Weight gain is associated with changes in neural response to palatable food tastes varying in sugar and fat and palatable food images: a repeated-measures fMRI study

Abstract

Background: Emerging 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.

Objective: We 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.

Methods: We 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.

Results: Adolescents 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.

Conclusions: Data 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.

Keywords: food image; food taste; repeated-measures fMRI; reward; taste processing; weight gain.

FIGURE 1

Significant group-by-time interactions in the right postcentral gyrus (A) (MNI coordinates: 33, −30, 45, Z = 6.97, k = 760), right insula (B) (MNI coordinates: 42, 0, 15, Z = 5.13, k = 92), and left precuneus (C) (MNI coordinates: −3, −66, 18, Z = 5.25, k = 102) in response to the high-fat/low-sugar > low-fat/low-sugar milkshake contrast at follow-up compared with baseline in the weight-gain (n = 36) compared with the weight-stable group (n = 31). Bar graphs represent mean parameter estimates (PE) per group extracted from the local peak response (i.e., right postcentral gyrus, right insula, and left precuneus) denoted by the crosshairs. Group-by-time interactions were analyzed with the use of 2 group (weight gain, weight stable) × 2 time (baseline, follow-up) repeated-measures ANOVA models. Peak coordinates within the clusters were considered significant at P uncorrected < 0.001, k ≥ 54, equal to P < 0.05, FWE-corrected for multiple comparison across the whole brain. FWE, family-wise error; MNI, Montreal Neurological Institute.

FIGURE 2

Significant group-by-time interactions in the left anterior insula (A) (MNI coordinates: −27, 21, −9, Z = 5.30, k = 77) and right lateral orbitofrontal cortex (B) (MNI coordinates: 33, 27, −12, Z = 5.19, k = 65) in response to the high-fat/high-sugar > low-fat/low-sugar milkshake contrast at follow-up compared with baseline in the weight-gain (n = 36) compared with the weight-stable group (n = 31). Bar graphs represent mean parameter estimates (PE) per group extracted from the local peak response (i.e., left anterior insula, right lateral orbitofrontal cortex) denoted by the crosshairs. Group-by-time interactions were analyzed with the use of 2 group (weight gain, weight stable) × 2 time (baseline, follow-up) repeated-measures ANOVA models. Peak coordinates within the clusters were considered significant at P uncorrected < 0.001, k ≥ 54, equal to P < 0.05, FWE-corrected for multiple comparison across the brain. FWE, family-wise error; MNI, Montreal Neurological Institute.

FIGURE 3

Significant group-by-time interactions in the left middle temporal gyrus (A) (MNI coordinates: 18, −96, −9, Z = 3.87, k = 58) and right cuneus (B) (MNI coordinates: 18, −96, −9, Z = 3.87, k = 58) in response to the appetizing food images > unappetizing food images contrast at follow-up compared with baseline in the weight-gain (n = 36) compared with the weight-stable (n = 31) group. Bar graphs represent mean parameter estimates (PE) per group extracted from the local peak response (i.e., middle temporal gyrus, right cuneus) denoted by the crosshairs. Group-by-time interactions were analyzed with the use of 2 group (weight gain, weight stable) × 2 time (baseline, follow-up) repeated-measures ANOVA models. Peak coordinates within the clusters were considered significant at P uncorrected < 0.001, k ≥ 53, equal to P < 0.05, FWE-corrected for multiple comparison across the whole brain. FWE, family-wise error; MNI, Montreal Neurological Institute.