Incentive-elicited mesolimbic activation and externalizing symptomatology in adolescents

Division of Clinical Neuroscience and Behavioral Research, National Institute on Drug Abuse, National Institutes of Health (NIH), Bethesda, MD 20892, USA.
Journal of Child Psychology and Psychiatry (Impact Factor: 6.46). 12/2009; 51(7):827-37. DOI: 10.1111/j.1469-7610.2009.02201.x
Source: PubMed


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).
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 $0, $0.20, $1, $5, or an unknown amount (ranging from $0.20 to $5).
Cues to respond for rewards activated the NAcc (relative to cues for no incentive), in both subject groups similarly, with greatest NAcc recruitment by cues for the largest reward. Loss-anticipatory NAcc signal increase was detected in a volume-of-interest analysis - but this increase occurred only in trials when subjects hit the target. Relative to controls, AED showed significantly elevated NAcc activation by a linear contrast between reward notification versus notification of failure to win reward. In a post hoc reanalysis, VS and pregenual anterior cingulate activation by the reward versus non-reward outcome contrast also directly correlated with Child Behavior Checklist (CBCL) Externalizing total scores (across all subjects) in lieu of a binary diagnosis. Finally, both groups showed right insula activation by loss notifications (contrasted with avoided losses).
Externalizing behavior, whether assessed dimensionally with a questionnaire, or in the form of a diagnostic categorization, is associated with an exaggerated limbic response to outcomes of reward-directed behavior. This could be a neurobiological signature of the behavioral sensitivity to laboratory reward delivery that is characteristic of children with externalizing symptomatology. Of interest is future research on incentive-motivational processing in more severe, clinically referred AED.

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Available from: Daniel W Hommer, Oct 05, 2015
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    • "The heightened ventral striatum reactivity was complemented by ADHD-specific medial prefrontal overactivation under social reward conditions. In ADHD, stronger medial prefrontal activation, including anterior cingulate and orbitofrontal cortex, in response to reward (i.e., money) has been quite consistently reported before (Bjork et al., 2010; Gatzke-Kopp et al., 2009; Ströhle et al., 2008; Wilbertz et al., 2012) and has been shown to be normalized through MPH administration (Rubia et al., 2009a). Our finding of medial prefrontal overreactivity in response to social reward can be seen in line with Wilbertz and colleagues who reported stronger orbitofrontal activity for non-monetary reward (i.e., checkmark for accurate task performance) in adults with ADHD (Wilbertz et al., 2012). "
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    ABSTRACT: Although attention deficit hyperactivity disorders (ADHD) and autism spectrum disorders (ASD) share certain neurocognitive characteristics, it has been hypothesized to differentiate the two disorders based on their brain’s reward responsiveness to either social or monetary reward. Thus, the present fMRI study investigated neural activation in response to both reward types in age and IQ-matched boys with ADHD versus ASD relative to typically controls (TDC). A significant group by reward type interaction effect emerged in the ventral striatum with greater activation to monetary versus social reward only in TDC, whereas subjects with ADHD responded equally strong to both reward types, and subjects with ASD showed low striatal reactivity across both reward conditions. Moreover, disorder-specific neural abnormalities were revealed, including medial prefrontal hyperactivation in response to social reward in ADHD versus ventral striatal hypoactivation in response to monetary reward in ASD. Shared dysfunction was characterized by fronto-striato-parietal hypoactivation in both clinical groups when money was at stake. Interestingly, lower neural activation within parietal circuitry was associated with higher autistic traits across the entire study sample. In sum, the present findings concur with the assumption that both ASD and ADHD display distinct and shared neural dysfunction in response to reward.
    Developmental Cognitive Neuroscience 08/2014; DOI:10.1016/j.dcn.2014.08.003 · 3.83 Impact Factor
    • "lescent social phobia ( Guyer , 2012 ) . However , we sought to under - stand individual differences in decision - making and reward processing in typically developing adolescents . Several studies investigating these differences have demonstrated that adolescents reporting more risky behavior ( Galvan et al . , 2007 ) or externalizing behaviors ( Bjork , Chen , et al . , 2010 ) in everyday life showed more anticipatory reward - related activity during the monetary incentive delay task . In the decision - making realm , several studies have demonstrated less risk - related dACC activity for those taking more risks ( Van Leijenhorst , Gunther Moor , et al . , 2010 ; Eshel et al . , 2007 ) . In our study , we l"
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    ABSTRACT: Adolescent decision-making is a topic of great public and scientific interest. However, much of the neuroimaging research in this area contrasts only one facet of decision-making (e.g., neural responses to anticipation or receipt of monetary rewards). Few studies have directly examined the processes that occur immediately before making a decision between two options that have varied and unpredictable potential rewards and penalties. Understanding adolescent decision-making from this vantage point may prove critical to ameliorating risky behavior and improving developmental outcomes. In this study, participants aged 14-16 engaged in a driving simulation game while undergoing fMRI. Results indicated activity in ventral striatum preceded risky decisions and activity in right inferior frontal gyrus (rIFG) preceded safe decisions. Furthermore, participants who reported higher sensation-seeking and sensitivity to reward and punishment demonstrated lower rIFG activity during safe decisions. Finally, over successive games, rIFG activity preceding risky decisions decreased, whereas thalamus and caudate activity increased during positive feedback (taking a risk without crashing). These results indicate that regions traditionally associated with reward processing and inhibition not only drive risky decision-making in the moment but also contribute to learning about risk tradeoffs during adolescence.
    Journal of Cognitive Neuroscience 08/2014; 27(1):1-13. DOI:10.1162/jocn_a_00694 · 4.09 Impact Factor
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    • "In humans, VS FDOPA K i values have been found to positively correlate with BOLD-fMRI activity to reward cues in limbic brain regions linked to incentive salience attribution (Siessmeier et al., 2006), and limbic BOLD-fMRI responses to reward cues are correlated with both disinhibitory personality traits (Beaver et al., 2006; Buckholtz et al., 2010) and externalizing symptomatology (Bjork et al., 2010). One possibility is that individuals high on externalizing risk show exaggerated phasic DA release to reward cues, resulting from a larger releasable pool of DA generated by increased DA synthesis capacity (Bello et al., 2011; Anzalone et al., 2012), triggering excessive attribution of incentive salience to environmental cues and their associated rewards, leading to behavioral disinhibition (Flagel et al., 2010; Lovic et al., 2011) (but see Huys et al., 2014 for an alternative proposal). "
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    Frontiers in Behavioral Neuroscience 03/2014; 8:86. DOI:10.3389/fnbeh.2014.00086 · 3.27 Impact Factor
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