Regional brain response to visual food cues is a marker of satiety that predicts food choice

Abstract

Background: Neuronal processes that underlie the subjective experience of satiety after a meal are not well defined.

Objective: We investigated how satiety alters the perception of and neural response to visual food cues.

Design: Normal-weight participants (10 men, 13 women) underwent 2 fMRI scans while viewing images of high-calorie food that was previously rated as incompatible with weight loss and "fattening" and low-calorie, "nonfattening" food. After a fasting fMRI scan, participants ate a standardized breakfast and underwent reimaging at a randomly assigned time 15-300 min after breakfast to vary the degree of satiety. Measures of subjective appetite, food appeal, and ad libitum food intake (measured after the second fMRI scan) were correlated with activation by "fattening" (compared with "nonfattening") food cues in a priori regions of interest.

Results: Greater hunger correlated with higher appeal ratings of "fattening" (r = 0.46, P = 0.03) but not "nonfattening" (r = -0.20, P = 0.37) foods. Fasting amygdalar activation was negatively associated with fullness (left: r = -0.52; right: r = -0.58; both P ≤ 0.01), whereas postbreakfast fullness was positively correlated with activation in the dorsal striatum (right: r = 0.44; left: r = 0.45; both P < 0.05). After breakfast, participants with greater activation in 4 regions-medial orbital frontal cortex (r = 0.49, P < 0.05), left amygdala (r = 0.49, P < 0.05), left insula (r = 0.47, P < 0.05), and nucleus accumbens (right: r = 0.57, P < 0.01; left: r = 0.43, P < 0.05)-chose buffet foods with higher fat content.

Conclusions: Postmeal satiety is shown in regional brain activation by images of high-calorie foods. Regions including the amygdala, nucleus accumbens, and dorsal striatum may alter perception of, and reduce motivation to consume, energy-rich foods, ultimately driving food choice. This trial was registered at clinicaltrials.gov as NCT01631045.

Figures

FIGURE 1.

Schematic of the study protocol. Participants (n = 23) underwent a fasting fMRI scanning session beginning at 0830 h followed by a standardized breakfast with 20% of their estimated daily caloric needs. Each participant was randomly assigned to a second fMRI session time (15, 30, 60, 120, 180, 240, or 300 min after the start of their standardized breakfast) to vary satiety across participants. Immediately after the second fMRI scanning session, participants were presented with an ad libitum buffet. Participants completed serial visual analog scale appetite ratings; appeal ratings followed each fMRI scanning session.

FIGURE 2.

Time elapsed since breakfast is related to subjective and objective measures of satiety. A, B: VAS appetite ratings; C, D: measures of food intake at the ad libitum buffet; E, F: subjective ratings of the appeal of “fattening” compared with “nonfattening” foods. Fattening food images depicted high-calorie foods that were previously rated as incompatible with weight loss and considered fattening. Pearson's correlation coefficients are presented with P values derived from linear regression (n = 20; 3 participants were excluded for consuming <20% of estimated needs at the standardized breakfast). VAS, visual analog scale.

FIGURE 3.

A–J: Ratings of food appeal and their correlation with measures of subjective and objective appetite. Appeal ratings were obtained immediately after the first fMRI scan (fasting) and second fMRI scan (postbreakfast). “Fattening” food images depicted high-calorie foods that were previously rated as incompatible with weight loss and considered fattening. In the fasted state, participants’ (n = 23) appeal ratings for fattening food, but not for nonfattening food, were positively associated with hunger and negatively associated with fullness. Postbreakfast appeal for fattening food, but not for nonfattening food, predicted the number of calories consumed at an ad libitum buffet but not food choice. Percentage fat (range: 7–46%) and carbohydrate (range: 39–90%) intake data were transformed by using a Box-Cox transformation. Pearson's correlation coefficients are presented with P values derived from linear regression. Ad lib, ad libitum; Carb, carbohydrate; VAS, visual analog scale.

FIGURE 4.

A–J: Activation by fattening food cues is a marker of subjective appetite in the amygdala, medial OFC, and dorsal striatum. Left panels: coronal sections of bilateral amygdala and bilateral dorsal striatum ROIs and sagittal section of the medial OFC ROI. Right panels: plots of individual mean ROI parameter estimates (n = 23) for the contrast fattening > nonfattening foods compared with average VAS appetite ratings for the fasting and postbreakfast fMRI scan. “Fattening” food images depicted high-calorie foods that were previously rated as incompatible with weight loss and considered fattening. Pearson's correlation coefficients are presented with P values derived from linear regression. A, anterior; L, left; OFC, orbital frontal cortex; P, posterior; R, right; ROI, region of interest; VAS, visual analog scale.

FIGURE 5.

A–E: Greater activation by fattening food cues predicts increased intake of calories from fat. Participants (n = 23) underwent fMRI scans at randomly assigned times after a standardized breakfast, followed by ad libitum intake of foods at a buffet. Left panels: coronal sections of bilateral nucleus accumbens, left amygdala, and left insula ROIs and sagittal section of the medial OFC ROI. Right panels: plots of individual mean ROI parameter estimates for the contrast fattening > nonfattening foods compared with percentage of fat intake. “Fattening” food images depicted high-calorie foods that were previously rated as incompatible with weight loss and considered fattening. Percentage fat intake data (range: 7–46%) were transformed by using a Box-Cox transformation. A, anterior; L, left; OFC, orbital frontal cortex; P, posterior; R, right; ROI, region of interest.