In this study, adolescents characterized by an enduring pattern of behavioral inhibition (documented at three time points from infancy up to age 4 years) demonstrated enhanced sensitivity of the reward-related neural system, relative to adolescents not classified as behaviorally inhibited. This sensitivity was specific to the experimental condition in which participants believed that their choice of an action determined reward acquisition. Between-group differences in neural activation did not occur in the case of systematically rewarded stimuli or simple motor responses. Taken together, these findings suggest that active agency is needed to bring to light temperament-related individual differences in striatal response. Indeed, as hypothesized, enhanced sensitivity in the inhibited group was manifest as greater nucleus accumbens activation. This group difference emerged even though behavioral performance, as indexed by RT, was comparable in the two groups.
Note that responses to the follow-up debriefing questionnaire (“Describe what each of the three different circles means”) indicated that, as intended, the participants perceived reward on the contingent trials as being affected by their choice of response. Furthermore, responses to questions assessing how subjects experienced the task did not differ between groups. These data suggest that between-group differences in subjective-emotional responses or in reward expectancy, elicited by contingent-reward cues, may not completely explain the observed between-group differences in striatal responding. However, it should be noted that our postscan measures of reward expectancy were unlikely to comprehensively capture psychological processes that occurred immediately upon presentation of the contingent-reward cues. The experimental design allowed us to probe a limited set of behaviors during the task, and future studies should examine between-group differences in the relations between reward expectancy and striatal responding, perhaps by employing alternative designs that probe more comprehensively levels of reward expectancy engaged by presentation of contingent-reward cues.
Regardless of this limitation, the behavioral data showed that the task did engage relevant psychological processes across participants. For example, the differences in RTs to the noncontingent, contingent, and motor cues, in both groups considered together, indicate that these cues were perceived and processed differently, providing further support to the efficacy of the experimental manipulation. Particularly noteworthy is the finding that RTs were longer for contingent cues than for noncontingent cues, which suggests that extra time was needed to execute a selection in the contingent condition.
When combined with prior findings, these new results provide an important framework for understanding the neural correlates of temperamental behavioral inhibition. Although theory and research on behavioral inhibition have typically focused on threat processing and the amygdala (Monk et al., 2006
; Pine, 2007
; Schwartz et al., 2003
), the present study indicates that behaviorally inhibited individuals may also show perturbations in response to positive stimuli and in reward-related neural circuitry. In particular, the nucleus accumbens subserves numerous adaptive and goal-directed behaviors, such as feeding, drinking, sex, and exploration (Kelley, 1999
; Meredith & Totterdell, 1999
). The present findings suggest that inhibited temperament is related to increased brain activation when active agency is at play in the context of reward processing. This is not surprising considering that inhibited temperament is typically most apparent when active participation is required (Coplan, Rubin, Fox, Calkins, & Stewart, 1994
Finally, hypersensitivity to contingency-related reward delivery is only one parsimonious, theoretically plausible explanation for these findings. Our findings could also be conceptualized as reflecting exaggerated concerns about performance in the inhibited group, relative to the noninhibited group. A comprehensive evaluation of these alternatives would require more in-depth investigation of relations among perceived action-reward contingency and performance-related concerns in behaviorally inhibited subjects. In this regard, it is noteworthy that levels of anxiety and depression, and psychiatric status, did not differ between the groups in our study.
The exploratory whole-brain analyses revealed between-group differences in activation in additional regions (precuneus, left thalamus, and left posterior cingulate). The activation patterns in these regions, however, were opposite to those for the nucleus accumbens, and possibly reflected additional and complementary processing required by the experimental conditions in our task. Additional work on the functional relatedness of these brain regions to reward processing is needed in order to clarify the full meaning of these preliminary findings.
In conclusion, the present findings extend understanding of behavioral inhibition by more precisely characterizing the neurocognitive processes associated with alterations in responses to reward. Our previous work demonstrated that behavioral inhibition is associated with perturbations in the appetitive-motivational system (Guyer et al., 2006
; Hardin et al., 2006
). In this study, we found that these perturbations were specific to the condition in which participants believed that choice of self-executed responses determined outcomes, and did not extend to the condition in which outcomes were independent of subjects’ agency. Indeed, a sense of “responsibility,” or self-agency, in a context of uncertainty (probabilistic outcomes) drives the neural system underlying appetitive motivation (i.e., nucleus accumbens) more strongly in temperamentally inhibited than noninhibited adolescents. One important next step will be to determine how the reward system interacts with fear circuitry among subjects characterized by behavioral inhibition and elevated anxiety (Frenkel, Lamy, Algom, & Bar-Haim, 2008
). A further goal will be to examine behavioral inhibition and its underlying neural circuitry across development. Finally, a better understanding of factors that contribute to individual differences in reward-related processes may eventually generate insights relevant for therapeutic interventions in anxiety, a diathesis closely related to shyness and behavioral inhibition.