Neural correlates of reward processing in adolescents with a history of inhibited temperament

Abstract

Functional imaging data were acquired during performance of a reward-contingency task in a unique cohort of adolescents (ages 14-18 years) who were characterized since infancy on measures of temperamental behavioral inhibition. Neural activation was examined in striatal structures (nucleus accumbens, putamen, caudate) with a known role in facilitating response to salient reward-related cues. Adolescents with a history of behavioral inhibition, relative to noninhibited adolescents, showed increased activation in the nucleus accumbens when they believed their selection of an action would affect reward outcome. Neural responses did not differ between the two groups when participants made a prespecified response that they knew would result in reward or when they produced random motor responses that they knew would not be rewarded. These results link inhibited temperament and perturbed neural responses to reward-contingency cues.

Fig. 1

Experimental design and task performance. In the reward-contingency task (a), a series of neutral stimuli (purple squares, displayed for 1,000 ms each) was interrupted randomly with infrequent experimental cues (large or small colored circles, displayed for 1,500 ms each). On noncontingent trials, the number “1” or the number “2” was presented in the center of the cue (shown here in orange), and subjects were instructed to press the button (“1” or “2”) that corresponded to the number in the circle. A correct response resulted in a small or large reward (denoted by the circle's size). On contingent trials, a question mark was presented in the center of the cue (shown here in blue), and subjects were instructed to press either button (“1” or “2”). They were led to believe that if their selected response was correct, they would receive a small or large reward (denoted by the circle's size), but in actuality, the reward was predetermined to be awarded on half the trials. On simple motor trials, the cue was always a small colored circle (shown here in yellow), and subjects were instructed to press either button (“1” or “2”). It was made explicit that no reward would be delivered on these trials. Assignment of cue colors to conditions was random across subjects. Feedback (FB; gain or no gain) and cumulative gain were provided (green box) at a variable interval following noncontingent and contingent trials. The graphs show mean response time (with standard errors of the mean) as a function of condition (b) and size of the reward (c).

Fig. 2

Results from the region-of-interest analysis of activation in the nucleus accumbens. The graph in (a) shows the average percentage of blood-oxygenation-level-dependent (BOLD) signal change (with standard errors of the mean) in 253 voxels of the nucleus accumbens cluster that surpassed the threshold of p < .05 in the analysis of the Condition (contingent vs. noncontingent) × Group (inhibited vs. noninhibited) interaction. Percentage signal change is shown in separate bars for the inhibited and noninhibited groups. The inset depicts a coronal slice at y = 8 mm, showing in yellow the location of this cluster (maxima of the Talairach coordinates: x = –7, y = 8, z = –9). The graph in (b) presents the mean percentage signal change (with standard errors of the mean) in the three experimental conditions relative to the baseline (neutral) condition, separately for the two groups.

Fig. 3

Results from the whole-brain analyses. The illustration at the top depicts a sagittal slice showing, in blue, areas of significant activation in the precuneus, left thalamus, and left posterior cingulate, as revealed in the analysis of the Condition (contingent vs. noncontingent) × Group (inhibited vs. noninhibited) interaction. For each region, the graph on the left shows the average percentage of blood-oxygenation-level-dependent (BOLD) signal change in voxels that surpassed a threshold of p < .05 in the interaction analysis, and the graph on the right presents the percentage signal change in each experimental condition relative to the baseline (neutral) condition; results are shown separately for the two groups. Error bars represent standard errors of the mean.