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Elevated reward response to receipt of palatable food predicts future weight variability in healthy-weight adolescents.

ABSTRACT: Background: Both an elevated brain-reward-region response to palatable food and elevated weight variability have been shown to predict future weight gain.Objective: We examined whether the brain-reward response to food is related to future weight variability.Design: A total of 162 healthy-weight adolescents, who were aged 14-18 y at baseline, were enrolled in the study and were assessed annually over a 3-y follow-up period with 127 participants completing the final 3-y follow-up assessment. With the use of functional magnetic resonance imaging, we tested whether the neural responses to a cue that signaled an impending milkshake receipt and the receipt of the milkshake predicted weight variability over the follow-up period. Weight variability was modeled with a root mean squared error method to reflect fluctuations in weight independent of the net weight change.Results: Elevated activation in the medial prefrontal cortex and supplementary motor area, cingulate gyrus, cuneus and occipital gyrus, and insula in response to milkshake receipt predicted greater weight variability. Greater activation in the precuneus and middle temporal gyrus predicted lower weight variability.Conclusions: From our study data, we suggest that the elevated activation of reward and emotional-regulation brain regions (medial prefrontal cortex, cingulate cortex, and insula) and lower activation in self-reference regions (precuneus) in response to milkshake receipt predict weight variability over 3 y of follow-up. The fact that the reward response in the current study emerged in response to high-calorie palatable food receipt suggests that weight variability may be a measure of propensity periods of a positive energy balance and should be examined in addition to measures of the net weight change. With our collective results, we suggest that weight variability and its brain correlates should be added to other variables that are predictive of weight gain to inform the design of obesity-preventive programs in adolescents. This trial was registered at clinicaltrials.gov as NCT01807572.

SUBMITTER: Winter SR

PROVIDER: S-EPMC5366045 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Elevated reward response to receipt of palatable food predicts future weight variability in healthy-weight adolescents.

Winter Samantha R SR Yokum Sonja S Stice Eric E Osipowicz Karol K Lowe Michael R MR

The American journal of clinical nutrition 20170222 4

Background: Both an elevated brain-reward-region response to palatable food and elevated weight variability have been shown to predict future weight gain.Objective: We examined whether the brain-reward response to food is related to future weight variability.Design: A total of 162 healthy-weight adolescents, who were aged 14-18 y at baseline, were enrolled in the study and were assessed annually over a 3-y follow-up period with 127 participants completing the final 3-y follo ...[more]

PMID: 28228422

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Project description:Because no large prospective study has investigated neural vulnerability factors that predict future weight gain, we tested whether neural response to receipt and anticipated receipt of palatable food and monetary reward predicted body fat gain over a 3-year follow-up in healthy-weight adolescent humans and whether the TaqIA polymorphism moderates these relations. A total of 153 adolescents completed fMRI paradigms assessing response to these events; body fat was assessed annually over follow-up. Elevated orbitofrontal cortex response to cues signaling impending milkshake receipt predicted future body fat gain (r = 0.32), which is a novel finding that provides support for the incentive sensitization theory of obesity. Neural response to receipt and anticipated receipt of monetary reward did not predict body fat gain, which has not been tested previously. Replicating an earlier finding (Stice et al., 2008a), elevated caudate response to milkshake receipt predicted body fat gain for adolescents with a genetic propensity for greater dopamine signaling by virtue of possessing the TaqIA A2/A2 allele, but lower caudate response predicted body fat gain for adolescents with a genetic propensity for less dopamine signaling by virtue of possessing a TaqIA A1 allele, though this interaction was only marginal [p-value <0.05 corrected using voxel-level familywise error rate (pFWE) = 0.06]. Parental obesity, which correlated with TaqIA allele status (odds ratio = 2.7), similarly moderated the relation of caudate response to milkshake receipt to future body fat gain, which is another novel finding. The former interaction implies that too much or too little dopamine signaling and reward region responsivity increases risk for overeating, suggesting qualitatively distinct reward surfeit and reward deficit pathways to obesity.Because no large prospective study has investigated neural vulnerability factors that predict future weight gain we tested whether neural response to receipt and anticipated receipt of palatable food and monetary reward predicted body fat gain over 3-year follow-up in healthy-weight adolescent humans and whether the TaqIA polymorphism moderates these relations. Elevated reward activation in response to food cues predicted future body fat gain. Elevated reward response to food receipt predicted body fat gain for adolescents with a TaqIA A2/A2 allele and lower reward response predicted body fat gain for those with a TaqIA A1 allele. Results imply that too much or too little dopamine signaling and reward region responsivity increases risk for overeating.

Project description:BackgroundEmerging data suggest that weight gain is associated with changes in neural response to palatable food tastes and palatable food cues, which may serve to maintain overeating.ObjectiveWe investigated whether weight gain is associated with neural changes in response to tastes of milkshakes varying in fat and sugar content and palatable food images.MethodsWe compared changes in neural activity between initially healthy-weight adolescents who gained weight (n = 36) and those showing weight stability (n = 31) over 2-3 y.ResultsAdolescents who gained weight compared with those who remained weight stable showed decreases in activation in the postcentral gyrus, prefrontal cortex, insula, and anterior cingulate cortex, and increases in activation in the parietal lobe, posterior cingulate cortex, and inferior frontal gyrus in response to a high-fat/low-sugar compared with low-fat/low-sugar milkshake. Weight gainers also showed greater decreases in activation in the anterior insula and lateral orbitofrontal cortex in response to a high-fat/high-sugar compared with low-fat/low-sugar milkshake than those who remained weight stable. No group differences emerged in response to a low-fat/high-sugar compared with a low-fat/low-sugar milkshake. Weight gainers compared with those who remained weight stable showed greater decreases in activation in the middle temporal gyrus and increases in cuneus activation in response to appetizing compared with unappetizing food pictures. The significant interactions were partially driven by group differences in baseline responsivity and by opposite changes in neural activation in adolescents who remained weight stable.ConclusionsData suggest that weight gain is associated with a decrease in responsivity of regions associated with taste and reward processing to palatable high-fat- and high-fat/high-sugar food tastes. Data also suggest that avoiding weight gain increases taste sensitivity, which may prevent future excessive weight gain.This trial was registered at clinicaltrials.gov as NCT01949636.

Dataset Information

Elevated reward response to receipt of palatable food predicts future weight variability in healthy-weight adolescents.

Publications

Elevated reward response to receipt of palatable food predicts future weight variability in healthy-weight adolescents.

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