Brain response to food cues varying in portion size is associated with individual differences in the portion size effect in children

Abstract

Large portions promote intake of energy dense foods (i.e., the portion size effect--PSE), but the neurobiological drivers of this effect are not known. We tested the association between blood oxygen level dependent (BOLD) brain response to food images varied by portion size (PS) and energy density (ED) and children's intake at test-meals of high- and low-ED foods served at varying portions. Children (N = 47; age 7-10 years) participated in a within-subjects, crossover study consisting of 4 meals of increasing PS of high- and low-ED foods and 1 fMRI to evaluate food images at 2 levels of PS (Large, Small) and 2 levels of ED (High, Low). Contrast values between PS conditions (e.g., Large PS - Small PS) were calculated from BOLD signal in brain regions implicated in cognitive control and reward and input as covariates in mixed models to determine if they moderated the PSE curve. Results showed a significant effect of PS on intake. Responses to Large relative to Small PS in brain regions implicated in salience (e.g., ventromedial prefrontal cortex and orbitofrontal cortex) were positively associated with the linear slope (i.e., increase in intake from baseline) of the PSE curve, but negatively associated with the quadratic coefficient for the total meal. Responses to Large PS High ED relative to Small PS High ED cues in regions associated with cognitive control (e.g., dorsolateral prefrontal cortex) were negatively associated with the linear slope of the PSE curve for high-ED foods. Brain responses to PS cues were associated with individual differences in children's susceptibility to overeating from large portions. Responses in food salience regions positively associated with PSE susceptibility while activation in control regions negatively associated with PSE susceptibility.

Trial registration: ClinicalTrials.gov NCT02759523.

Keywords: Brain; Eating behavior; Pediatrics; Portion size; fMRI.

Conflict of interest statement

Conflict of Interest: The authors declare no conflict of interest

Copyright © 2018 Elsevier Ltd. All rights reserved.

Figures

Figure 1

a) Mean intakes by weight (± SEM) as a function of weight of food served (g) for the total meal and for high-ED and low-ED foods served to 47 children. Mean curves of food intake in response to increases in the weight of food served were modeled using a random coefficient analysis. Individual curves were modeled for each child. The weight of food served significantly influenced intake by weight of the total meal (F1,41=17.9; P < 0.0001), and of high-ED (F1,41=17.1; P < 0.0001) and low-ED (F1,41=8.9; P < 0.005) foods analyzed separately. There were no differences in the intake curves as a function of energy density. b) Mean intakes by kcal (± SEM) as a function of weight of food served (g) for the total meal and for high-ED and low-ED foods served to 47 children. Mean curves of energy intake in response to increases in the weight of food served were modeled using a random coefficient analysis. Individual curves were modeled for each child. The weight of food served significantly influenced energy intake of the total meal (F1,41=20.8; P < 0.0001), and of high-ED (F1,41=17.1; P < 0.0001) and low-ED (F1,41=8.9; P < 0.005) foods analyzed separately.

Figure 2

a) Mean intakes by weight (± SEM) as a function of weight of food served (g) for the total meal for children who had high (red – square) or low (blue- circle) BOLD signal activation in the left vmPFC in response to Large PS > Small PS (collapsed across ED). High and low activation levels were categorized based on a median split. Activation in the vmPFC interacted with weight of food served to influence the trajectory of the PSE curve (F1,41 = 5.70; P = 0.02). Children who had high activation in the left vmPFC increased intake from baseline by 32% more than children who had low activation in the vmPFC in response to Large PS > Small PS. Overall, children with high vmPFC activation followed a curvilinear trajectory while children with low vmPFC activation followed a linear trajectory. b) Location of the ROI tested based on a 5-mm sphere drawn around the Talairach coordinates (x, y, z; −9, 45, 2) on a sample brain template created in BrainVoyager Brain Tutor (version 2.8, Brain Innovation, Maastricht, The Netherlands). Images are pictured from both the coronal (top) and transverse (bottom) views. c) Mean intakes by weight (± SEM) as a function of weight of food served (g) for the total meal for children who had high (red – square) or low (blue- circle) BOLD signal activation in the left OFC in response to Large PS > Small PS (collapsed across ED). High and low activation levels were categorized based on a median split. Activation in the OFC interacted with weight of food served to influence the trajectory of the PSE curve (F1,41 = 8.5; P = 0.004). Children who had high activation in the left OFC increased intake from baseline by 14% more than children who had low activation in the vmPFC in response to Large PS > Small PS. Overall, children with high OFC activation followed a curvilinear trajectory while children with low OFC activation followed a linear trajectory. d) Location of the ROI tested based on a 5-mm sphere drawn around the Talairach coordinates (x, y, z; −32, 29, −3) on a sample brain template created in BrainVoyager Brain Tutor (version 2.8, Brain Innovation, Maastricht, The Netherlands). Images are pictured from both the coronal (top) and transverse (bottom) views.

Figure 3

a) Mean intakes by weight (± SEM) as a function of weight of food served (g) for the total meal for children who had high (red – square) or low (blue- circle) BOLD signal activation in the right IFG in response to Large PS High ED > Small PS High ED. High and low activation levels were categorized based on a median split. Activation in the IFG interacted with weight of food served to influence the trajectory of the PSE curve (F1,41 = 17.04; P < 0.0001). Children who had low activation in the right IFG increased intake from baseline by 87% more than children who had high activation in the IFG in response to Large PS High ED > Small PS High ED. b) Location of the ROI tested based on a 5-mm sphere drawn around the Talairach coordinates (x, y, z; 50, 4, 16) on a sample brain template created in BrainVoyager Brain Tutor (version 2.8, Brain Innovation, Maastricht, The Netherlands). Images are pictured from both the coronal (top) and transverse (bottom) views. c) Mean intakes by weight (± SEM) as a function of weight of food served (g) for the total meal for children who had high (red – square) or low (blue- circle) BOLD signal activation in the right caudate in response to Large PS High ED > Small PS High ED. High and low activation levels were categorized based on a median split. Activation in the caudate interacted with weight of food served to influence the trajectory of the PSE curve (F1,41 = 4.9; P = 0.03). Children who had low activation in the right caudate increased intake from baseline by 57% more than children who had high activation in the caudate in response to Large PS High ED > Small PS High ED. Overall, children with high right caudate activation followed a linear trajectory while children with low right caudate activation followed a curvilinear trajectory. d) Location of the ROI tested based on a 5-mm sphere drawn around the Talairach coordinates (x, y, z; 14, 8, 22) on a sample brain template created in BrainVoyager Brain Tutor (version 2.8, Brain Innovation, Maastricht, The Netherlands). Images are pictured from both the coronal (top) and transverse (bottom) views.