Enhanced Striatal Sensitivity to Aversive Reinforcement in Adolescents versus Adults

Galván, Adriana; McGlennen, Kristine M.

doi:10.1162/jocn_a_00326

Cited by 97 publications

(81 citation statements)

References 97 publications

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“…S3). This is consistent with heightened adolescent behavioral sensitivity to aversive stimuli (30) and similar or heightened measurements of adolescent risk perception relative to adults (31), which challenges the anecdotal lore that adolescents think they are invulnerable to negative outcomes. More research on this important question is necessary.…”

Section: Discussionsupporting

confidence: 63%

Neural representation of expected value in the adolescent brain

Barkley-Levenson

Galván

2014

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

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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: Discussionsupporting

confidence: 63%

Neural representation of expected value in the adolescent brain

Barkley-Levenson

Galván

2014

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

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105

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“…A recent study by Galvan and McGlennen using aversive liquids found a similar age difference within the anterior insula where adolescents’ responses to loss were reduced compared to adults’ (Galvan & McGlennen 2013). While Galvan and McGlennen interpreted this result to indicate that aversive outcomes are more affectively salient for adults than adolescents , we interpret our results as indicating a difference in general salience of cue/feedback between adults and children , as we observed similar age differences (i.e., reduced child responses) within this region following both gain and loss, as discussed in more detail below.…”

Section: Discussionmentioning

confidence: 84%

“…Firstly, the complex nature of these tasks may make them particularly sensitive to age differences in cognitive components of feedback processing, but less sensitive to age differences in emotional/hedonic components of feedback processing. Secondly, developmental incentive studies have primarily utilized secondary rewards, such as money or token economies, (see (Galvan & McGlennen 2013) for liquid incentives in adolescents and adults). While such rewards have many advantages, they may bias findings particularly with younger school-age/preschool children.…”

Section: Introductionmentioning

confidence: 99%

Kids, candy, brain and behavior: Age differences in responses to candy gains and losses

Luking

Luby

Deanna

2014

Developmental Cognitive Neuroscience

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The development of reward-related neural systems, from adolescence through adulthood, has received much recent attention in the developmental neuroimaging literature. However, few studies have investigated behavioral and neural responses to both gains and losses in pre-pubertal child populations. To address this gap in the literature, in the present study healthy children aged 7–11 years and young-adults completed an fMRI card-guessing game using candy pieces delivered post-scan as an incentive. Age differences in behavioral and neural responses to candy gains/losses were investigated. Adults and children displayed similar responses to gains, but robust age differences were observed following candy losses within the caudate, thalamus, insula, and hippocampus. Interestingly, when task behavior was included as a factor in post-hoc mediation analyses, activation following loss within the caudate/thalamus related to task behavior and relationships with age were no longer significant. Conversely, relationships between response to loss and age within the hippocampus and insula remained significant even when controlling for behavior, with children showing heightened loss responses within the dorsal/posterior insula. These results suggest that both age and task behavior influence responses within the extended reward circuitry, and that children seem to be more sensitive than adults to loss feedback particularly within the dorsal/posterior insula.

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“…Importantly, "liking" can be measured objectively through neural responses, whether or not the individual is consciously aware of their feelings of pleasure (1). For example, human and rodent research has shown that adolescents, more so than children or adults, show heightened activation in the ventral striatum following the receipt of hedonic rewards, including money, sucrose, and immediate rather than long-term rewards (7,15,19,20). Moreover, during risk taking, adolescents show higher activation in the ventral striatum than younger or older individuals (21).…”

Section: Significancementioning

confidence: 99%

Neural sensitivity to eudaimonic and hedonic rewards differentially predict adolescent depressive symptoms over time

Telzer

Fuligni²,

Lieberman³

et al. 2014

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

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129

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The pursuit of happiness and reward is an impetus for everyday human behavior and the basis of well-being. Although optimal well-being may be achieved through eudaimonic activities (e.g., meaning and purpose), individuals tend to orient toward hedonic activities (e.g., pleasure seeking), potentially placing them at risk for ill-being. We implemented a longitudinal study and followed adolescents over 1 y to examine whether neural sensitivity to eudaimonic (e.g., prosocial decisions) and hedonic (e.g., selfish rewards and risky decisions) rewards differentially predicts longitudinal changes in depressive symptoms. Ventral striatum activation during eudaimonic decisions predicted longitudinal declines in depressive symptoms, whereas ventral striatum activation to hedonic decisions related to longitudinal increases in depressive symptoms. These findings underscore how the motivational context underlying neural sensitivity to rewards can differentially predict changes in well-being over time. Importantly, to our knowledge, this is the first study to show that striatal activation within an individual can be both a source of risk and protection.adolescence | fMRI | depression T he pursuit of happiness and reward is an impetus for everyday human behavior and the basis of well-being (1). In the fourth century B.C., Aristotle distinguished between two aspects of well-being: hedonia (pleasure, desire) and eudaimonia (meaning and purpose, a life well-lived). Aristotle argued that optimal well-being is achieved through eudaimonia, whereas pleasure and desire can be harmful to human growth (2). Contemporary psychological research has continued to distinguish between eudaimonic well-being and hedonic well-being, (e.g., refs. 3 and 4), with empirical studies demonstrating the long-term benefits of eudaimonic pursuits and the sometimes detrimental effects of hedonic pursuits (e.g., ref. 5). Whereas the distinction between hedonic and eudaimonic rewards has received theoretical and empirical attention in adult work, we know little about how these two types of rewards are experienced during adolescence, a developmental period during which rewards take on particular salience and vulnerability for ill-being dramatically rises (6).Neural systems involved in the generation of reward processing undergo significant changes during adolescence, resulting in a greater orientation toward rewards (6). Adolescents, more so than children or adults, show heightened activation in brain regions involved in reward processing when receiving rewards (7). Although some types of reward-seeking behaviors may be adaptive during this developmental period (e.g., engaging in meaningful social relationships), other types of reward-seeking behaviors may be detrimental (e.g., engaging in health-compromising risk taking). Therefore, the ways in which adolescents respond to different rewards may have significant implications for their well-being. In the current study, we examined how neural sensitivity to hedonic and eudaimonic rewards differentially predicts c...

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Enhanced Striatal Sensitivity to Aversive Reinforcement in Adolescents versus Adults

Cited by 97 publications

References 97 publications

Neural representation of expected value in the adolescent brain

Neural representation of expected value in the adolescent brain

Kids, candy, brain and behavior: Age differences in responses to candy gains and losses

Neural sensitivity to eudaimonic and hedonic rewards differentially predict adolescent depressive symptoms over time

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