A multimodal MRI study of the neural mechanisms of emotion regulation impairment in women with obesity

Abstract

Maladaptive emotion regulation contributes to overeating and impedes weight loss. Our study aimed to compare the voluntary downregulation of negative emotions by means of cognitive reappraisal in adult women with obesity (OB) and female healthy controls (HC) using a data-driven, multimodal magnetic resonance imaging (MRI) approach. Women with OB (n = 24) and HC (n = 25) carried out an emotion regulation task during functional MRI scanning. Seed-to-voxel resting-state connectivity patterns derived from activation peaks identified by this task were compared between groups. Diffusion tensor imaging (DTI) was used to examine white matter microstructure integrity between regions exhibiting group differences in resting-state functional connectivity. Participants in the OB group presented reduced activation in the ventromedial prefrontal (vmPFC) cortex in comparison to the HC group when downregulating negative emotions, along with heightened activation in the extrastriate visual cortex (p < 0.05, AlphaSim-corrected). Moreover, vmPFC peak activity levels during cognitive reappraisal were negatively correlated with self-reported difficulties in emotion regulation. OB patients exhibited decreased functional connectivity between the vmPFC and the temporal pole during rest (peak-pFWE = 0.039). Decreased fractional white-matter track volume in the uncinate fasciculus, which links these two regions, was also found in participants with OB. Taken together, our findings are indicative of emotion regulation deficits in OB being underpinned by dysfunctional hypoactivity in the vmPFC and hyperactivity in the extrastriate visual cortex. Our results provide a potential target circuit for neuromodulatory interventions to improve emotion regulation skills and weight-loss intervention outcomes.

Fig. 1

a Increased activation was found in the left ventromedial prefrontal cortex (vmPFC) in the healthy control group in comparison to the obese group (p < 0.05, AlphaSim cluster-extent corrected) during the emotion regulation task (Regulate vs. Maintain). Color bar represents t-values. b A scatterplot depicting the negative association between extracted activation eigenvalues from the vmPFC peak during the emotion regulation task (Regulate vs. Maintain) and Difficulties in Emotion Regulation Scale (DERS) total scores in the obesity group [n = 24, r(22) = −0.466, p = 0.022)]. Error bars show the 95% confidence interval. c Increased task-induced connectivity between the vmPFC and the left globus pallidus was found in the healthy control group in comparison to the obesity group using psychophysiological interactions (PPI) analysis (p < 0.05, AlphaSim cluster-extent corrected). Color bar represents t-values

Fig. 2

a Brain regions showing increased activation in the obese group during the emotion regulation task (Regulate vs. Maintain). Increased activation was found in the right extrastriatal visual cortex in the obese group in comparison to the HC group (p < 0.05, AlphaSim cluster-extent corrected). Color bar represents t-values. b A scatterplot depicting the positive correlation between extracted activation eigenvalues from the extrastriatal visual cortex peak during the emotion regulation task (Regulate vs. Maintain) and total body fat percentage in the control group [n = 25, (r(23) = 0.431, p = 0.031)]. Error bars show the 95% confidence interval (CI). c Increased psychophysiological interactions (PPI) connectivity using the extrastriatal visual cortex as a seed was found in the left inferior temporal lobe, the left precuneus, and the left supramarginal gyrus in the obese group in comparison to the healthy control group. Color bar represents t-values

Fig. 3

a Targets for probabilistic fiber tracking, derived from the resting-state analyses results (featured in the box), included the left ventromedial prefrontal cortex (vmPFC) and the left temporal pole (marked in red). An example of the uncinate fasciculus tracts connecting the vmPFC target with the temporal pole target is shown (marked in yellow). SUMA/AFNI Surface Mapper software was used for DTI image preparation. b A scatterplot depicting the negative correlation between the fractional volume of the left uncinate fasciculus and residual Difficulties in Emotion Regulation Scale (DERS) Lack of Clarity scores in the obese group controlling for age [n = 21, r(19) = −0.624, p = 0.002]. Error bars show the 95% confidence interval (CI). *This correlation remained significant after excluding the highlighted subject (p = 0.003 vs. p = 0.010)