The brain has a central role in regulating ingestive behavior in obesity. Analogous to addiction behaviors, an imbalance in the processing of rewarding and salient stimuli results in maladaptive eating behaviors that override homeostatic needs. We performed network analysis based on graph theory to examine the association between body mass index (BMI) and network measures of integrity, information flow and global communication (centrality) in reward, salience and sensorimotor regions and to identify sex-related differences in these parameters.
Structural and diffusion tensor imaging were obtained in a sample of 124 individuals (61 males and 63 females). Graph theory was applied to calculate anatomical network properties (centrality) for regions of the reward, salience and sensorimotor networks. General linear models with linear contrasts were performed to test for BMI and sex-related differences in measures of centrality, while controlling for age.
In both males and females, individuals with high BMI (obese and overweight) had greater anatomical centrality (greater connectivity) of reward (putamen) and salience (anterior insula) network regions. Sex differences were observed both in individuals with normal and elevated BMI. In individuals with high BMI, females compared to males showed greater centrality in reward (amygdala, hippocampus and nucleus accumbens) and salience (anterior mid-cingulate cortex) regions, while males compared to females had greater centrality in reward (putamen) and sensorimotor (posterior insula) regions.
In individuals with increased BMI, reward, salience and sensorimotor network regions are susceptible to topological restructuring in a sex-related manner. These findings highlight the influence of these regions on integrative processing of food-related stimuli and increased ingestive behavior in obesity, or in the influence of hedonic ingestion on brain topological restructuring. The observed sex differences emphasize the importance of considering sex differences in obesity pathophysiology.
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This research was supported by grants from the National Institutes of Health including K23 DK106528 (AG), R01 DK048351 (EAM), P50 DK064539 (EAM), P30 DK041301, R01 AT007137 (KT), R03 DK084169 (JSL), and pilot funds were provided for brain scanning by the Ahmanson-Lovelace Brain Mapping Center.
Study concept and design, analysis and interpretation of the data, drafting and revision of manuscript were done by AG. Drafting and critical review of manuscript, approval of final version of the manuscript, interpretation of the data and study funding were done by EM. Generation of the data and data analysis were done by KH. Analysis of the data was done by RB, CF, MA, CT, CA-M and JDVH. BN and KT reviewed the manuscript and did the study funding. CPS drafted and critically reviewed the manuscript. JSL helped with the study concept and design, analyzed the data, drafted and revised the manuscript, approved the final version of the manuscript.
The authors declare no conflict of interest.
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Gupta, A., Mayer, E., Hamadani, K. et al. Sex differences in the influence of body mass index on anatomical architecture of brain networks. Int J Obes 41, 1185–1195 (2017). https://doi.org/10.1038/ijo.2017.86
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