Elevated reward region responsivity predicts future substance use onset but not overweight/obesity onset

Abstract

Background: We tested the hypotheses that adolescents who show elevated reward region responsivity are at increased risk for initial onset of overweight/obesity and substance use, which is important because there have been no such prospective tests of the reward surfeit model of these motivated behaviors.

Methods: One hundred sixty-two adolescents (mean age = 15.3±1.06 years) with healthy weights (mean body mass index = 20.8±1.90) completed functional magnetic resonance imaging paradigms that assessed neural activation in response to receipt and anticipated receipt of palatable food and monetary reward; body fat and substance use were assessed at baseline and 1-year follow-up.

Results: Elevated caudate (r = .31, p<.001) and putamen (r = .28, p<.001) response to monetary reward predicted substance use onset over 1-year follow-up, but reward circuitry responsivity did not predict future overweight/obesity onset. Adolescents who reported substance use versus abstinence at baseline also showed less caudate (r =-.31, p<.001) response to monetary reward.

Discussion: Results show that hyper-responsivity of reward circuitry increases risk for future substance use onset, providing novel support for the reward surfeit model. Results also imply that even a limited substance use history was associated with reduced reward region responsivity, extending results from studies that compared substance-dependent individuals with healthy control subjects and suggesting that substance use downregulates reward circuitry. However, aberrant reward region responsivity did not predict initial unhealthy weight gain.

Figure 1

Example of timing and ordering of presentation of (A) pictures and beverages during the food reward paradigm and of (B) presentation of images and notification of monetary reward during the monetary reward paradigm.

Figure 2

Participants showing substance use onset by 1-year follow-up exhibited greater activation in (A) the caudate (Montreal Neurological Institute [MNI] coordinates: –9, 8, 1, Z = 3.93, k = 17) and putamen (MNI coordinates: 21, 11, 1, Z = 3.60, k = 12) in response to receipt of monetary reward compared with those reporting continued abstinence. Participants reporting substance use at baseline showed less activation in (B) the caudate (MNI coordinates: 21, –10, 31, Z = –3.98, k = 35) in response to receipt of monetary reward compared with participants reporting abstinence at baseline.