Adolescent neural response to reward is related to participant sex and task motivation

Abstract

Risky decision making is prominent during adolescence, perhaps contributed to by heightened sensation seeking and ongoing maturation of reward and dopamine systems in the brain, which are, in part, modulated by sex hormones. In this study, we examined sex differences in the neural substrates of reward sensitivity during a risky decision-making task and hypothesized that compared with girls, boys would show heightened brain activation in reward-relevant regions, particularly the nucleus accumbens, during reward receipt. Further, we hypothesized that testosterone and estradiol levels would mediate this sex difference. Moreover, we predicted boys would make more risky choices on the task. While boys showed increased nucleus accumbens blood oxygen level-dependent (BOLD) response relative to girls, sex hormones did not mediate this effect. As predicted, boys made a higher percentage of risky decisions during the task. Interestingly, boys also self-reported more motivation to perform well and earn money on the task, while girls self-reported higher state anxiety prior to the scan session. Motivation to earn money partially mediated the effect of sex on nucleus accumbens activity during reward. Previous research shows that increased motivation and salience of reinforcers is linked with more robust striatal BOLD response, therefore psychosocial factors, in addition to sex, may play an important role in reward sensitivity. Elucidating neurobiological mechanisms that support adolescent sex differences in risky decision making has important implications for understanding individual differences that lead to advantageous and adverse behaviors that affect health outcomes.

Keywords: Adolescence; Motivation; Reward; Risk taking; Sex differences; Sex hormones.

Fig. 1

Boys showed greater striatal BOLD response during reward processing. Statistical maps of sex differences in percent BOLD activation in Win – No Win contrast (controlling for age) overlaid on a standard Talairach template are depicted here. Boys showed more activation (orange) than girls (blue) in bilateral lentiform nucleus (extending to caudate nucleus, putamen, nucleus accumbens and thalamus). Percent BOLD signal change in these regions is also depicted by trial type (No Win and Win) and their contrast (Win – No Win). In all cases, boys showed higher percent BOLD signal change during Win trials, compared to girls. In contrast, there were no sex differences in No Win BOLD activation. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Boys showed greater cortical BOLD response during reward processing. Statistical maps of sex differences in percent BOLD activation in Win – No Win contrast (controlling for age) overlaid on a standard Talairach template are depicted here. Boys showed more activation (orange) than girls (blue) in paracentral gyrus (extending to cingulate cortex and precuneus), superior/inferior parietal lobule (extending to precuneus) and fusiform gyrus (extending to lingual gyrus). Percent BOLD signal change in these regions is also depicted by trial type (No Win and Win) and their contrast (Win – No Win). In all cases, boys showed higher percent BOLD signal change during Win trials, compared to girls. In contrast, there were no sex differences in No Win BOLD activation. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

Boys showed greater BOLD response in nucleus accumbens during reward processing. (A) Bilateral nucleus accumbens mask (peak coordinates: 12, −8, −8 and −12, −8, −8) overlaid on standard Talairach atlas. (B) Statistical map of sex differences in nucleus accumbens region of interest analysis overlaid on a standard Talairach template. Percent BOLD signal change in the Win – No Win contrast is displayed for one significant cluster in right nucleus accumbens (p < 0.05 voxel and α < 0.05 cluster correction) in which boys had significantly more activation than girls. (C) Mean ± SEM percent BOLD signal change in right nucleus accumbens is plotted by trial type.