Modulation of meso-limbic reward processing by motivational tendencies in young adolescents and adults

Abstract

Adolescence is a particularly vulnerable period for the onset of substance use disorders and other psychopathology. Individual variability in motivational tendencies and temperament and significant changes in functional brain organization during adolescence are important factors to consider in the development of substance use and dependence. Recent conceptualizations suggest that sensitivity to reward is heightened in adolescence and that this motivation tendency may precipitate subsequent substance abuse. The present study examined the role of personality traits in mesolimbic neurobehavioral response on a monetary incentive delay (MID) task in young adolescents (11-14 years) and emerging adults (18-25 years) using functional magnetic resonance imaging. As a group, adolescents were not more sensitive to gains than losses compared to adults during either anticipatory and feedback phases; instead, compared to adults they showed less sensitivity to incentive magnitude in mesolimbic circuitry during anticipation and feedback stages. However, personality modulated this response such that adolescents high in impulsivity or low in avoidance tendencies showed greater gain sensitivity and adolescents high in avoidance showed greater loss sensitivity during cue anticipation. In adults, mesolimbic response was modulated by the impulsivity construct such that high-impulsive adults showed reduced magnitude sensitivity during both anticipation and feedback compared to low impulsive adults. The present findings suggest that impulsive personality significantly modulates mesolimbic reward response during both adolescence and adulthood but avoidance and approach tendencies also modulate this response in adolescents. Moreover, personality modulated incentive valence in adolescents but incentive magnitude in adults. Collectively, these findings suggest that mesolimbic reward circuitry function is modulated by somewhat different parameters in adolescence than in adulthood.

Keywords: Brain development; FMRI; Monetary incentive delay; Reward.

Figure 1

(a) Monetary Incentive Delay task used in the present study. Participants could earn or lose money depending on speed of responding to a target stimulus (white rectangle). Each trial consisted of cue, target and feedback phases. The cue phase displayed a monetary value that could be won or lost. The target phase consisted of a simple stimulus presented briefly, and participants were instructed to respond within the duration of the target display (on the order of 250 ms). If the response time was less than the target duration a checkmark appeared on the feedback screen and the participant earned or avoided losing money. If the response time exceeded the target duration, an X appeared on the feedback screen and the participant did not win or incurred a loss of money. Across trials, the target display duration was adjusted to maintain trial accuracy at 67%. (b) The slope parameter indicates the slope of the linear component of a quadratic function fit to the fMRI signal in the different incentive conditions. A positive slope indicates greater fMRI response to positive incentive values and a negative slope indicates greater fMRI response to negative incentive values. (c) The curvature parameter indicates the degree of curvature of the quadratic function. A curvature value of 0 indicates no curvature; a positive curvature value indicates greater concavity and a negative curvature value indicates greater convexity. In other words, a more concave function would reflect greater fMRI signal for the extreme compared to small incentive values but a more convex function would reflect a greater fMRI signal for small values.

Figure 2

Behavioral results. (a) accuracy as a function of incentive value and age group. (b) Accuracy as a function of incentive value and sensation seeking group. (c) Speed of responding as a function of incentive value and age group. (d) Speed of responding as a function of incentive value and sensation seeking group. The trend line represents the curvature parameter based on the group mean (but note that the analyses calculated curvature and slope separately for each subject). HSS = high sensation seekers; LSS = low sensation seekers. Error bars are standard error of the mean.

Figure 3

fMRI incentive functions in the 8 regions-of-interest for the cue phase. Regions indicated with * had a significant effect of age on the curvature of the fMRI incentive function. The trend line represents the curvature parameter based on the group mean (but note that the analyses calculated curvature and slope separately for each subject).

Figure 4

fMRI incentive functions in the 8 regions-of-interest for the feedback phase. Regions indicated with * had a significant effect of age on the magnitude of the fMRI incentive function. The trend line represents the cruvature parameter based on the group mean (but note that the analyses calculated curvature and slope separately for each subject).

Figure 5

Modulation of fMRI incentive function magnitude parameter by impulsivity in adults. (a) regions modulated by impulsivity in the cue phase. (b) regions modulated by impulsivity in the feedback phase. Although the graphs depict the fMRI incentive functions by high (blue) and low (red) impulsivity groups, the primary analysis was a correlation between the curvature parameter of the incentive function (cue-magnitude variable or feedback-magnitude variable) and the impulsivity factor score. The correlation between the impulsivity personality dimension and the curvature parameter was significant in each of these regions. The trend line represents the curvature parameter based on the high or low group means (but note that the analyses calculated curvature and slope separately for each subject).

Figure 6

Modulation of fMRI incentive function valence parameter by (a) avoidance, (b) approach and (c) impulsivity personality constructs in adolescents. Although the graphs depict the fMRI incentive functions by high and low groups for each construct, the primary analysis was a correlation between the slope parameter of the incentive function (cue-valence variable) and the personality construct factor score. The trend line represents the slope parameter based on the high or low group means (but note that the analyses calculated curvature and slope separately for each subject).

Figure 7

Results of the voxel-wise analyses for the gain-sensitive, magnitude-sensitive and negative magnitude-sensitivity contrasts. Activation for adults is depicted in red-yellow; activation for adolescents is depicted in purple; activation for Adults > Adolescents is depicted in green. All activations are significant at p < .05, cluster corrected. (a) Cue phase gain sensitivity. (b) Cue phase magnitude sensitivity. (c) Feedback phase gain sensitivity. (d) Feedback phase magnitude sensitivity. (e) Feedback phase negative magnitude-sensitivity.