Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms

Forbes, Erika E.; Ryan, Neal D.; Phillips, Mary L.; Manuck, Stephen B.; Worthman, Carol M.; Moyles, Donna L.; Tarr, Jill A.; Sciarrillo, Samantha R.; Dahl, Ronald E.

doi:10.1016/j.jaac.2009.11.006

Cited by 188 publications

(175 citation statements)

References 45 publications

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“…fMRI reward studies that find less activation in VS in adolescents versus adults in anticipation of reward (35,36), or no age-related differences in response to reward receipt compared with children (37) or adults (27,36), may have used computer tasks that are not developmentally appropriate. For instance, the monetary incentive delay (MID) task (37) used by Bjork et al (35,36) and the card-guessing game (38) used by Forbes et al (39,40) were designed for adults without modification for use with younger populations. As noted by the authors, the MID task requires "unusual vigilance and anticipatory motor preparation-especially for high-incentive targets.…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, the MID task requires the participant to hold multiple conditions and rules in working memory to perform optimally, which may lead to less interest on the task (41). In the card-guessing game study by Forbes et al (39,40), task performance had no effect on participant payment, which may have diminished motivation. These issues may have contributed to the blunted/or null activation in their adolescent samples compared with adults.…”

Section: Discussionmentioning

confidence: 99%

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Neural representation of expected value in the adolescent brain

Barkley-Levenson

Galván

2014

Proc. Natl. Acad. Sci. U.S.A.

105

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Previous work shows that the adolescent reward system is hyperactive, but this finding may be confounded by differences in how teens value money. To address this, we examined the neural ontogeny of objective value representation. Adolescent and adult participants performed a monetary gambling task in which they chose to accept or reject gambles of varying expected value. Increasing expected value had a stronger influence over gambling choices in adolescents relative to adults, an effect that was paralleled by greater activation in the ventral striatum in adolescents. This unique adolescent ventral striatum response remained even after matching groups on acceptance behavior. These behavioral and neural data suggest that the value of available options has a greater influence in adolescent versus adult choices, even when objective value and subjective choice are held constant. This research provides further evidence that hyperactivation of reward circuitry in adolescence may be a normative ontogenetic shift that is due to greater valuation in the adolescent brain.A dolescence is characterized by heightened sensitivity to rewards (1). This phenotype is subserved by exaggerated neural response in ventral striatum (VS) to the anticipation (2) and receipt of expected (3-5) and unexpected reward (6) in adolescents versus other age groups. The question remains, however, whether this effect is mediated by ontogenetic differences or simply a methodological consequence of using money as the rewarding stimulus. In other words, does the adolescent brain attribute greater value to available rewards, or is the effect driven by adolescents valuing money to a greater extent than adults because they typically have less access to and experience with it? The goal of this study was to disentangle these possibilities by examining subjective valuation (indexed by behavior) of objectively valued choices.Subjective value (SV) is defined as the value that an individual places on a stimulus (7). To make a choice, an organism determines the SV of each alternative and then selects the one with the greatest SV (8, 9). A recent metaanalysis of 206 studies of SV in adults identified the ventromedial prefrontal cortex (VMPFC) and VS as a "valuation system" (8). These regions represent SV during choice for monetary stimuli (10-14), charitable donations (15), consumer goods (16), and food (17)(18)(19). Despite the wealth of knowledge on the neural correlates of SV in adults, no previous studies have examined the neurobiological development of SV, which precludes ruling out the possibility that previous findings in support of a hyperactive adolescent reward system were confounded by differences in participant valuation.One approach to understanding the neural computation of SV is through measurement of expected value (EV), the sum of all of the possible outcomes of a particular choice multiplied by their probabilities (20). In adults, increasing EV yields parametric activation increases in bilateral VS, midbrain, medial prefrontal cortex (MPFC), an...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Neural representation of expected value in the adolescent brain

Barkley-Levenson

Galván

2014

Proc. Natl. Acad. Sci. U.S.A.

105

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“…This age marks a pubertal stage when sexual maturation is completing in both sexes, but behavioral, emotional, and cerebral development can still widely differ among individuals (Giedd et al, 1999;Crone et al, 2008;Monahan and Steinberg, 2011). Accordingly, we quantify pubertal development with an endogenous physiological marker, salivary testosterone, that is sensitive to those interindividual differences (Giedd et al, 2006;Forbes and Dahl, 2010;Berenbaum and Beltz, 2011) and is mechanistically involved in mediating neural development (Sisk and Zehr, 2005;Nguyen et al, 2013b;Herting et al, 2014). We expect that relatively less mature 14-year-old adolescents control their emotional action tendencies by relying on a pulvino-amygdalar system.…”

Section: Introductionmentioning

confidence: 99%

Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex

et al. 2016

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Increased limbic and striatal activation in adolescence has been attributed to a relative delay in the maturation of prefrontal areas, resulting in the increase of impulsive reward-seeking behaviors that are often observed during puberty. However, it remains unclear whether and how this general developmental pattern applies to the control of social emotional actions, a fundamental adult skill refined during adolescence. This domain of control pertains to decisions involving emotional responses. When faced with a social emotional challenge (e.g., an angry face), we can follow automatic response tendencies and avoid the challenge or exert control over those tendencies by selecting an alternative action. Using an fMRI-adapted social approach-avoidance task, this study identifies how the neural regulation of emotional action control changes as a function of human pubertal development in 14-year-old adolescents (n ϭ 47). Pubertal maturation, indexed by testosterone levels, shifted neural regulation of emotional actions from the pulvinar nucleus of the thalamus and the amygdala to the anterior prefrontal cortex (aPFC). Adolescents with more advanced pubertal maturation showed greater aPFC activity when controlling their emotional action tendencies, reproducing the same pattern consistently observed in adults. In contrast, adolescents of the same age, but with less advanced pubertal maturation, showed greater pulvinar and amygdala activity when exerting similarly effective emotional control. These findings qualify how, in the domain of social emotional actions, executive control shifts from subcortical to prefrontal structures during pubertal development. The pulvinar and the amygdala are suggested as the ontogenetic precursors of the mature control system centered on the anterior prefrontal cortex.

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“…That is, gonadal hormone levels significantly increase during adolescence and have both organizational and activating effects on brain functioning (Blakemore, Burnett, & Dahl, 2010;Sisk & Zehr, 2005). For instance, higher testosterone levels have been associated with increased VS activation (Forbes et al, 2010;Op de Macks et al, 2011) and to adolescent typical risk-behavior such as experimentation with alcohol (De Water, Braams, Crone, & Peper, 2013).…”

Section: Introductionmentioning

confidence: 99%

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

Duijvenvoorde

Macks

Overgaauw

et al. 2014

Brain and Cognition

Self Cite

104

102

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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 2 years 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.

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Healthy Adolescents' Neural Response to Reward: Associations With Puberty, Positive Affect, and Depressive Symptoms

Cited by 188 publications

References 45 publications

Neural representation of expected value in the adolescent brain

Neural representation of expected value in the adolescent brain

Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex

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

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