Mesolimbic white matter connectivity mediates the preference for sweet food

Abstract

Dopaminergic brain structures like the nucleus accumbens (NAc) are thought to encode the incentive salience of palatable foods motivating appetitive behaviour. Animal studies have identified neural networks mediating the regulation of hedonic feeding that comprise connections of the NAc with the ventral tegmental area (VTA) and the lateral hypothalamus (LH). Here, we investigated how structural connectivity of these pathways relates to individual variability in decisions on sweet food consumption in humans. We therefore combined probabilistic tractography on diffusion imaging data from 45 overnight fasted lean to overweight participants with real decisions about high and low sugar food consumption. Across all individuals, sugar preference and connectivity strength were not directly related, however, multiple regression analysis revealed interaction of mesolimbic structure and sugar preference to depend on individuals' BMI score. In overweight individuals (BMI: ≥25 kg/m², N = 22) higher sugar preference was thereby specifically related to stronger connectivity within the VTA-NAc pathway while the opposite pattern emerged in participants with normal BMI (BMI: <25 kg/m², N = 23). Our structural results complement previous functional findings on the critical role of the human mesolimbic system for regulating hedonic eating in overweight individuals.

Figure 1

Food wanting task and behavioural data. (a,b) Food wanting task: Participants indicated in a two-step procedure how much they wanted to eat the displayed food at the moment. The wanting (a) or rejection (b) of an item was followed by 4-point rating scale ranging from weakest wanting (+) or rejection (−) to strongest wanting (++++) or rejection (− − − −). Answers selected by the participant were highlighted in green in order to provide visual feedback (c/e) Behavioural data: Results from the two-step ratings were combined to a 8-point food wanting score (see text for details). Mean values across items for each participant are depicted in (c). Within subject correlation between the item-wise combined wanting rating and sugar (fat) content are shown for each participant (see text for details) in (d). Every point refers to the result/data of one participant; the black line represents the mean across all participants. BMI_norm: BMI: 18.5–24.9 kg/m², N = 23; BMI_over: BMI ≥ 25 kg/m², BMI_over, N = 22.

Figure 2

Results from structural connectivity analyses. (a,b) Group probability maps of VTA-Nac (a) and NAc-LH (b) tracts. Individual participant’s probabilistic tractography results were transformed into standard space, binarized, and summed across all subjects. For illustration purposes, the summed tract images were thresholded to show only overlapping pathways in 75% of subjects (i.e. N = 34). (c) Single-subject connectivity indices separated by BMI group. Every point refers to the data of one participant; the black line represents the mean across all participants. BMI_norm: BMI: 18.5–24.9 kg/m², N = 23; BMI_over: BMI ≥ 25 kg/m², N = 22.

Figure 3

Correlation between VTA-NAc structure and sugar wanting and its relationship with BMI. (a) The interaction of sugar wanting index and VTA-NAc connectivity correlated significantly with BMI. (b) Further exploration of this effect shows a significantly positive correlation between sugar wanting index and VTA-NAc connectivity only in the BMI_over group, which differed significantly from the correlation within the BMI_norm group (Z = 3.13, p = 0.001). Plots of non-significant results for the VTA-NAc tract are provided in the Supplementary Fig. S1.