We explored maturational differences between adolescents and adults in motivational and consummatory components of incentive neurocircuitry. Both adolescents and adults showed significant recruitment of VS and mFC by the standard contrasts of the MID task, in accord with previous experiments on human incentive processing 
. We report here some additional evidence that developmental differences in limbic recruitment by instrumental behavior may depend on the component or stage of instrumental behavior 
. Chiefly, in accord with our hypothesis, we found that adolescents showed mildly reduced activation of the right NAcc by anticipation of responding for gains or to avoid losses, where in the VOI analysis, there was a mild positive correlation across all participants between age and net reward cue-elicited activation in the right NAcc. In contrast with our second hypothesis, adolescents did not show appreciable differences from adults in NAcc or mFC reactivity to reward deliveries. These findings essentially replicate results of our previous developmental comparison using the MID task 
. Our results were not appreciably affected when 12-year-old subjects (n
3) were excluded from analysis (supplemental Figures S3
An ancillary finding was that suprathreshold activation of ACC by loss outcomes (as a contrast with avoided losses) was present in adults but not adolescents. Despite how the direct group-wise activation difference did not survive FDR correction, we retain mention of this difference as a preliminary finding due to the extensive implication of this portion of ACC in error monitoring 
. In particular, adolescents have shown decrements relative to adults in ACC recruitment by pre-decision conflict when opting for rewards with a potential for error 
Among adolescent participants, neither recruitment of the NAcc by reward cues nor recruitment by reward deliveries correlated with either age or Tanner scores. Indeed, as illustrated in (parts E and F), there was greater variation of NAcc responses to potential reward within age group than between age groups. Extensive individual differences in VS responsiveness to fMRI task rewards has been found in other studies (e.g. 
). It may be that incentive neurocircuitry is essentially well-developed in the human brain by mid-to late- adolescence (the majority of adolescents were of Tanner stage 4+), with little remaining development-based variance. Surveying children across a wider (i.e. younger) age range or Tanner stage may be necessary to reveal clear developmental trends prior to adulthood.
Collectively, these findings, on the surface, do not generally support the opponent-process developmental account 
of adolescent risky behavior. We found essentially no evidence for increased mesolimbic responsiveness to either reward-predictive instrumental cues, or to actual reward deliveries in adolescents compared to adults. However, we note that any developmental deficit in behavior control resulting from some combination of overactive reward processing and deficient inhibitory processing would operate in an incentive- or context-specific manner—i.e. when the individual is offered a particular real-world risky incentive. It may be that other incentive paradigms may naturalistically reflect risky incentive scenarios (thus invoking maturationally-deficient dual-processing) better than the MID task.
The MID task features several unique characteristics compared to other incentive paradigms used in children that may explain divergent findings. First, the expected values (contingencies) signaled by anticipatory cues are trained in advance, such there is no discovery or learning in the task, except for discovery of trial-wise success. In particular, adolescents showed increased NAcc responsiveness to rewards of uncertain (secret) magnitude compared to adults 
, whereas subjects in this experiment were explicitly shown the exact (modest) amounts of money they won in a trial. Second, MID task visual stimuli are mundane compared to those of other incentive tasks (e.g. the pirate cartoons of 
and slot-machine wheels of 
). We note too that other tasks often feature risky decision-making and waiting for the outcomes of gambles 
, akin to placing a roulette wheel bet, and this is probably more entertaining than a simple MID reaction-time task. Third, the MID task requires unusual vigilance and anticipatory motor preparation- especially for high-incentive targets. Indeed, we cannot rule out that reduced attentional capacity contributed to blunted anticipatory NAcc activation in adolescents. Critically, impaired sleep is common among adolescents 
, and has been linked to deficient striatal recruitment during reward anticipation 
. In addition, both adults 
and adolescents 
with attention-deficit disorder have shown reduced reward-anticipatory activity in the MID task. It can be argued, however, that focused attention is simply one downstream manifestation of motivation, and that adolescents were simply not as motivated as adults to execute the instrumental responses. Finally, we note that in contrast to comparisons between mid-adolescents and very young adults (e.g. 
), we selected a somewhat older, post-college age group of adults that markedly differs from adolescents in general incidence of behavior-related mortality and morbidity (U.S. Centers for Disease Control).
Taken together with results from our previous experiment 
, these results indicate that if adolescents tend to have greater mesolimbic sensitivity to rewards, this does not generalize to all contexts or tasks. We believe that rather than being a source of confusion, these divergent findings present an intriguing avenue for future research. In particular, if adolescents show reduced motivational neurocircuitry recruitment in the context of mundane work for explicit rewards, but increased activation in the context of more entertaining tasks or non-explicit rewards, this could represent a maturational risk factor for behavior-related mortality and morbidity in adolescence within the domain of reward processing alone—all in the context of reduced top-down executive control. Put differently, in adolescents, there may be unusually great appeal in trying to win $10 racing the adjacent car to the next stoplight as opposed to earning it raking leaves. Of great interest are future experiments that parametrically modulate these different aspects of an incentive task within-subject
, across the course of a scan, so see if adolescents show greater modulation (interaction) of mesolimbic activation as a function of entertaining task features.
This study has limitations that should be considered. First, this experiment used explicit amounts of money as the incentive. As with any study of groupwise differences in mesolimbic recruitment by monetary incentives, we cannot rule out that observed differences resulted from the amounts of money at stake being more intrinsically valuable in one group compared to another. Therefore, these data may not generalize to other incentives. However, we note that there were no group differences in self-reported excitement or happiness at the prospect of winning money, or in reaction-time to incentivized targets. Also, the directionality of the observed difference in reward-anticipatory activation runs counter to an assumption that the monetary rewards would be more valuable to an adolescent compared to an adult wage-earner.
Second, there was a pronounced effect of incentive magnitude on RT, and by extension, on hit rates because the distribution of target durations for each task run was not varied across incentive amounts. It may be that the slower pace of this variant of the MID task made it easier, and enabled maximization of attentional resources of all subjects for the occasional high-value targets. This may also explain the lack of a correlation here between individual differences in self-reported excitement about high-reward cues and NAcc recruitment, which is often found in experiments using the original (briskly-paced) MID task (e.g. 
) The slow pace of trials, however, was the necessary trade-off in task design to promote separate detection of anticipation- versus notification-elicited BOLD signal. Third, the psychologically healthy adolescents scanned in this experiment are not at particular risk for adverse psychiatric outcomes. Rather, it is youth with histories of conduct disorder or other externalizing symptomatology who are most likely to engage in risky behaviors 
, including substance abuse 
. Notably, in another recent experiment 
, we found that unmedicated teens with externalizing disorders had significantly greater NAcc activation by notification of rewards and greater NAcc deactivation by missed rewards, compared to age- and gender-matched controls.
Finally, we note that these and other neurodevelopmental brain research findings are merely descriptive and correlational. Accordingly, we can only speculate that observed age-group differences in structure or function of incentive-related brain regions play a role in the increased behavior-related mortality and morbidity of adolescents. It may be that the maturation of incentive neurocircuitry by adolescence is essentially sufficient for rational decision-making, and that psychosocial or cultural factors may underlie increased engagement in risky behaviors among American adolescents 
. For example, within an economic, expected-utility framework, adolescent risk-taking has been described as rational in the context of social reinforcement contingencies unique to adolescence 
. However, in light of the extensively-documented maturational differences in structure and function of brain regions extensively implicated in incentive processing and in top-down executive control (reviewed in 
), we nevertheless raise the possibility that these neurodevelopmental differences may contribute to vulnerability of adolescents to mortality and morbidity to behavioral causes.
In conclusion, this experiment largely replicates findings from our initial investigation 
, where adolescents showed reduced recruitment of the right NAcc by reward-predictive cues, but similar activation of mesolimbic incentive-motivational neurocircuitry to reward notifications. In addition, we found significant recruitment of ACC by notification of losses in adults but not adolescents. Future experiments could expand on these findings by artificially manipulating instrumental trial outcomes (such as omissions of expected rewards), and could reconcile divergent findings of maturational differences in incentive processing by modulating stimulus or other features of incentive tasks.