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Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence.

ABSTRACT: Figure 2 was distorted in production. The correct version is presented in the erratum.] Adolescence is a period of radical normative changes and increased risk for substance use, mood disorders, and physical injury. Researchers have proposed that increases in reward sensitivity (i.e., sensitivity of the behavioral approach system [BAS]) and/or increases in reactivity to all emotional stimuli (i.e., reward and threat sensitivities) lead to these phenomena. The present study is the first longitudinal investigation of changes in reward (i.e., BAS) sensitivity in 9- to 23-year-olds across a 2-year follow-up. Support was found for increased reward sensitivity from early to late adolescence, and evidence was found for decline in the early 20s. This decline is combined with a decrease in left nucleus accumbens (Nacc) volume, a key structure for reward processing, from the late teens into the early 20s. Furthermore, we found longitudinal increases in sensitivity to reward to be predicted by individual differences in the Nacc and medial orbitofrontal cortex (OFC) volumes at baseline in this developmental sample. Similarly, increases in sensitivity to threat (i.e., behavioral inhibition system sensitivity) were qualified by sex, with only females participants experiencing this increase, and predicted by individual differences in lateral OFC volumes at baseline.

SUBMITTER: Urosevic S

PROVIDER: S-EPMC3370133 | biostudies-literature | 2012 Sep

REPOSITORIES: biostudies-literature

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Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence.

Urošević Snežana S Collins Paul P Muetzel Ryan R Lim Kelvin K Luciana Monica M

Developmental psychology 20120305 5

Figure 2 was distorted in production. The correct version is presented in the erratum.] Adolescence is a period of radical normative changes and increased risk for substance use, mood disorders, and physical injury. Researchers have proposed that increases in reward sensitivity (i.e., sensitivity of the behavioral approach system [BAS]) and/or increases in reactivity to all emotional stimuli (i.e., reward and threat sensitivities) lead to these phenomena. The present study is the first longitudi ...[more]

PMID: 22390662

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Project description:A food's reward value is dependent on its caloric content. Furthermore, a food's acute reward value also depends on hunger state. The drive to obtain rewards (reward sensitivity), however, differs between individuals. Here, we assessed the association between brain responses to calories in the mouth and trait reward sensitivity in different hunger states. Firstly, we assessed this in data from a functional neuroimaging study (van Rijn et al., 2015), in which participants (n = 30) tasted simple solutions of a non-caloric sweetener with or without a non-sweet carbohydrate (maltodextrin) during hunger and satiety. Secondly, we expanded these analyses to regular drinks by assessing the same relationship in data from a study in which soft drinks sweetened with either sucrose or a non-caloric sweetener were administered during hunger (n = 18) (Griffioen-Roose et al., 2013). First, taste activation by the non-caloric solution/soft drink was subtracted from that by the caloric solution/soft drink to eliminate sweetness effects and retain activation induced by calories. Subsequently, this difference in taste activation was correlated with reward sensitivity as measured with the BAS drive subscale of the Behavioral Activation System (BAS) questionnaire. When participants were hungry and tasted calories from the simple solution, brain activation in the right ventral striatum (caudate), right amygdala and anterior cingulate cortex (bilaterally) correlated negatively with BAS drive scores. In contrast, when participants were satiated, taste responses correlated positively with BAS drive scores in the left caudate. These results were not replicated for soft drinks. Thus, neural responses to oral calories from maltodextrin were modulated by reward sensitivity in reward-related brain areas. This was not the case for sucrose. This may be due to the direct detection of maltodextrin, but not sucrose in the oral cavity. Also, in a familiar beverage, detection of calories per se may be overruled by a conditioned response to its flavor. In conclusion, the brain reward response to calories from a long chain starch sugar (maltodextrin) varies with trait reward sensitivity. The absence of this effect in a familiar beverage warrants further research into its relevance for real life ingestive behavior.

Project description:Importance:Psychoticlike experiences (PLEs) are subclinical manifestations of psychotic symptoms and may reflect an increased vulnerability to psychotic disorders. Contemporary models of psychosis propose that dysfunctional reward processing is involved in the cause of these clinical illnesses. Objective:To examine the neuroimaging profile of healthy adolescents at 14 and 19 years old points with PLEs, using a reward task. Design, Setting, and Participants:A community-based cohort study, using both a cross-sectional and longitudinal design, was conducted in academic centers in London, Nottingham, United Kingdom, and Dublin, Ireland; Paris, France; and Berlin, Hamburg, Mannheim, and Dresden, Germany. A group of 1434 healthy adolescent volunteers was evaluated, and 2 subgroups were assessed at ages 14 and 19 years. Those who scored as either high or low PLE (based on the upper and lower deciles) on the Community Assessment of Psychic Experiences Questionnaire (CAPE-42) at age 19 years were included in the analysis. The study was conducted from January 1, 2016, to January 1, 2017. Main Outcomes and Measures:Participants were assessed at age 14 and 19 year points using functional magnetic resonance imaging while performing a monetary incentive delay reward task. A first-level model focused on 2 predefined contrasts of anticipation and feedback of a win. The second-level analysis examined activation within the reward network using an a priori-defined region of interest approach. The main effects of group, time, and their interaction on brain activation were examined. Results:Of the 1434 adolescents, 2 groups (n = 149 each) (high PLEs, n = 149, 50 [33.6%] male; low PLEs, n = 149, 84 [56.4%] male) were compared at ages 14 and 19 years. Two regions within the left and right middle frontal gyri showed a main effect of time on brain activation (F1, 93 = 5.559; P = .02; F1, 93 = 5.009; P = .03, respectively); there was no main effect of group. One region within the right middle frontal gyrus demonstrated a significant time × group interaction (F1, 93 = 7.448; P = .01). Conclusion and Relevance:The findings are consistent with evidence implicating alterations in prefrontal and striatal function during reward processing in the etiology of psychosis. Given the nature of this nonclinical sample this may reflect a combination of aberrant salience yielding abnormal experiences and a compensatory cognitive control mechanism necessary to contextualize them.

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Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence.

Publications

Longitudinal changes in behavioral approach system sensitivity and brain structures involved in reward processing during adolescence.

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