Developmental differences in posterior mesofrontal cortex recruitment by risky rewards

Abstract

Might increased risk taking in adolescence result in part from underdeveloped conflict-monitoring circuitry in the posterior mesofrontal cortex (PMC)? Adults and adolescents underwent functional magnetic resonance imaging during a monetary game of "chicken." As subjects watched ostensible winnings increase over time, they decided when to press a button to bank their winnings, knowing that if they did not stop pursuing money reward before a secret varying time limit, they would "bust" and either lose the money accrued on the current trial (low-penalty trials) or forfeit trial winnings plus a portion of previous winnings (high-penalty trials). Reward accrual at risk of low penalty (contrasted with guaranteed reward) activated the PMC in adults but not in adolescents. Across all subjects, this activation (1) correlated positively with age but negatively with risk exposure and (2) was greater when subjects busted on the previous low-penalty trial. Reward accrual at risk of high penalty was terminated sooner and recruited the PMC in both adults and adolescents when contrasted with guaranteed reward. Predecision PMC activation in the high-penalty trials was significantly reduced in trials when subjects busted. These data suggest that (1) under threat of an explicit severe penalty, recruitment of the PMC is similar in adolescents and adults and correlates with error avoidance, and (2) when potential penalties for a rewarding behavior are mild enough to encourage some risk taking, predecision PMC activation by a reward/risk conflict is sensitive to previous error outcomes, predictive of risk-aversive behavior in that trial, and underactive in adolescents.

Figure 1.

Diagram of the RTT. The RTT presented subjects with four types of pseudorandomly presented trials (duration 14 s; n = 24 each). In motor control trials, subjects pressed on cue twice (to the $ cue and to the word press) for no incentive. In no-penalty trials, subjects began accruing money after pressing in response to the $ cue and accumulated winnings throughout the trial with no chance of penalty. In low-penalty trials, each trial was assigned a secret time limit of either 4, 6, 8, or 10 s after the $ cue, during which the subject was allowed to accumulate money. If the subject voluntarily stopped reward accrual before the secret time limit (top bifurcated outcome), he or she added accrued trial winnings to total winnings. If he or she failed to stop reward accrual before the secret time limit (bottom bifurcated outcome), he or she busted and forfeited all winnings in that trial and was instructed to press a second time. In high-penalty trials, subjects were also required to terminate reward accrual before the secret varying time limit, but busts resulted in subtraction of trial-accumulated winnings from previous winnings.

Figure 2.

RTT behavior. A, Mean time to respond with the first press to the $ cue was significantly slower in adolescents in motor control, no-penalty, and high-penalty trial types. B, Reward accrual time (and therefore risky reward pursuit) did not significantly differ between adults and adolescents. Both groups on average terminated accrual in the high-penalty trials before penalty outcomes could occur. Error bars indicate SEM. * p < 0.05.

Figure 3.

Affect ratings reported on postscan questionnaire. A–D, Self-reports (scale 0–3) of feeling anxious (A), happy (B), excited (C), and bored (D) when playing the motor control (MC), no-penalty (NP), low-penalty (LP), and high-penalty (HP) trials of the RTT. The group by trial type interaction effect on anxiety ratings (but not the other mood ratings) was significant (p < 0.0001), where self-reported anxiety reflected the magnitude of potential penalty in adults but not adolescents. Group-wise differences (p < 0.05) are indicated by an asterisk. All 20 adult subjects reported “0” boredom in penalty trials. Error bars indicate SEM.

Figure 4.

Brain activation by risky versus nonrisky reward accrual. A, B, Adults (A) but not adolescents (B) showed significant recruitment of the PMC during accrual of reward at risk of forfeiture of reward for that trial (low penalty) contrasted with reward accrual at no risk of forfeiture. C, This resulted in a net activation decrement among adolescents when adults and adolescents were compared in a voxelwise t test. D, E, Accruing reward at the risk of forfeiture of reward for that trial plus loss of an identical amount of previous winnings (high penalty) contrasted with accruing certain reward, activating the PMC in both adults (D) and adolescents (E), with no group activation differences.

Figure 5.

Trial-wise BOLD signal in a region of the PMC previously reported to be activated by a variety of predecision conflict imaging paradigms (shown in white in the inset of the brain image). Signal change did not differ between adults and adolescents in motor control and no-penalty reward trials. A, B, In both low-penalty (A) and high-penalty (B) trials, there were significant group by time interaction effects on BOLD signal, with reduced or delayed signal increases in adolescents. Asterisks denote significant signal differences (p < 0.05) at individual time points. Error bars indicate SEM. C, In low-penalty trials, when subjects took more risks, age correlated positively with peak predecision PMC signal increases (leverage plot) after controlling for RT to initiate the trial (task engagement) and individual differences in reward accrual time (risk-taking). D, Reward accrual time negatively correlated with PMC signal after controlling for age and RT to initiate the trial (leverage plot).

Figure 6.

A–F, Behavior change and predecision PMC signal change in penalty trials as a function of error outcomes in the current (A, B) or previous (C–F) penalty trial of that type. A, In low-penalty trials, predecision PMC signal change did not differ between win and bust outcomes but was significantly lower in adolescents in both successful and busted trials. B, In high-penalty trials, predecision PMC signal increase was lower in trials when subjects ultimately busted compared with trials with wins. C, D, Duration of risky reward accrual (in nonbusted trials) was reduced in low-penalty trials that followed a bust in the previous low-penalty trial (C) but did not differ in (nonbusted) high-penalty trials as a function of previous high-penalty trial outcome (D). E, F, Predecision PMC signal increase was significantly greater in low-penalty trials that were preceded by a bust in the previous low-penalty trial (E), and there was a trend for greater activation in high-penalty trials that followed a bust in the previous high-penalty trial (F). There were no interaction effects of age group on error-related behavior or signal change differences. *p < 0.10; **p < 0.05; ***p < 0.01. Error bars indicate SEM.