AED did not differ from controls in VS recruitment by reward-anticipatory cues. Rather, AED showed greater VS activation by the contrast between receiving versus not receiving rewards in reward trials. Reward (hit) and nonreward (miss) notifications in reward trials, when analyzed separately, indicted that the group difference in the contrast activation resulted from both greater VS activation by reward notifications in AED as well as greater VS deactivation by nonreward notifications in AED. Substituting CBCL-externalizing scale scores for the dichotomous ExD diagnosis also revealed a direct voxelwise correlation between externalizing symptomatology and reward-outcome-elicited activation. It appears, then, that the motivational neurocircuitry of AED with predominantly ODD/CD symptomatology is more sensitive to instrumental reward trial outcomes, but there were no significant group differences in response-anticipatory
. Finally, loss notifications activated right anterior insula in both groups. This is consistent with previous data implicating anterior insula in the mental representation of affective reactions during incentive tasks (Paulus, Rogalsky, Simmons, Feinstein, & Stein, 2003
As with previous experiments (Bjork, Hommer, Grant, & Danube, 2004
; Bjork, Smith, & Hommer, 2008
; Knutson, Adams et al., 2001
), BOLD signal change in a NAcc VOI correlated with individual differences in self-reported excitement upon seeing the high-reward-predictive cue. Interestingly, the VOI analysis also revealed that anticipatory NAcc activation by prospective losses was evident in successful trials only. Conversely, anticipatory NAcc activation by prospective gains was similar during both successful and unsuccessful trials. This suggests that in adolescents, the NAcc is more consistently recruited across trials by the prospect of winning rewards than by the prospect of avoiding losses.
The greater NAcc and ACC activation by notification of rewards in the AED may be a neurophysiological reflection of how externalizing children show greater behavioral sensitivity to gains in laboratory decision tasks (Lane & Cherek, 2001
; Matthys et al., 1998
; Matthys, van Goozen, Snoek, & van Engeland, 2004
) and is possibly a manifestation or underpinning of a heritable, generalized behavioral risk factor for SUD (Giancola & Moss, 1998
) identified in large-scale twin (Iacono, Carlson, Taylor, Elkins, & McGue, 1999
; Slutske et al., 1998
; Slutske et al., 2002
; Young et al., 2000
) and longitudinal (Clark, Kirisci, & Moss, 1998
) studies. Interestingly, the exaggerated VS activation by the reward versus nonreward outcome contrast in AED seen here is similar to that of adults with SUD (Bjork et al., 2008
We did not replicate the VS deficit in reward-anticipation activation previously reported in adolescents (Scheres et al., 2007
) and adults (Strohle et al., 2008
) with ADHD. In contrast, we replicated findings of more prominent mesofrontal cortex activation by reward vs nonreward notifications in adults with ADHD (Strohle et al., 2008
). We posit that the key difference was that our subjects primarily had ODD or CD with additional subclinical internalizing symptoms. In contrast, a population selected primarily for “cold-cognitive” attentional decrements may be more vulnerable to reduced VS response to reward anticipation in the MID, because it requires intense vigilance.
This study has several limitations. First, the AED were diagnostically-mixed, reflecting the common co-occurrence of ADHD, ODD and CD, thus compromising syndrome specificity. However, we also included a dimensional approach in addition to binary diagnostic classification. Second, the sample size is modest. However, it nonetheless revealed both a significant group difference in NAcc activation by the reward notification contrast, and no trend toward a group difference in Nacc recruitment by anticipatory cues (to warrant additional subject recruitment). Third, the lack of anticipation-related activation differences may have resulted from our use of a community-recruited sample of AED. Although this mitigated medication confounds, a clinically-referred sample with severe symptomatology might show more activation differences. Fourth, while the scanning range of this study provided fine spatial resolution in the NAcc and the ventral mFC, it missed potential task-elicited activations in superior cerebrum. Finally, although applicants who met lifetime criteria for an affective disorder were excluded, AED also had significantly elevated internalizing symptoms, as is reported in epidemiological study (Boylan, Vaillancourt, Boyle, & Szatmari, 2007
). We note, however, that in an exploratory analysis where CBCL internalizing total scores were substituted for externalizing scores, there were no significant voxelwise correlations.
In conclusion, this experiment provides evidence that adolescents characterized by clinically-significant externalizing behavior symptomatology show an exaggerated response of mesolimbic incentive neurocircuitry to reward notifications. Future studies should explore incentive neurocircuitry in more severe cases, and whether deviant mesolimbic incentive processing in early adolescence portends subsequent SUD.
- Children with externalizing symptoms have shown heightened behavioral sensitivity to reward delivery in several laboratory tasks
- This experiment demonstrates that the motivational neurocircuitry of adolescents with externalizing symptoms is hypersensitive to reward notifications
- At a relaxed threshold, externalizing subjects showed more ventral striatum (VS) activation by reward notifications, and more VS deactivation by notifications of failure to win reward
- Externalizing symptomatology did not correlate with cue-elicited, reward-anticipatory activation of the VS