Novel insights from the Yellow Light Game: Safe and risky decisions differentially impact adolescent outcome-related brain function.

Changes across the span of adolescence in the adolescent reward system are thought to increase the tendency to take risks. While developmental differences in decision and outcome-related reward processes have been studied extensively, existing paradigms have largely neglected to measure how different types of decisions modulate reward-related outcome processes. We modified an existing decision-making paradigm (the Stoplight Task; Chein et al., 2011) to create a flexible laboratory measure of decision-making and outcome processing, including the ability to assess modulatory effects of safe versus risky decisions on reward-related outcome processes: the Yellow Light Game (YLG). We administered the YLG in the MRI scanner to 81 adolescents, ages 11-17 years, recruited from the community. Results showed that nucleus accumbens activation was enhanced for (1) risky > safe decisions, (2) positive > negative outcomes, and (3) outcomes following safe decisions compared to outcomes following risky decisions, regardless of whether these outcomes were positive or negative. Outcomes following risky decisions (compared to outcomes following safe decisions) were associated with enhanced activity in cortical midline structures. Furthermore, while there were no developmental differences in risk-taking behavior, more pubertally mature adolescents showed enhanced nucleus accumbens activation during positive > negative outcomes. These findings suggest that outcome processing is modulated by the types of decisions made by adolescents and highlight the importance of investigating processes involved in safe as well as risky decisions to better understand the adolescent tendency to take risks.

Win for your kin: Neural responses to personal and vicarious rewards when mothers win for their adolescent children.

Mother-child relationships change considerably in adolescence, but it is not yet understood how mothers experience vicarious rewards for their adolescent children. In the current study, we investigated neural responses of twenty mothers winning and losing money for their best friend and for their adolescent child in a gambling task. During the task, functional neuroimaging data were acquired. We examined the activation patterns when playing for or winning for self, adolescent children and friends in four a-priori selected ROIs (nucleus accumbens, dorsomedial prefrontal cortex, precuneus and temporo-parietal junction). Behaviorally, mothers indicated that they experienced most enjoyment when they gained money for their children and that their children deserved to win more, relative to friends and self. At the neural level, nucleus accumbens activity was stronger when winning versus losing. This pattern was not only found when playing for self, but also for friends and children, possibly reflecting the rewarding value of vicarious prosocial gains. In addition, dorsomedial prefrontal cortex, precuneus, and temporo-parietal junction were more active when receiving outcomes for children and friends compared to self, possibly reflecting increased recruitment of mentalizing processes. Interestingly, activity in this network was stronger for mothers who indicated that their children and friends deserved to win more. These findings provide initial evidence that vicarious rewards for one's children are processed similarly as rewards for self, and that activation in social brain regions are related to social closeness.

The effect of social rank feedback on risk taking and associated reward processes in adolescent girls.

The onset of adolescence is associated with an increased tendency to engage in risky behaviors and a developmental shift toward peers that contributes to increased prioritization for learning about and achieving social status. There is relatively little understanding about the specific links between these adolescent-typical phenomena, particularly regarding their neural underpinnings. Based on existing models that suggest the role of puberty in promoting adolescent status-seeking and risk-taking tendencies, we investigated the relation of pubertal hormones with behavioral and neural responses to status-relevant social information in the context of risk taking. We used a probabilistic decision task in which 11- to 13-year-old girls chose to take a risk, or not, while receiving either social rank or monetary performance feedback. While feedback type did not differentially influence risk-taking behavior, whole-brain imaging results showed that activation in the anterior insula was increased for risk taking in the social rank feedback condition compared to the monetary feedback condition. This heightened activation was more pronounced in girls with higher estradiol levels. These findings suggest that brain processes involved in adolescent risky decisions may be influenced by the desire for social-status enhancement and provide preliminary evidence for the role of pubertal hormones in enhancing this adolescent-typical social sensitivity.

Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry.

Adolescence is a developmental period characterized by a greater tendency to take risks. While the adult literature has shown that sex steroids influence reward-related brain functioning and risk taking, research on the role of these hormones during puberty is limited. In this study, we examined the relation between pubertal hormones and adolescent risk taking using a probabilistic decision-making task. In this task, participants could choose on each trial to play or pass based on explicit information about the risk level and stakes involved in their decision. We administered this task to 58 11-to-13-year-old girls while functional MRI images were obtained to examine reward-related brain processes associated with their risky choices. Results showed that higher testosterone levels were associated with increased risk taking, which was mediated by increased medial orbitofrontal cortex activation. Furthermore, higher estradiol levels were associated with increased nucleus accumbens activation, which in turn related to decreased risk taking. These findings offer potential neuroendocrine mechanisms that can explain why some adolescent girls might engage in more risk taking compared to others.

A cross-sectional and longitudinal analysis of reward-related brain activation: effects of age, pubertal stage, and reward sensitivity.

Neurobiological models suggest that adolescents are driven by an overactive ventral striatum (VS) response to rewards that may lead to an adolescent increase in risk-taking behavior. However, empirical studies showed mixed findings of adolescents' brain response to rewards. In this study, we aimed to elucidate the relationship between reward-related brain activation and risky decision-making. In addition, we examined effects of age, puberty, and individuals' reward sensitivity. We collected two datasets: Experiment 1 reports cross-sectional brain data from 75 participants (ages 10-25) who played a risky decision task. Experiment 2 presents a longitudinal extension in which a subset of these adolescents (n=33) was measured again 2years later. Results showed that (1) a reward-related network including VS and medial PFC was consistently activated over time, (2) the propensity to choose the risky option was related to increased reward-related activation in VS and medial PFC, and (3) longitudinal comparisons indicated that self-reported reward sensitivity was specifically related to VS activation over time. Together, these results advance our insights in the brain circuitry underlying reward processing across adolescence.

Social exclusion and punishment of excluders: neural correlates and developmental trajectories.

Social exclusion is a distressing experience and can result in a reduction of prosocial behavior. In this fMRI study we examined the neural networks involved in social exclusion and subsequent fairness considerations across adolescent development. Participants from 3 age groups (10-12, 14-16 and 19-21 year olds) participated in the study and performed two tasks; first, participants played Cyberball to induce feelings of social inclusion and exclusion, followed by a Dictator game in which participants were asked to divide coins between themselves and the players who previously included or excluded them. Results revealed a network of regions associated with social exclusion, which involve the medial prefrontal cortex (mPFC)/ventral anterior cingulate cortex (vACC), subgenual ACC and the lateral PFC, as well as the insula and the dorsal ACC. Although social exclusion generated strong distress for all age groups, 10-12 year olds showed increased activity in the subgenual ACC in the exclusion game, which has been associated in previous studies with negative affective processing. Results of the Dictator game revealed that all age groups selectively punished the excluders by making lower offers. These offers were associated with activation in the temporoparietal junction (TPJ), superior temporal sulcus (STS) and the lateral PFC. Age comparisons revealed that adults showed additional activity in the insula and dorsal ACC when making offers to the excluders. The results are discussed in the light of recent findings on neural networks involved in social exclusion and the development of social brain regions.

Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents.

Risk taking is an integral part of learning and development, particularly during adolescence the prevalence of risky behaviors peak. It is hypothesized that the tendency to take risks is related to pubertal maturation, where there is interplay between gonadal hormones, the neural mechanisms that underlie affective (e.g., reward) processing, and risky behavior. To test this hypothesis, fifty healthy adolescents (aged 10-16 years; 33 girls, 17 boys) at different stages of puberty performed a gambling task while lying in the MRI scanner, and provided saliva samples for hormone assessment. Gonadal hormone levels were correlated with the neural response to receiving a monetary reward. Results showed that testosterone level correlated positively with activation in the striatum for both boys and girls, suggesting that individual differences in hormones at puberty are related to the way adolescents respond to reward, which can ultimately affect risk-taking behavior.

Adolescent risky decision-making: neurocognitive development of reward and control regions.

Recent models hypothesize that adolescents' risky behavior is the consequence of increased sensitivity to rewards in the ventral medial (VM) prefrontal cortex (PFC) and the ventral striatum (VS), paired with immature cognitive control abilities due to slow maturation of the dorsal anterior cingulate cortex (ACC) and lateral PFC. We tested this hypothesis with fMRI using a gambling task in which participants chose between Low-Risk gambles with a high probability of obtaining a small reward (1 Euro) and High-Risk gambles with a smaller probability of obtaining a higher reward (2, 4, 6, or 8 Euro). We examined neural responses during choice selection and outcome processing in participants from 4 age groups (pre-pubertal children, early adolescents, older adolescents and young adults). High-Risk choices increased with rewards for all ages, but risk-taking decreased with age for low reward gambles. The fMRI results confirmed that High-Risk choices were associated with activation in VMPFC, whereas Low-Risk choices were associated with activation in lateral PFC. Activation in dorsal ACC showed a linear decrease with age, whereas activation in VMPFC and VS showed an inverted U-shaped developmental pattern, with a peak in adolescence. In addition, behavioral differences in risk-taking propensity modulated brain activation in all age groups. These findings support the hypothesis that risky behavior in adolescence is associated with an imbalance caused by different developmental trajectories of reward and regulatory brain circuitry.