Adolescents' Neural Processing of Risky Decisions: Effects of Sex and Behavioral Disinhibition

Abstract

BackgroundAccidental injury and homicide, relatively common among adolescents, often follow risky behaviors; those are done more by boys and by adolescents with greater behavioral disinhibition (BD).HypothesisNeural processing during adolescents' risky decision-making will differ in youths with greater BD severity, and in males vs. females, both before cautious behaviors and before risky behaviors.Methodology/Principal Findings81 adolescents (Patients with substance and conduct problems, and comparison youths (Comparisons)), assessed in a 2 x 2 design (Patients:Comparisons x Male:Female) repeatedly decided between doing a cautious behavior that earned 1 cent, or a risky one that either won 5 or lost 10 cents. Odds of winning after risky responses gradually decreased. Functional magnetic resonance imaging captured brain activity during 4-sec deliberation periods preceding responses. Most neural activation appeared in known decision-making structures. Patients, who had more severe BD scores and clinical problems than Comparisons, also had extensive neural hypoactivity. Comparisons' greater activation before cautious responses included frontal pole, medial prefrontal cortex, striatum, and other regions; and before risky responses, insula, temporal, and parietal regions. Males made more risky and fewer cautious responses than females, but before cautious responses males activated numerous regions more than females. Before risky behaviors female-greater activation was more posterior, and male-greater more anterior.Conclusions/SignificanceNeural processing differences during risky-cautious decision-making may underlie group differences in adolescents' substance-related and antisocial risk-taking. Patients reported harmful real-life decisions and showed extensive neural hypoactivity during risky-or-cautious decision-making. Males made more risky responses than females; apparently biased toward risky decisions, males (compared with females) utilized many more neural resources to make and maintain cautious decisions, indicating an important risk-related brain sexual dimorphism. The results suggest new possibilities for prevention and management of excessive, dangerous adolescent risk-taking.

Sex differences in animal models of decision making

“…The authors found that the OFC in females was more dynamically engaged than males during task performance (Lee et al 2009): while there were no correlations between neural activity and behavior in males, there was a negative correlation between neural activity in the OFC and choice of the uncertain reward when preceded by a punished outcome (i.e., no reward delivery) and a positive correlation between OFC neural signal and choice of the uncertain outcome when preceded by a uncertain, but unpunished, outcome. Interestingly, in a recent study (Crowley et al 2015), males had greater OFC activation than females prior to making safe choices in another risk-based decision-making task. These last two studies suggest that the OFC in females may be more selectively tuned to process punishment and uncertainty whereas the OFC in males may be more selectively recruited to process information regarding safe reinforcement.…”

Brain circuitry associated with the development of substance use in bipolar disorder and preliminary evidence for sexual dimorphism in adolescents

“…Ventral and paralimbic cortical regions implicated, i.e. OFC, insular and temporopolar cortices, are associated with affective processing and regulation, self-awareness, stimulus-reinforcement associations, behavioral control and risky decision making (Clark et al 2008; Craig 2002; Crowley et al 2015; Etkin et al 2011; Fellows 2007; Kringelbach and Rolls 2004; Manes et al 2002; Modinos et al 2009; Muhlert and Lawrence 2015; Rolls 2004; Van Leijenhorst et al 2010; Xue et al 2010). …”

Children’s brain activation during risky decision-making: A contributor to substance problems?

“…Such alternatives force risky-vs.-cautious decisions. Unfortunately, many decision-making brain structures are hypoactive as adolescents with substance and/or conduct problems process risky-vs.-cautious decisions (Crowley et al, 2015; Heitzeg et al, 2014; Jones et al, 2016; Shanmugan et al, 2016). Reported regions have included, e.g.…”

“…To assess that possibility we examined in elementary-school children the association between severity of externalizing behavior and regional intensity of neural activation during risky-vs.-cautious decision-making, using the same decision-making game that we had employed earlier in adolescents with severe substance and conduct problems (Crowley et al, 2015). Seeking children with minimal or no substance exposure, we recruited 9–11 year-olds, since many children who will develop substance problems are using regularly by age 13 (Young et al, 1995).…”

“…Growing evidence from adolescents also had shown sex differences in both severity of externalizing behaviors (Dodge et al, 2006) and brain activation during risky decision-making (Crowley et al, 2015). Therefore, we additionally hypothesized that in these young children, neural activation patterns would show significant sex differences during risky-or-cautious decision-making.…”