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Journal of Neurology
Published in: Journal of Neurology 7/2020

01-07-2020 | Obesity | Original Communication

Laparoscopic sleeve gastrectomy improves brain connectivity in obese patients

Authors: Yang Hu, Gang Ji, Guanya Li, Wenchao Zhang, Jia Wang, Ganggang Lv, Yang He, Kai Yuan, Karen M. von Deneen, Antao Chen, Guangbin Cui, Huaning Wang, Peter Manza, Dardo Tomasi, Nora D. Volkow, Yongzhan Nie, Gene-Jack Wang, Yi Zhang

Published in: Journal of Neurology | Issue 7/2020

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Abstract

Objective

Obese individuals have shown functional abnormalities in frontal–limbic regions, and bariatric surgery is an effective treatment for morbid obesity. The aim of the study was to investigate how bariatric surgery modulates brain regional activation and functional connectivity (FC) to food cues, and whether the underlying structural connectivity (SC) alterations contribute to these functional changes as well as behavioral changes.

Methods

A functional magnetic resonance imaging cue-reactivity task with high- (HiCal) and low-calorie (LoCal) food pictures and diffusion tensor imaging (DTI) with deterministic tractography were used to investigate brain reactivity, FC and SC in 28 obese participants tested before and 1 month after laparoscopic sleeve gastrectomy (LSG). Twenty-two obese controls (Ctr) without surgery were also tested at baseline and 1 month later.

Results

LSG significantly decreased right dorsolateral prefrontal cortex (DLPFC) activation to HiCal versus LoCal cues and increased FC between DLPFC and ventral anterior cingulate cortex (vACC), which are regions involved in self-regulation of feeding behaviors. LSG also increased SC between DLPFC and ACC as quantified by fractional anisotropy. Increases in SC and FC between DLPFC and ACC were associated with greater reductions in BMI, and SC changes were positively correlated with FC changes. Increased SC between right DLPFC and ACC mediated the relationship between reduced BMI and increased right DLPFC–vACC FC; likewise, increases in right DLPFC–vACC FC mediated the relationship between increased right DLPFC–ACC SC and reduced BMI.

Conclusion

LSG might induce weight loss in part by increasing SC and FC between DLPFC and ACC, and thus strengthening top-down control over food intake.
Appendix
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Literature
1.
Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J, Alexoff D, Ding YS, Wong C, Ma Y, Pradhan K (2008) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. Neuroimage 42:1537–1543PubMedCrossRef
2.
Tracy AL, Wee CJ, Hazeltine GE, Carter RA (2015) Characterization of attenuated food motivation in high-fat diet-induced obesity: critical roles for time on diet and reinforcer familiarity. Physiol Behav 141:69–77PubMedCrossRef
3.
Bohon C (2014) Greater emotional eating scores associated with reduced frontolimbic activation to palatable taste in adolescents. Obesity (Silver Spring) 22:1814–1820CrossRef
4.
Li G, Ji G, Hu Y, Liu L, Jin Q, Zhang W, Liu L, Wang Y, Zhao J, von Deneen KM, Chen A, Cui G, Han Y, Wang H, Zhao Q, Wu K, Wiers CE, Tomasi D, Leggio L, Volkow ND, Nie Y, Zhang Y, Wang GJ (2019) Reduced plasma ghrelin concentrations are associated with decreased brain reactivity to food cues after laparoscopic sleeve gastrectomy. Psychoneuroendocrinology 100:229–236PubMedCrossRef
5.
Levitan RD, Rivera J, Silveira PP, Steiner M, Gaudreau H, Hamilton J, Kennedy JL, Davis C, Dube L, Fellows L, Wazana A, Matthews S, Meaney MJ (2015) Gender differences in the association between stop-signal reaction times, body mass indices and/or spontaneous food intake in pre-school children: an early model of compromised inhibitory control and obesity. Int J Obes (Lond) 39:614–619CrossRef
6.
Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324:646–648PubMedCrossRef
7.
Killgore WD, Weber M, Schwab ZJ, Kipman M, DelDonno SR, Webb CA, Rauch SL (2013) Cortico-limbic responsiveness to high-calorie food images predicts weight status among women. Int J Obes (Lond) 37:1435–1442CrossRef
8.
Lenard NR, Berthoud HR (2008) Central and peripheral regulation of food intake and physical activity: pathways and genes. Obesity (Silver Spring) 16(Suppl 3):S11–S22CrossRef
9.
Lowe MR, van Steenburgh J, Ochner C, Coletta M (2009) Neural correlates of individual differences related to appetite. Physiol Behav 97:561–571PubMedCrossRef
10.
11.
Pepino MY, Finkbeiner S, Mennella JA (2009) Similarities in food cravings and mood states between obese women and women who smoke tobacco. Obesity (Silver Spring) 17:1158–1163CrossRef
12.
Volkow ND, Wang GJ, Baler RD (2011) Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 15:37–46PubMedCrossRef
13.
Meng Q, Han Y, Ji G, Li G, Hu Y, Liu L, Jin Q, von Deneen KM, Zhao J, Cui G, Wang H, Tomasi D, Volkow ND, Liu J, Nie Y, Zhang Y, Wang GJ (2018) Disrupted topological organization of the frontal-mesolimbic network in obese patients. Brain Imaging Behav 12:1544–1555PubMedCrossRef
14.
Zhang Y, Ji G, Xu M, Cai W, Zhu Q, Qian L, Zhang YE, Yuan K, Liu J, Li Q, Cui G, Wang H, Zhao Q, Wu K, Fan D, Gold MS, Tian J, Tomasi D, Liu Y, Nie Y, Wang GJ (2016) Recovery of brain structural abnormalities in morbidly obese patients after bariatric surgery. Int J Obes (Lond) 40:1558–1565CrossRef
15.
Liu L, Ji G, Li G, Hu Y, Jin Q, Hu C, Zhao J, Meng Q, von Deneen KM, Chen A, Cui G, Wang H, Zhao Q, Wu K, Tian J, Shokri-Kojori E, Tomasi D, Volkow ND, Nie Y, Zhang Y, Wang GJ (2019) Structural changes in brain regions involved in executive-control and self-referential processing after sleeve gastrectomy in obese patients. Brain Imaging Behav 13:830–840PubMedCrossRef
16.
Arterburn D, Gupta A (2018) Comparing the outcomes of sleeve gastrectomy and Roux-en-Y gastric bypass for severe obesity. JAMA 319:235–237PubMedCrossRef
17.
Ochner CN, Stice E, Hutchins E, Afifi L, Geliebter A, Hirsch J, Teixeira J (2012) Relation between changes in neural responsivity and reductions in desire to eat high-calorie foods following gastric bypass surgery. Neuroscience 209:128–135PubMedCrossRef
18.
Ochner CN, Kwok Y, Conceicao E, Pantazatos SP, Puma LM, Carnell S, Teixeira J, Hirsch J, Geliebter A (2011) Selective reduction in neural responses to high calorie foods following gastric bypass surgery. Ann Surg 253:502–507PubMedCrossRef
19.
Frank S, Wilms B, Veit R, Ernst B, Thurnheer M, Kullmann S, Fritsche A, Birbaumer N, Preissl H, Schultes B (2014) Altered brain activity in severely obese women may recover after Roux-en Y gastric bypass surgery. Int J Obes (Lond) 38:341–348CrossRef
20.
Batterink L, Yokum S, Stice E (2010) Body mass correlates inversely with inhibitory control in response to food among adolescent girls: an fMRI study. Neuroimage 52:1696–1703PubMedCrossRef
21.
Adachi Y, Osada T, Sporns O, Watanabe T, Matsui T, Miyamoto K, Miyashita Y (2012) Functional connectivity between anatomically unconnected areas is shaped by collective network-level effects in the macaque cortex. Cereb Cortex 22:1586–1592PubMedCrossRef
22.
Cunningham SI, Tomasi D, Volkow ND (2017) Structural and functional connectivity of the precuneus and thalamus to the default mode network. Hum Brain Mapp 38:938–956PubMedCrossRef
23.
Damoiseaux JS, Greicius MD (2009) Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct Funct 213:525–533PubMedCrossRef
24.
Garcia-Gorro C, de Diego-Balaguer R, Martinez-Horta S, Perez-Perez J, Kulisevsky J, Rodriguez-Dechicha N, Vaquer I, Subira S, Calopa M, Munoz E, Santacruz P, Ruiz-Idiago J, Mareca C, Caballol N, Camara E (2018) Reduced striato-cortical and inhibitory transcallosal connectivity in the motor circuit of Huntington’s disease patients. Hum Brain Mapp 39:54–71PubMedCrossRef
25.
Park HJ, Friston K (2013) Structural and functional brain networks: from connections to cognition. Science 342:1238411PubMedCrossRef
26.
Li G, Ji G, Hu Y, Xu M, Jin Q, Liu L, von Deneen KM, Zhao J, Chen A, Cui G, Wang H, Zhao Q, Wu K, Shokri-Kojori E, Tomasi D, Volkow ND, Nie Y, Zhang Y, Wang GJ (2018) Bariatric surgery in obese patients reduced resting connectivity of brain regions involved with self-referential processing. Hum Brain Mapp 39:4755–4765PubMedPubMedCentralCrossRef
27.
Zhang Y, Ji G, Li G, Hu Y, Liu L, Jin Q, Meng Q, Zhao J, Yuan K, Liu J, von Deneen KM, Chen A, Cui G, Wang H, Zhao Q, Wu K, Tian J, Manza P, Tomasi D, Volkow ND, Nie Y, Wang GJ (2019) Ghrelin reductions following bariatric surgery were associated with decreased resting state activity in the hippocampus. Int J Obes (Lond) 43:842–851CrossRef
28.
29.
30.
Gearhardt AN, Corbin WR, Brownell KD (2009) Preliminary validation of the Yale Food Addiction Scale. Appetite 52:430–436PubMedCrossRef
31.
Clark SM, Saules KK (2013) Validation of the Yale Food Addiction Scale among a weight-loss surgery population. Eat Behav 14:216–219PubMedCrossRef
32.
Bradley M, Lang P (2007) The International Affective Picture System (IAPS) in the study of emotion and attention. In: Coan J, Allen J (eds) Handbook of emotion elicitation and assessment. Oxford University Press, New York, pp 29–46
33.
Stoeckel LE, Weller RE, Cook ER, Twieg DB, Knowlton RC, Cox JE (2008) Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 41:636–647PubMedCrossRef
34.
Contreras-Rodriguez O, Martin-Perez C, Vilar-Lopez R, Verdejo-Garcia A (2017) Ventral and dorsal striatum networks in obesity: link to food craving and weight gain. Biol Psychiatry 81:789–796PubMedCrossRef
35.
Flandin G, Friston KJ (2019) Analysis of family-wise error rates in statistical parametric mapping using random field theory. Hum Brain Mapp 40:2052–2054PubMedCrossRef
36.
37.
Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269PubMedCrossRef
38.
van den Bos W, Rodriguez CA, Schweitzer JB, McClure SM (2015) Adolescent impatience decreases with increased frontostriatal connectivity. Proc Natl Acad Sci USA 112:E3765–E3774PubMedCrossRefPubMedCentral
39.
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289PubMedCrossRef
40.
Uddin LQ, Supekar KS, Ryali S, Menon V (2011) Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. J Neurosci 31:18578–18589PubMedPubMedCentralCrossRef
41.
Jones DK, Cercignani M (2010) Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23:803–820PubMedCrossRef
42.
Lei X, Chen C, Xue F, He Q, Chen C, Liu Q, Moyzis RK, Xue G, Cao Z, Li J, Li H, Zhu B, Liu Y, Hsu AS, Li J, Dong Q (2014) Fiber connectivity between the striatum and cortical and subcortical regions is associated with temperaments in Chinese males. Neuroimage 89:226–234PubMedCrossRef
43.
Tomasi D, Volkow ND (2012) Gender differences in brain functional connectivity density. Hum Brain Mapp 33:849–860PubMedCrossRef
44.
Gong G, He Y, Evans AC (2011) Brain connectivity: gender makes a difference. Neuroscientist 17:575–591PubMedCrossRef
45.
46.
Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, Ochsner KN (2010) Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci USA 107:14811–14816PubMedCrossRefPubMedCentral
47.
Preacher KJ, Hayes AF (2004) SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behav Res Methods Instrum Comput 36:717–731PubMedCrossRef
48.
Lowe CJ, Hall PA, Staines WR (2014) The effects of continuous theta burst stimulation to the left dorsolateral prefrontal cortex on executive function, food cravings, and snack food consumption. Psychosom Med 76:503–511PubMedCrossRef
49.
Lavagnino L, Arnone D, Cao B, Soares JC, Selvaraj S (2016) Inhibitory control in obesity and binge eating disorder: a systematic review and meta-analysis of neurocognitive and neuroimaging studies. Neurosci Biobehav Rev 68:714–726PubMedCrossRef
50.
DelParigi A, Chen K, Salbe AD, Hill JO, Wing RR, Reiman EM, Tataranni PA (2007) Successful dieters have increased neural activity in cortical areas involved in the control of behavior. Int J Obes (Lond) 31:440–448CrossRef
51.
Burger KS, Stice E (2011) Relation of dietary restraint scores to activation of reward-related brain regions in response to food intake, anticipated intake, and food pictures. Neuroimage 55:233–239PubMedCrossRef
52.
Wallis CU, Cardinal RN, Alexander L, Roberts AC, Clarke HF (2017) Opposing roles of primate areas 25 and 32 and their putative rodent homologs in the regulation of negative emotion. Proc Natl Acad Sci USA 114:E4075–E4084PubMedCrossRefPubMedCentral
53.
Riederer JW, Shott ME, Deguzman M, Pryor TL, Frank GK (2016) Understanding neuronal architecture in obesity through analysis of white matter connection strength. Front Hum Neurosci 10:271PubMedPubMedCentralCrossRef
54.
Betzel RF, Byrge L, He Y, Goni J, Zuo XN, Sporns O (2014) Changes in structural and functional connectivity among resting-state networks across the human lifespan. Neuroimage 102(Pt 2):345–357PubMedCrossRef
55.
Kullmann S, Heni M, Veit R, Ketterer C, Schick F, Haring HU, Fritsche A, Preissl H (2012) The obese brain: association of body mass index and insulin sensitivity with resting state network functional connectivity. Hum Brain Mapp 33:1052–1061PubMedCrossRef
56.
Cohen MX, Heller AS, Ranganath C (2005) Functional connectivity with anterior cingulate and orbitofrontal cortices during decision-making. Brain Res Cogn Brain Res 23:61–70PubMedCrossRef
Metadata
Title
Laparoscopic sleeve gastrectomy improves brain connectivity in obese patients
Authors
Yang Hu
Gang Ji
Guanya Li
Wenchao Zhang
Jia Wang
Ganggang Lv
Yang He
Kai Yuan
Karen M. von Deneen
Antao Chen
Guangbin Cui
Huaning Wang
Peter Manza
Dardo Tomasi
Nora D. Volkow
Yongzhan Nie
Gene-Jack Wang
Yi Zhang
Publication date
01-07-2020
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 7/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-09780-w

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