Habenular Connectivity Predict Weight Loss and Negative Emotional-related Eating Behavior After Laparoscopic Sleeve Gastrectomy

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2022 May 17

PMID 35580853

Authors

Jia Wang

Gang Ji

Guanya Li

Yang Hu

Wenchao Zhang

Weibin Ji

Zongxin Tan

Hao Li

Fukun Jiang

Yaqi Zhang

Feifei Wu

Karen M von Deneen

Juan Yu

Yu Han

Guangbin Cui

Peter Manza

Dardo Tomasi

Nora D Volkow

Yongzhan Nie

Yi Zhang

Gene-Jack Wang

Affiliations

Soon will be listed here.

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.

Citing Articles

Medial orbitofrontal cortex structure, function, and cognition associates with weight loss for laparoscopic sleeve gastrectomy.

Li X, Zhang W, Bi Y, Duan Y, Sun X, Chen J Obesity (Silver Spring). 2025; 33(2):308-320.

PMID: 39873400 PMC: 11774012. DOI: 10.1002/oby.24207.

FTO variant is associated with changes in BMI, ghrelin, and brain function following bariatric surgery.

Li G, Hu Y, Zhang W, Wang J, Sun L, Yu J JCI Insight. 2024; 9(17).

PMID: 39088267 PMC: 11385082. DOI: 10.1172/jci.insight.175967.

Obesity is associated with alterations in anatomical connectivity of frontal-corpus callosum.

Hu Y, Li G, Zhang W, Wang J, Ji W, Yu J Cereb Cortex. 2024; 34(2).

PMID: 38300178 PMC: 11486688. DOI: 10.1093/cercor/bhae014.

Presurgical microstructural coherence predicts cognitive change for bariatric surgery patients.

Chen A, Gullett J, Williamson J, Cohen R Obesity (Silver Spring). 2023; 31(9):2325-2334.

PMID: 37605633 PMC: 10449364. DOI: 10.1002/oby.23837.

Brain functional and structural magnetic resonance imaging of obesity and weight loss interventions.

Li G, Hu Y, Zhang W, Wang J, Ji W, Manza P Mol Psychiatry. 2023; 28(4):1466-1479.

PMID: 36918706 PMC: 10208984. DOI: 10.1038/s41380-023-02025-y.

References

Lazaridis I, Tzortzi O, Weglage M, Martin A, Xuan Y, Parent M . A hypothalamus-habenula circuit controls aversion. Mol Psychiatry. 2019; 24(9):1351-1368. PMC: 6756229. DOI: 10.1038/s41380-019-0369-5. View

Yuan K, Yu D, Zhao M, Li M, Wang R, Li Y . Abnormal frontostriatal tracts in young male tobacco smokers. Neuroimage. 2018; 183:346-355. DOI: 10.1016/j.neuroimage.2018.08.046. View

Wang J, Li G, Hu Y, Zhang W, Zhang L, Tan Z . Habenular and mediodorsal thalamic connectivity predict persistent weight loss after laparoscopic sleeve gastrectomy. Obesity (Silver Spring). 2021; 30(1):172-182. DOI: 10.1002/oby.23325. View

Kowski A, Geisler S, Krauss M, Veh R . Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol. 2008; 507(4):1465-78. DOI: 10.1002/cne.21610. View

Liu L, Ji G, Li G, Hu Y, Jin Q, Hu C . Structural changes in brain regions involved in executive-control and self-referential processing after sleeve gastrectomy in obese patients. Brain Imaging Behav. 2018; 13(3):830-840. DOI: 10.1007/s11682-018-9904-2. View

Koob G . Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development. Pharmacol Rev. 2020; 73(1):163-201. PMC: 7770492. DOI: 10.1124/pharmrev.120.000083. View

Stunkard A, Messick S . The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J Psychosom Res. 1985; 29(1):71-83. DOI: 10.1016/0022-3999(85)90010-8. View

Noonan M, Walton M, Behrens T, Sallet J, Buckley M, Rushworth M . Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex. Proc Natl Acad Sci U S A. 2010; 107(47):20547-52. PMC: 2996698. DOI: 10.1073/pnas.1012246107. View

Haber S, Knutson B . The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology. 2009; 35(1):4-26. PMC: 3055449. DOI: 10.1038/npp.2009.129. View

10.

Rudenga K, Sinha R, Small D . Acute stress potentiates brain response to milkshake as a function of body weight and chronic stress. Int J Obes (Lond). 2012; 37(2):309-16. PMC: 3381866. DOI: 10.1038/ijo.2012.39. View

11.

Noonan M, Chau B, Rushworth M, Fellows L . Contrasting Effects of Medial and Lateral Orbitofrontal Cortex Lesions on Credit Assignment and Decision-Making in Humans. J Neurosci. 2017; 37(29):7023-7035. PMC: 6705719. DOI: 10.1523/JNEUROSCI.0692-17.2017. View

12.

Bao A, Swaab D . The human hypothalamus in mood disorders: The HPA axis in the center. IBRO Rep. 2019; 6:45-53. PMC: 6562194. DOI: 10.1016/j.ibror.2018.11.008. View

13.

Hikosaka O . The habenula: from stress evasion to value-based decision-making. Nat Rev Neurosci. 2010; 11(7):503-13. PMC: 3447364. DOI: 10.1038/nrn2866. View

14.

Maldonado M, Molfese D, Viswanath H, Curtis K, Jones A, Hayes T . The habenula as a novel link between the homeostatic and hedonic pathways in cancer-associated weight loss: a pilot study. J Cachexia Sarcopenia Muscle. 2018; 9(3):497-504. PMC: 5989751. DOI: 10.1002/jcsm.12286. View

15.

Tiedemann L, Alink A, Beck J, Buchel C, Brassen S . Valence Encoding Signals in the Human Amygdala and the Willingness to Eat. J Neurosci. 2020; 40(27):5264-5272. PMC: 7329310. DOI: 10.1523/JNEUROSCI.2382-19.2020. View

16.

Batalla A, Homberg J, Lipina T, Sescousse G, Luijten M, Ivanova S . The role of the habenula in the transition from reward to misery in substance use and mood disorders. Neurosci Biobehav Rev. 2017; 80:276-285. DOI: 10.1016/j.neubiorev.2017.03.019. View

17.

Zhang Y, Ji G, Xu M, Cai W, Zhu Q, Qian L . Recovery of brain structural abnormalities in morbidly obese patients after bariatric surgery. Int J Obes (Lond). 2016; 40(10):1558-1565. DOI: 10.1038/ijo.2016.98. View

18.

Loonen A, Ivanova S . Circuits Regulating Pleasure and Happiness: The Evolution of the Amygdalar-Hippocampal-Habenular Connectivity in Vertebrates. Front Neurosci. 2016; 10:539. PMC: 5118621. DOI: 10.3389/fnins.2016.00539. View

19.

Leong J, Pestilli F, Wu C, Samanez-Larkin G, Knutson B . White-Matter Tract Connecting Anterior Insula to Nucleus Accumbens Correlates with Reduced Preference for Positively Skewed Gambles. Neuron. 2016; 89(1):63-9. PMC: 4720154. DOI: 10.1016/j.neuron.2015.12.015. View

20.

Volkow N, Wang G, Tomasi D, Baler R . Obesity and addiction: neurobiological overlaps. Obes Rev. 2012; 14(1):2-18. PMC: 4827343. DOI: 10.1111/j.1467-789X.2012.01031.x. View