Youth at risk for obesity show greater activation of striatal and somatosensory regions to food

Abstract

Obese humans, compared with normal-weight humans, have less striatal D2 receptors and striatal response to food intake; weaker striatal response to food predicts weight gain for individuals at genetic risk for reduced dopamine (DA) signaling, consistent with the reward-deficit theory of obesity. Yet these may not be initial vulnerability factors, as overeating reduces D2 receptor density, D2 sensitivity, reward sensitivity, and striatal response to food. Obese humans also show greater striatal, amygdalar, orbitofrontal cortex, and somatosensory region response to food images than normal-weight humans do, which predicts weight gain for those not at genetic risk for compromised dopamine signaling, consonant with the reward-surfeit theory of obesity. However, after pairings of palatable food intake and predictive cues, DA signaling increases in response to the cues, implying that eating palatable food contributes to increased responsivity. Using fMRI, we tested whether normal-weight adolescents at high- versus low-risk for obesity showed aberrant activation of reward circuitry in response to receipt and anticipated receipt of palatable food and monetary reward. High-risk youth showed greater activation in the caudate, parietal operculum, and frontal operculum in response to food intake and in the caudate, putamen, insula, thalamus, and orbitofrontal cortex in response to monetary reward. No differences emerged in response to anticipated food or monetary reward. Data indicate that youth at risk for obesity show elevated reward circuitry responsivity in general, coupled with elevated somatosensory region responsivity to food, which may lead to overeating that produces blunted dopamine signaling and elevated responsivity to food cues.

Figure 1.

A, B, Examples of timing and ordering of presentation of pictures and drinks during the food reward paradigm (A) and presentation of pictures during the monetary-reward paradigm (B).

Figure 2.

A–D, Greater activation in the right caudate (A: 6, 9, 24; Z = 3.14; p = 0.04, FDR; k = 3; B: 6, 9, 30; Z = 3.23, p = 0.04, FDR; k = 3), right frontal operculum (C: 39, 21, 21; Z = 3.44, p = 0.02, FDR; k = 5), and left parietal operculum (D: −54, 15, 21; Z = 3.36; p = 0.02, FDR; k = 2) in the high-risk versus low-risk group during milkshake receipt–tasteless receipt, with the bar graphs of parameter estimates from those peak voxels.

Figure 3.

A–D, Greater activation in high-risk versus low-risk group in response to the win–neutral display in the right putamen (A, square: 18, 0, 9; Z = 3.44; p = 0.018, FDR; k = 3), left putamen (circle: −18, 0, 12; Z = 3.74, p = 0.007, FDR, whole brain; k = 5) with bar graphs of the parameter estimates from those regions (B, right putamen; C, left putamen) and in the right orbitofrontal cortex (D: 45, 33, −6; Z = 5.61, p < 0.001, FDR; k = 16) with bar graphs of the parameter estimates from that voxel.