Brain Responses to Food Choices and Decisions Depend on Individual Hedonic Profiles and Eating Habits in Healthy Young Women

Abstract

The way different food consumption habits in healthy normal-weight individuals can shape their emotional and cognitive relationship with food and further disease susceptibility has been poorly investigated. Documenting the individual consumption of Western-type foods (i.e., high-calorie, sweet, fatty, and/or salty) in relation to psychological traits and brain responses to food-related situations can shed light on the early neurocognitive susceptibility to further diseases and disorders. We aimed to explore the relationship between eating habits, psychological components of eating, and brain responses as measured by blood oxygen level-dependent functional magnetic resonance imaging (fMRI) during a cognitive food choice task and using functional connectivity (FC) during resting-state fMRI (rsfMRI) in a population of 50 healthy normal-weight young women. A Food Consumption Frequency Questionnaire (FCFQ) was used to classify them on the basis of their eating habits and preferences by principal component analysis (PCA). Based on the PCA, we defined two eating habit profiles, namely, prudent-type consumers (PTc, N = 25) and Western-type consumers (WTc, N = 25), i.e., low and high consumers of western diet (WD) foods, respectively. The first two PCA dimensions, PCA1 and PCA2, were associated with different psychological components of eating and brain responses in regions involved in reward and motivation (striatum), hedonic evaluation (orbitofrontal cortex, OFC), decision conflict (anterior cingulate cortex, ACC), and cognitive control of eating (prefrontal cortex). PCA1 was inversely correlated with the FC between the right nucleus accumbens and the left lateral OFC, while PCA2 was inversely correlated with the FC between the right insula and the ACC. Our results suggest that, among a healthy population, distinct eating profiles can be detected, with specific correlates in the psychological components of eating behavior, which are also related to a modulation in the reward and motivation system during food choices. We could detect different patterns in brain functioning at rest, with reduced connectivity between the reward system and the frontal brain region in Western-type food consumers, which might be considered as an initial change toward ongoing modified cortico-striatal control.

Keywords: brain; decision-making; eating behavior; fMRI; healthy subjects; rsfMRI.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Coquery, Gautier, Serrand, Meurice, Bannier, Thibault, Constant, Moirand and Val-Laillet.

Figures

FIGURE 1

Overall study design. With the principal component analysis (PCA) performed on the Food Frequency Questionnaire (FCFQ) data obtained from 178 volunteers, 50 participants were selected by the values of the first PCA axis (PCA1) that discriminated Western-type from prudent-type consumers (WTc, with high PCA1 values vs. PTc, with low PCA1 values). The first two axes of the PCA (PCA1 and PCA2) were used to further characterize the 50 selected participants.

FIGURE 2

Principal component analysis (PCA) performed on the Food Frequency Questionnaire data obtained from 178 volunteers, with the (A) projection vectors of the different food items included in the questionnaire focused on Western-type foods, and (B) individual values projected on the first two axes of the PCA. WTc, Western-type consumers (N = 25) with the highest values for PCA1 among the 50 volunteers selected for the brain imaging study. PTc, prudent-type consumers (N = 25) with the lowest values for PCA1 among the 50 volunteers selected for the brain imaging study. The first two axes of the PCA bear, respectively, 22.39 and 13.92% of the population variability.

FIGURE 3

Brain activations detected in the fMRI two-choice task viewed in coronal slices (A) for all participants (n = 50), (B) depending on the PCA1 values, and (C) depending on PCA2 values. MNI y-coordinates are indicated for each coronal slice. ACC, anterior cingulate cortex; MCC, middle cingulate cortex; Fus, fusiform gyrus; LG, lingual gyrus; PreC, precuneus; PCG, posterior central gyrus; FMG, frontal middle gyrus; FSG, frontal superior gyrus; SupMotor, superior motor gyrus; Thal, thalamus; Ins, insular cortex; OFC, orbitofrontal cortex; SCA, subgenual cingulate area; Put, putamen; Cd, caudate nucleus; Ac, accumbens nucleus.

FIGURE 4

Resting-state functional magnetic resonance imaging functional connectivity maps (conn toolbox). (A) Depending on the PCA1 values with the right accumbens as seed and (B) depending on PCA2 values with the right insula as seed. MNI coordinates are indicated for each coronal slice. OFC, orbitofrontal cortex; ACC, anterior cingulate cortex.