Habenular connectivity predict weight loss and negative emotional-related eating behavior after laparoscopic sleeve gastrectomy

Author:

Wang Jia12345,Ji Gang67,Li Guanya12345,Hu Yang12345,Zhang Wenchao12345,Ji Weibin12345,Tan Zongxin12345,Li Hao12345,Jiang Fukun12345,Zhang Yaqi12345,Wu Feifei12345,von Deneen Karen M12345,Yu Juan67,Han Yu89,Cui Guangbin89,Manza Peter1011ORCID,Tomasi Dardo1011ORCID,Volkow Nora D1011ORCID,Nie Yongzhan67,Zhang Yi12345ORCID,Wang Gene-Jack1011ORCID

Affiliation:

1. Center for Brain Imaging , , , Xi'an, Shaanxi 710126, China

2. School of Life Science and Technology , , , Xi'an, Shaanxi 710126, China

3. Xidian University & Engineering Research Center of Molecular and Neuro Imaging, Ministry of Education , , , Xi'an, Shaanxi 710126, China

4. International Joint Research Center for Advanced Medical Imaging and Intelligent Diagnosis and Treatment & Xi'an Key Laboratory of Intelligent Sensing and Regulation of trans-Scale Life Information , School of Life Science and Technology, , Xi'an, Shaanxi 710126, China

5. Xidian University , School of Life Science and Technology, , Xi'an, Shaanxi 710126, China

6. State Key Laboratory of Cancer Biology , National Clinical Research Center for Digestive Diseases and Xijing Hospital of Digestive Diseases, , Xi'an, Shaanxi 710032, China

7. Air Force Medical University , National Clinical Research Center for Digestive Diseases and Xijing Hospital of Digestive Diseases, , Xi'an, Shaanxi 710032, China

8. Department of Radiology , Tangdu Hospital, , Xi'an, Shaanxi 710038, China

9. Air Force Medical University , Tangdu Hospital, , Xi'an, Shaanxi 710038, China

10. Laboratory of Neuroimaging , , Bethesda, MD 20892, USA

11. National Institute on Alcohol Abuse and Alcoholism , , Bethesda, MD 20892, USA

Abstract

Abstract Habenular (Hb) processes negative emotions that may drive compulsive food-intake. Its functional changes were reported following laparoscopic-sleeve-gastrectomy (LSG). However, structural connectivity (SC) of Hb-homeostatic/hedonic circuits after LSG remains unclear. We selected regions implicated in homeostatic/hedonic regulation that have anatomical connections with Hb as regions-of-interest (ROIs), and used diffusion-tensor-imaging with probabilistic tractography to calculate SC between Hb and these ROIs in 30 obese participants before LSG (PreLSG) and at 12-month post-LSG (PostLSG12) and 30 normal-weight controls. Three-factor-eating-questionnaire (TFEQ) and Dutch-eating-behavior-questionnaire (DEBQ) were used to assess eating behaviors. LSG significantly decreased weight, negative emotion, and improved self-reported eating behavior. LSG increased SC between the Hb and homeostatic/hedonic regions including hypothalamus (Hy), bilateral superior frontal gyri (SFG), left amygdala (AMY), and orbitofrontal cortex (OFC). TFEQ-hunger negatively correlated with SC of Hb-Hy at PostLSG12; and increased SC of Hb-Hy correlated with reduced depression and DEBQ-external eating. TFEQ-disinhibition negatively correlated with SC of Hb-bilateral SFG at PreLSG. Increased SC of Hb-left AMY correlated with reduced DEBQ-emotional eating. Higher percentage of total weight-loss negatively correlated with SC of Hb-left OFC at PreLSG. Enhanced SC of Hb-homeostatic/hedonic regulatory regions post-LSG may contribute to its beneficial effects in improving eating behaviors including negative emotional eating, and long-term weight-loss.

Funder

National Natural Science Foundation of China

Natural Science Basic Research Program of Shaanxi

National Clinical Research Center for Digestive Diseases

Fundamental Research Funds for the Central Universities

National Institute on Alcoholism and Alcohol Abuse

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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