A pathway linking reward circuitry, impulsive sensation-seeking and risky decision-making in young adults: identifying neural markers for new interventions

Abstract

High trait impulsive sensation seeking (ISS) is common in 18-25-year olds, and is associated with risky decision-making and deleterious outcomes. We examined relationships among: activity in reward regions previously associated with ISS during an ISS-relevant context, uncertain reward expectancy (RE), using fMRI; ISS impulsivity and sensation-seeking subcomponents; and risky decision-making in 100, transdiagnostically recruited 18-25-year olds. ISS, anhedonia, anxiety, depression and mania were measured using self-report scales; clinician-administered scales also assessed the latter four. A post-scan risky decision-making task measured 'risky' (possible win/loss/mixed/neutral) fMRI-task versus 'sure thing' stimuli. 'Bias' reflected risky over safe choices. Uncertain RE-related activity in left ventrolateral prefrontal cortex and bilateral ventral striatum was positively associated with an ISS composite score, comprising impulsivity and sensation-seeking-fun-seeking subcomponents (ISSc; P⩽0.001). Bias positively associated with sensation seeking-experience seeking (ES; P=0.003). This relationship was moderated by ISSc (P=0.009): it was evident only in high ISSc individuals. Whole-brain analyses showed a positive relationship between: uncertain RE-related left ventrolateral prefrontal cortical activity and ISSc; uncertain RE-related visual attention and motor preparation neural network activity and ES; and uncertain RE-related dorsal anterior cingulate cortical activity and bias, specifically in high ISSc participants (all ps<0.05, peak-level, family-wise error corrected). We identify an indirect pathway linking greater levels of uncertain RE-related activity in reward, visual attention and motor networks with greater risky decision-making, via positive relationships with impulsivity, fun seeking and ES. These objective neural markers of high ISS can guide new treatment developments for young adults with high levels of this debilitating personality trait.

Figure 1

Reward paradigm design. (a) Trial structure demonstrating choice phase, anticipation phase, numerical feedback and outcome (win, loss and neutral). (b) Description of the outcomes associated with each of the four stimuli (win, mixed, neutral and loss respectively). Transition probabilities are 0.5 except for the neutral stimulus. (c) Example of a post-task trial, in which participant has to choose between card stimulus and ‘sure thing' option.

Figure 2

(a) Associations between ISSc with left vlPFC (blue; r=0.32, P=0.001) and left VS (red; r=0.28, P=0.005). (b) Association between SSS ES and bias score (r=0.29, P=0.006). These figures show relationships without the addition of covariates. The relationships remained significant with the addition of covariates (see Results). ES, experience seeking; ISSc, impulsive sensation seeking subcomponents; SSS, Sensation Seeking Scale; vIPFC, ventrolateral prefrontal cortex; VS, ventral striatum.

Figure 3

Distinct patterns of association between reward expectancy (RE) and ISSc (red), and RE and SSS ES (blue). Both maps thresholded at P<0.001 uncorrected, k=20 for display purposes. ES, experience seeking; ISSc, impulsive sensation seeking subcomponents; SSS, Sensation Seeking Scale. Scales reflect T statistics; numbers above axial slices reflect z coordinate of slice.