Sexually dimorphic functional connectivity in response to high vs. low energy-dense food cues in obese humans: an fMRI study

Abstract

Sexually-dimorphic behavioral and biological aspects of human eating have been described. Using psychophysiological interaction (PPI) analysis, we investigated sex-based differences in functional connectivity with a key emotion-processing region (amygdala, AMG) and a key reward-processing area (ventral striatum, VS) in response to high vs. low energy-dense (ED) food images using blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) in obese persons in fasted and fed states. When fed, in response to high vs. low-ED food cues, obese men (vs. women) had greater functional connectivity with AMG in right subgenual anterior cingulate, whereas obese women had greater functional connectivity with AMG in left angular gyrus and right primary motor areas. In addition, when fed, AMG functional connectivity with pre/post-central gyrus was more associated with BMI in women (vs. men). When fasted, obese men (vs. women) had greater functional connectivity with AMG in bilateral supplementary frontal and primary motor areas, left precuneus, and right cuneus, whereas obese women had greater functional connectivity with AMG in left inferior frontal gyrus, right thalamus, and dorsomedial prefrontal cortex. When fed, greater functional connectivity with VS was observed in men in bilateral supplementary and primary motor areas, left postcentral gyrus, and left precuneus. These sex-based differences in functional connectivity in response to visual food cues may help partly explain differential eating behavior, pathology prevalence, and outcomes in men and women.

Keywords: Food cues; Gender; Neural connectivity; Obese; PPI; fMRI.

Figure 1

Sex-based differences in functional connectivity with amygdala (AMG) in response to visual high vs. low-ED food cues. Top left) When fed, obese males (vs. females) had greater functional connectivity with AMG in sub-genual anterior cingulate (z=-12, -8). Top right whereas females had greater connectivity with AMG in angular (z=36) and precentral gyrus (z=48). Lower left) When fasted obese males had greater functional connectivity with AMG in precuneus (z=22, 28), supplementary motor area and precentral gyrus (z=40, 60). Lower Right) whereas females had greater functional connectivity with AMG in thalamus and inferior frontal gyrus (z=0) and dorsomedial prefrontal gyrus (z=52) (M=males, F=females). Only supra-threshold clusters are mentioned in this caption; for sub-threshold cluster labels see Tables 1 and 2.

Figure 2

Sex-based differences in functional connectivity with ventral striatum (VS) in response to visual high vs. low-ED food cues. Top left and right: When fed, no supra-threshold clusters appeared in obese males greater than females nor for females greater than males (panels depict sub-threshold clusters; see Table 3 for labels.Bottom left: When fasted, obese males had greater neural connectivity with VS in precentral gyrus (z=44, 52), supplementary motor area (z=64, 68) and precuneus (z=68). Bottom right: When fasted, no supra-threshold clusters appeared in obese females greater than males (panels depict sub-threshold clusters; see Table 4 for labels). (M=males, F=females).