Nucleus accumbens microstructure mediates the relationship between obesity and eating behavior in adults

Abstract

Objective Basal ganglia regions are part of the brain’s reward‐processing networks and are implicated in the neurobiology of obesity and eating disorders. This study examines basal ganglia microstructural properties in adults with and without obesity. Methods Diffusion basis spectrum imaging (DBSI) images were analyzed to obtain putative imaging markers of neuroinflammation. Relationships between basal ganglia DBSI metrics and reward sensitivity and eating behaviors were also explored. Results A total of 46 participants (25 people with obesity; aged 20‐40 years; 37 women) were included. Relative to the people in the normal‐weight group, people with obesity had smaller caudate and larger nucleus accumbens (NAcc) volumes (p < 0.05) and lower DBSI fiber fraction (reflecting apparent axonal/dendrite density) in NAcc and putamen, higher DBSI nonrestricted fraction (reflecting tissue edema) in NAcc and caudate, and higher DBSI restricted fraction (reflecting tissue cellularity) in putamen (p ≤ 0.01, all). Increased emotional and reward eating behaviors were related to lower NAcc axonal/dendrite density and greater tissue edema (p ≤ 0.002). The relationships between emotional eating and adiposity measures were mediated by NAcc microstructure. Conclusions These findings provide evidence that microstructural alterations in basal ganglia relate to obesity and insights linking NAcc microstructure and eating behavior in adults.

Childhood obesity is linked to putative neuroinflammation in brain white matter, hypothalamus, and striatum

“…Overall, the pattern of our results in children agrees with previous DBSI assessments of obesityrelated neuroinflammation in adults (Ly et al, 2021;Samara et al, 2020Samara et al, , 2021. Patterns in apparent axonal/dendritic density (DBSI-FF) and cellularity (DBSI-RF) were spatially widespread in WM tracts in both adults and in children in the current study.…”

“…Furthermore, the association between baseline nucleus accumbens cellularity and future weight gain, as observed by us and others (Rapuano et al, 2020, 2022), relates to striatal neuroinflammation-mediated overfeeding in rodent studies (Décarie-Spain et al, 2018). Interestingly, we previously found that putative neuroinflammation in the nucleus accumbens mediates the relationship between obesity and greater self-reported emotional eating in adults (Samara et al, 2021) and Rapuano et al (2022) recently observed that greater putative cellular density in this region mediates the relationship between greater dietary fat intake and higher waist circumference and BMI in children. Taken together, the MRI-based assessments of the hypothalamus and striatum by our lab and others are consistent and report putative neuroinflammation in these regions in childhood obesity, in agreement with studies in rodent models and human adults.…”

“…Based on previously reported effect sizes for obesity-related neuroinflammation assessed by DBSI (Cohen’s d ’s ≥ 0.7) (Samara et al, 2021), RSI (Cohen’s d ’s ∼ 0.5) (Rapuano et al, 2020), and quantitative T2-weighted MRI (Cohen’s d ’s ≥ 0.65) (Sewaybricker et al, 2019; Sewaybricker, Melhorn, et al, 2021), a sample size of 140 would provide 0.8 statistical power at α = 0.05 to detect obesity-related neuroinflammation as assessed by DBSI. To better ensure sufficient power, which is often overestimated in power analyses, we first randomly selected 200 participants.…”

“…DBSI-assessed putative neuroinflammation in white matter (WM) correlates with cerebrospinal fluid biomarkers in Alzheimer's disease (Wang et al, 2019). Using DBSI, we have observed putative neuroinflammatory processes including cellularity, vasogenic edema, and lower apparent axonal and dendritic densities in white matter (WM) tracts, striatal, and limbic regions in adults with obesity (Samara et al, 2020(Samara et al, , 2021. DBSI has not yet been used to assess obesity-related putative neuroinflammation in children.…”

Longitudinal Evidence of a Vicious Cycle Between Nucleus Accumbens Microstructure and Childhood Weight Gain

“…First, although the study motivation and interpretation are based on prior work conducted in animal models of obesity and neuroinflammation [19], the ABCD Study release 3.0 dataset does not include direct markers of neuroinflammation. Recent work has used diffusion-based spectrum imaging (DBSI) to relate imaging markers of striatal neuroinflammation to selfreport emotional eating and obesity in adults [50]. DBSI provides biomarkers of inflammation by characterizing water diffusion properties associated with axon/myelin injury and inflammation [51] and may provide convergent information alongside RSI-based measures of cell density.…”