautious left press consequence: +1 cent on counter, dull “thud” sound, unchanged balloon. Then, “jittered” fixation. DirBa's (B, lower) are identical to their paired DecBa's except: only half of initial yellow light illuminates, signaling (i) start of a DirBa and (ii) button to press during green light (e.g., right illumination – press right) – the same button chosen during preceding paired DecBa. Green-light press on directed button: +2 cents on counter. Then balloon repeats the consequence (puff up, pop, or no change) of previous paired DecBa; subject was told that DirBa consequences would not affect earnings. Finally, jittered fixation screen. C. During DecBa, declining proportion of right presses programmed to win as game progresses. Mostly pressing left later in game saves earnings. D. Visual Analog Scales (VAS). After sessions subjects rated their opinions about the stated questions on 100mm lines. Marked positions represent all-subject means; groups did not differ significantly. Upper VAS: subjects' understanding of decision-making source for DecBa vs. DirBa. Lower VAS: Different emotional responses to puff-ups or pops of DecBa, vs. DirBa. E. Mean numbers, DecBa selections.CC BY · PubMed Central
Figure 3 Selected regions more activated in one group (patients or controls) than in the other. Regions significantly more activated in controls than in patients: Left column, during decision-making (cf. Table 5 for contrast and details); middle column, while experiencing wins (cf. Table 8 for contrast and details). Regions significantly more activated in patients than in controls: right column, while experiencing losses (cf. Table 11 for contrast and details). Row 2: left is at bottom. Rows 3–6: left is at left. Values of “y”: for slices in that row, distance (mm) rostral (+) or caudal (−) from anterior commissure. Numbered regions: 1, middle frontal gyrus BA 10; 2, middle temporal gyrus BA 21; 3, medial frontal gyrus BA 9; 4, uvula (vermis) and pyramis; 5, medial frontal gyrus BA 10; 6, middle frontal gyrus BA 11, 47; 7, anterior cingulate BA 24, 32; 8, middle frontal gyrus BA 11; 9, superior frontal gyrus BA 8; 10, middle frontal gyrus BA 11, 47; 11, anterior cingulate BA 24; 12, putamen; 13, superior temporal gyrus, BA 38; 14, insula BA 13; 15, superior temporal gyrus BA 22; 16, middle frontal gyrus BA 6; 17, insula BA 13; 18, amygdala; 19, middle and inferior temporal gyri BA 21; 20, inferior temporal gyrus BA 21.
Figure 3 Selected regions more activated in one group (patients or controls) than in the other. Regions significantly more activated in controls than in patients: Left column, during decision-making (cf. Table 5 for contrast and details); middle column, while experiencing wins (cf. Table 8 for contrast and details). Regions significantly more activated in patients than in controls: right column, while experiencing losses (cf. Table 11 for contrast and details). Row 2: left is at bottom. Rows 3–6: left is at left. Values of “y”: for slices in that row, distance (mm) rostral (+) or caudal (−) from anterior commissure. Numbered regions: 1, middle frontal gyrus BA 10; 2, middle temporal gyrus BA 21; 3, medial frontal gyrus BA 9; 4, uvula (vermis) and pyramis; 5, medial frontal gyrus BA 10; 6, middle frontal gyrus BA 11, 47; 7, anterior cingulate BA 24, 32; 8, middle frontal gyrus BA 11; 9, superior frontal gyrus BA 8; 10, middle frontal gyrus BA 11, 47; 11, anterior cingulate BA 24; 12, putamen; 13, superior temporal gyrus, BA 38; 14, insula BA 13; 15, superior temporal gyrus BA 22; 16, middle frontal gyrus BA 6; 17, insula BA 13; 18, amygdala; 19, middle and inferior temporal gyri BA 21; 20, inferior temporal gyrus BA 21.CC BY · PubMed Central
Figure 4 DecBa BOLD activity minus DirBa BOLD activity during yellow-light decision periods for patients and controls. Mean DecBa-minus-DirBa values are shown for patients, and separately for controls, in brain regions with significant control-patient differences (see Table 5). Negative deflections in some regions indicate that subjects' mean activity there was less during DecBa than during DirBa. Some regions extend across several anatomical structures. Some structures appear more than once because they contained more than one activated cluster. SPM activation units: see Methods. Abbreviations: Ant, anterior. Gy, gyrus. Med, medial. Pre-SMA, region immediately anterior to the supplementary motor area. Sup, superior.
Figure 4 DecBa BOLD activity minus DirBa BOLD activity during yellow-light decision periods for patients and controls. Mean DecBa-minus-DirBa values are shown for patients, and separately for controls, in brain regions with significant control-patient differences (see Table 5). Negative deflections in some regions indicate that subjects' mean activity there was less during DecBa than during DirBa. Some regions extend across several anatomical structures. Some structures appear more than once because they contained more than one activated cluster. SPM activation units: see Methods. Abbreviations: Ant, anterior. Gy, gyrus. Med, medial. Pre-SMA, region immediately anterior to the supplementary motor area. Sup, superior.CC BY · PubMed Central
Figure 5 Influences of ADHD, depression, tobacco smoking, prescription medications, or handedness on control-patient group differences. Right sagittal view. Explanation in Methods and Results.
Figure 5 Influences of ADHD, depression, tobacco smoking, prescription medications, or handedness on control-patient group differences. Right sagittal view. Explanation in Methods and Results.CC BY · PubMed Central

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Cites

Research works printed but not linked: 2

  1. 2000, Diagnostic and Statistical Manual of Mental Disorders 4th Edition, Text Revision
  2. TJ Crowley, 1998, Substance-dependent, conduct-disordered adolescent males: Severity of diagnosis predicts two-year outcome., Drug Alcohol Depend, 49, 225

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Metadata

Authors
Crowley, T. J., Dalwani, M. S., Mikulich-Gilbertson, S. K., Du, Y. P., Lejuez, C. W., Raymond, K. M., & Banich, M. T.
Affiliations
  • University of Colorado Denver (US)
  • University of Maryland, College Park (US)
  • University of Colorado Boulder (US)
Corresponding author
Crowley, Thomas J.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2010-09-22
Volume
5
Issue
9
Pages
e12835
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0012835
PMC
PMC2943904
OpenAlex
W2121848896
Cited by
142
References
93
Citations by year
2026: 3 · 2025: 5 · 2024: 6 · 2023: 8 · 2022: 5 · 2021: 2 · 2020: 8 · 2019: 13 · 2018: 10 · 2017: 10 · 2016: 12 · 2015: 22 · 2014: 10 · 2013: 13 · 2012: 6
FWCI
5.22
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • KU ScholarWorks (The University of Kansas) (submittedVersion, other-oa)
Funders
  • U.S. Public Health Service (011015)
  • National Institute on Drug Abuse (P60DA011015, DA009842, R37DA009842, R01DA009842)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
  • Social Sciences › Psychology › Clinical Psychology › Psychopathy, Forensic Psychiatry, Sexual Offending
Keywords
risky decision making, adolescent boys, substance use disorders, conduct disorder, reward processing, punishment processing, orbitofrontal cortex, dorsolateral prefrontal cortex, anterior cingulate cortex, cerebellum, brainstem, risk-taking
MeSH terms
Adolescent, Antisocial Personality Disorder, Brain, Brain Mapping, Decision Making, Humans, Magnetic Resonance Imaging, Male, Risk-Taking, Substance-Related Disorders, Young Adult

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