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.

Brain white matter microstructure in obese women with binge eating disorder

“…Based on our data, we propose that in BED, WM alterations in AD and FA in pathways connecting fronto‐limbic and temporal–parietal regions may be associated with repetitive difficulties during processes of eating‐related decisions (Bissonette & Roesch, 2016; Ostlund & Balleine, 2005; Steward et al, 2019).…”

Whole‐brain functional connectivity correlates of obesity phenotypes

“…Further, increased macroscale connectivity, particularly in the prefrontal, parietal, and cingulate cortices is known to be related to eating behaviors in people with obesity (Park et al, 2016; Park, Lee, et al, 2018; Park, Moon, et al, 2018). Indeed, imbalance in inhibitory control and food‐related reward system in the prefrontal cortex and paralimbic areas is associated with increased feelings of hunger (Tataranni et al, 1999; Tataranni & DelParigi, 2003) and may lead to overeating and weight gain (Brooks et al, 2013; Ding et al, 2020; Olivo et al, 2017; Steward, Juaneda‐Seguí, et al, 2019; Steward, Picó‐Pérez, et al, 2019; Vainik, Dagher, Dubé, & Fellows, 2013; Van Meer et al, 2019; Van Opstal et al, 2018; Van Opstal et al, 2019; Verdejo‐Román et al, 2017; Volkow, Wang, Telang, et al, 2008; Ziauddeen et al, 2015). In contrast, we found negative associations with obesity phenotypes in brain regions involved in multisensory processing, particularly precentral gyrus, inferior temporal gyrus, fusiform gyrus, superior temporal sulcus, and thalamus.…”

“…First, we used a large‐scale ( n ~ 2,400) fMRI dataset spanning four independent sites. Many previous studies had used small sample sizes and single cohorts, perhaps resulting in conflicting reports concerning obesity phenotype‐associated brain regions (Ding et al, 2020; Gupta et al, 2017; Herrmann et al, 2019; Marqués‐Iturria et al, 2013; Van Meer et al, 2019; Opel et al, 2015; Van Opstal et al, 2019; Park et al, 2015; Park et al, 2016; Park, Lee, et al, 2018; Park, Moon, et al, 2018; Shott et al, 2015; Steward, Picó‐Pérez, et al, 2019; Stoeckel et al, 2008). Our study attempted to circumvent these shortcomings by leveraging a large‐scale dataset from different cohorts, which included a wide range of ages and ethnicities.…”

“…Neurobiological studies have found that dysregulation of reward and inhibitory circuits gives rise to an increased threshold for satiation, ultimately leading to overeating (Martin et al, 2010; Murray et al, 2014; Steward, Miranda‐Olivos, Soriano‐Mas, & Fernández‐Aranda, 2019; Val‐Laillet et al, 2015; Van Opstal et al, 2018; Verdejo‐Román et al, 2017; Ziauddeen et al, 2015). Recent neuroimaging studies have increasingly shown associations between obesity and alterations in cortical and subcortical morphology (Herrmann, Tesar, Beier, Berg, & Warrings, 2019; Marqués‐Iturria et al, 2013; Shott et al, 2015), brain activity (Brooks, Cedernaes, & Schiöth, 2013; Goldstone et al, 2009; Gupta et al, 2018; Opel et al, 2015; Park, Hong, & Park, 2017; Steward, Juaneda‐Seguí, et al, 2019; Stoeckel et al, 2008; Van Meer et al, 2019), functional connectivity (García‐García et al, 2013; García‐García et al, 2015; Lips et al, 2014; Park, Seo, & Park, 2016; Park, Seo, Yi, & Park, 2015), and diffusivity (Gupta et al, 2017; Olivo et al, 2017; Steward, Picó‐Pérez, et al, 2019). These studies collectively show that the pathophysiology of obesity is associated with various types of brain measurements.…”

What Difference Does it Make? Risk-Taking Behavior in Obesity after a Loss is Associated with Decreased Ventromedial Prefrontal Cortex Activity

“…This finding suggests the existence of a high-risk subset of individuals with OB that is characterized by decreased vmPFC activation and higher risk taking. Indeed, one recent study linked vmPFC alterations to emotion regulation deficits in OB [35], and impulsive eating behaviors have been associated with poorer decision making on the Iowa Gambling Task, a task whose performance is understood to be contingent on vmPFC activity [36]. Previous research has posited that the vmPFC, which is generally active in risk-taking tasks, integrates cognitive control and affect signals to attribute value to stimuli, to associate that value with choices, and to determine whether it should be approached or avoided [37].…”