Frontostriatal and behavioral adaptations to daily sugar-sweetened beverage intake: a randomized controlled trial

Abstract

Background: Current obesity theories suggest that the repeated intake of highly palatable high-sugar foods causes adaptions in the striatum, parietal lobe, and prefrontal and visual cortices in the brain that may serve to perpetuate consumption in a feed-forward manner. However, the data for humans are cross-sectional and observational, leaving little ability to determine the temporal precedence of repeated consumption on brain response.Objective: We tested the impact of regular sugar-sweetened beverage intake on brain and behavioral responses to beverage stimuli.Design: We performed an experiment with 20 healthy-weight individuals who were randomly assigned to consume 1 of 2 sugar-sweetened beverages daily for 21 d, underwent 2 functional MRI sessions, and completed behavioral and explicit hedonic assessments.Results: Consistent with preclinical experiments, daily beverage consumption resulted in decreases in dorsal striatal response during receipt of the consumed beverage (r = -0.46) and decreased ventromedial prefrontal response during logo-elicited anticipation (r = -0.44). This decrease in the prefrontal response correlated with increases in behavioral disinhibition toward the logo of the consumed beverage (r = 0.54; P = 0.02). Daily beverage consumption also increased precuneus response to both juice logos compared with a tasteless control (r = 0.45), suggesting a more generalized effect toward beverage cues. Last, the repeated consumption of 1 beverage resulted in an explicit hedonic devaluation of a similar nonconsumed beverage (P < 0.001).Conclusions: Analogous to previous reports, these initial results provide convergent data for a role of regular sugar-sweetened beverage intake in altering neurobehavioral responses to the regularly consumed beverage that may also extend to other beverage stimuli. Future research is required to provide evidence of replication in a larger sample and to establish whether the neurobehavioral adaptations observed herein are specific to high-sugar and/or nonnutritive-sweetened beverages or more generally related to the repeated consumption of any type of food. This trial was registered at clinicaltrials.gov as NCT02624206.

Keywords: dorsal striatum; fMRI; habit-based decision making; obesity; reward; sugar-sweetened beverage; ventromedial prefrontal cortex.

© 2017 American Society for Nutrition.

Figures

FIGURE 1

Individual participant study timeline (A) and flow of all samples through the intervention (B).

FIGURE 2

Sample epoch timing for the juice and anticipation fMRI paradigm.

FIGURE 3

Alterations in brain response as a function of daily beverage consumption. (A) Changes in brain response during exposure to the assigned anticipatory logo in the vmPFC presented in axial slices and (B) parameter estimates of brain response graphically represented at baseline and follow-up. (C) Changes in brain response during the intake of the assigned sugar-sweetened beverage in the caudate presented in axial slices and (D) parameter estimates of brain response graphically represented at baseline and follow-up. The color bands in panels A and C reflect the t value of the BOLD response. dACC, dorsal anterior cingulate cortex; vmPFC, ventromedial prefontal cortex.

FIGURE 4

Alterations in behavioral responses and explicit hedonic ratings as a function of daily beverage consumption. Significant changes in (A) reaction times toward juice logos, (B) juice pleasantness, and (C) desire to consume juice from baseline to follow-up are shown. The full scales in panels B and C ranging from −100 to 100 (with 0 indicating neutral) were truncated for display purposes.

FIGURE 5

The impact of daily beverage consumption on body mass and hedonic ratings throughout the intervention. No significant changes were observed in (A) body mass and (B and C) perceptual hedonic ratings of the assigned juice over the 3-wk intervention period. The full scales shown in panels B and C ranging from −100 to 100 (with 0 indicating neutral) were truncated for display purposes.