Ashley R. Smith

Adolescents, Adults and Rewards: Comparing Motivational Neurocircuitry Recruitment Using fMRI

Background Adolescent risk-taking, including behaviors resulting in injury or death, has been attributed in part to maturational differences in mesolimbic incentive-motivational neurocircuitry, including ostensible oversensitivity of the nucleus accumbens (NAcc) to rewards. Methodology/Principal Findings To test whether adolescents showed increased NAcc activation by cues for rewards, or by delivery of rewards, we scanned 24 adolescents (age 12–17) and 24 adults age (22–42) with functional magnetic resonance imaging while they performed a monetary incentive delay (MID) task. The MID task was configured to temporally disentangle potential reward or potential loss anticipation-related brain signal from reward or loss notification-related signal. Subjects saw cues signaling opportunities to win or avoid losing

Striatal sensitivity to reward deliveries and omissions in substance dependent patients.

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The dual systems model: Review, reappraisal, and reaffirmation.

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Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking

5 for responding quickly to a subsequent target. Subjects then viewed feedback of their trial success after a variable interval from cue presentation of between 6 to17 s. Adolescents showed reduced NAcc recruitment by reward-predictive cues compared to adult controls in a linear contrast with non-incentive cues, and in a volume-of-interest analysis of signal change in the NAcc. In contrast, adolescents showed little difference in striatal and frontocortical responsiveness to reward deliveries compared to adults. Conclusions/Significance In light of divergent developmental difference findings between neuroimaging incentive paradigms (as well as at different stages within the same task), these data suggest that maturational differences in incentive-motivational neurocircuitry: 1) may be sensitive to nuances of incentive tasks or stimuli, such as behavioral or learning contingencies, and 2) may be specific to the component of the instrumental behavior (such as anticipation versus notification).

Developmental differences in posterior mesofrontal cortex recruitment by risky rewards.

Some motivational theories of substance dependence (SD) posit either pathologically increased or decreased ventral striatum (VS) recruitment by cues for nondrug rewards. The incentive-sensitization hypothesis, alternatively, attributes SD to enhanced incentive salience of drug-predictive cues specifically, with no requirement for altered nondrug incentive processing. We assessed whether individuals undergoing inpatient therapy for SD are characterized by altered recruitment of mesolimbic incentive neurocircuitry by cues and deliveries of nondrug rewards. During functional magnetic resonance imaging, substance-dependent patients (SDP) and controls performed a modified monetary incentive delay task featuring: a) anticipatory cues that signaled opportunities to respond to a target to either win money or avoid losing money, b) notifications of wins and losses, and c) unexpected replacement of reward trial outcomes with a demand to repeat the trial. Both anticipatory reward cues and loss cues elicited similar mood responses and VS activation between SDP and controls. However, in SDP (but not controls), reward notifications also activated VS and mesial frontal cortex, and loss notifications activated anterior insula. Finally, substitution of expected outcomes in reward trials with notifications to repeat the trial deactivated the VS in SDP but not in controls. These data do not suggest that SD is characterized by altered recruitment of VS circuitry by cues for nondrug incentives. Rather, SDP may instead have increased limbic system sensitivity to reward and loss delivery, consistent with the role of impulsivity in SD.

Incentive-elicited mesolimbic activation and externalizing symptomatology in adolescents.

Highlights • Evidence related to the dual systems model of adolescent risk taking is reviewed.• The review encompasses both the psychological and neuroimaging literatures.• Recent findings (since 2008) generally support the dual systems model.• Recommendations are made for future research directions.

Peers Increase Adolescent Risk Taking Even When the Probabilities of Negative Outcomes Are Known

While there is little doubt that risk-taking is generally more prevalent during adolescence than before or after, the underlying causes of this pattern of age differences have long been investigated and debated. One longstanding popular notion is the belief that risky and reckless behavior in adolescence is tied to the hormonal changes of puberty. However, the interactions between pubertal maturation and adolescent decision making remain largely understudied. In the current review, we discuss changes in decision making during adolescence, focusing on the asynchronous development of the affective, reward-focused processing system and the deliberative, reasoned processing system. As discussed, differential maturation in the structure and function of brain systems associated with these systems leaves adolescents particularly vulnerable to socio-emotional influences and risk-taking behaviors. We argue that this asynchrony may be partially linked to pubertal influences on development and specifically on the maturation of the affective, reward-focused processing system.

Age differences in the impact of peers on adolescents' and adults' neural response to reward

Might increased risk taking in adolescence result in part from underdeveloped conflict-monitoring circuitry in the posterior mesofrontal cortex (PMC)? Adults and adolescents underwent functional magnetic resonance imaging during a monetary game of “chicken.” As subjects watched ostensible winnings increase over time, they decided when to press a button to bank their winnings, knowing that if they did not stop pursuing money reward before a secret varying time limit, they would “bust” and either lose the money accrued on the current trial (low-penalty trials) or forfeit trial winnings plus a portion of previous winnings (high-penalty trials). Reward accrual at risk of low penalty (contrasted with guaranteed reward) activated the PMC in adults but not in adolescents. Across all subjects, this activation (1) correlated positively with age but negatively with risk exposure and (2) was greater when subjects busted on the previous low-penalty trial. Reward accrual at risk of high penalty was terminated sooner and recruited the PMC in both adults and adolescents when contrasted with guaranteed reward. Predecision PMC activation in the high-penalty trials was significantly reduced in trials when subjects busted. These data suggest that (1) under threat of an explicit severe penalty, recruitment of the PMC is similar in adolescents and adults and correlates with error avoidance, and (2) when potential penalties for a rewarding behavior are mild enough to encourage some risk taking, predecision PMC activation by a reward/risk conflict is sensitive to previous error outcomes, predictive of risk-aversive behavior in that trial, and underactive in adolescents.

The role of the anterior insula in adolescent decision making.

BACKGROUND Opponent-process theories of externalizing disorders (ExD) attribute them to some combination of overactive reward processing systems and/or underactive behavior inhibition systems. Reward processing has been indexed by recruitment of incentive-motivational neurocircuitry of the ventral striatum (VS), including nucleus accumbens (NAcc). METHODS We used functional magnetic resonance imaging (fMRI) with an incentive task to determine whether externalizing symptomatology in adolescence is correlated with an enhanced VS recruitment by cues for rewards, or by deliveries of rewards. Twelve community-recruited adolescents with externalizing disorders (AED) and 12 age/gender-matched controls responded to targets to win or avoid losing

Mesolimbic recruitment by nondrug rewards in detoxified alcoholics: Effort anticipation, reward anticipation, and reward delivery †

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