Original Research

Integration of Neural Reward Processing and Appetite-Related Signaling in Obese Females: Evidence From Resting-State fMRI

Peng Zhang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Yang Liu MD

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

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Han Lv MD,

Han Lv MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Meng-yi Li MD,

Meng-yi Li MD

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

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Feng-xia Yu MD,

Feng-xia Yu MD

Medical Imaging Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China

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Zheng Wang MD,

Zheng Wang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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He-yu Ding MD,

He-yu Ding MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Li-xue Wang BS,

Li-xue Wang BS

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

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Kai-xin Zhao BS,

Kai-xin Zhao BS

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

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Zheng-yu Zhang MD,

Zheng-yu Zhang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Peng-fei Zhao MD,

Peng-fei Zhao MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Jing Li MD,

Jing Li MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Zheng-han Yang MD,

Zheng-han Yang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Zhong-tao Zhang MD,

Corresponding Author

Zhong-tao Zhang MD

[email protected]

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

Address reprint requests to: Z.-c.W., Department of Radiology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yong An Road, Xicheng District, Beijing, 100050, China. E-mail: [email protected] or Z.-t.Z., Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, No. 95 Yong An Road, Xicheng District, Beijing, 100050, China. E-mail: [email protected]Search for more papers by this author

Zhen-chang Wang MD,

Corresponding Author

Zhen-chang Wang MD

[email protected]

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Peng Zhang MD,

Peng Zhang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Yang Liu MD,

Yang Liu MD

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

Search for more papers by this author

Han Lv MD,

Han Lv MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Meng-yi Li MD,

Meng-yi Li MD

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

Search for more papers by this author

Feng-xia Yu MD,

Feng-xia Yu MD

Medical Imaging Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Zheng Wang MD,

Zheng Wang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

He-yu Ding MD,

He-yu Ding MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Li-xue Wang BS,

Li-xue Wang BS

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

Search for more papers by this author

Kai-xin Zhao BS,

Kai-xin Zhao BS

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

Search for more papers by this author

Zheng-yu Zhang MD,

Zheng-yu Zhang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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Peng-fei Zhao MD,

Peng-fei Zhao MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Jing Li MD,

Jing Li MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Zheng-han Yang MD,

Zheng-han Yang MD

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

Search for more papers by this author

Zhong-tao Zhang MD,

Corresponding Author

Zhong-tao Zhang MD

[email protected]

Department of General Surgery, Beijing Friendship Hospital, Capital Medical University & National Clinical Research Center for Digestive Diseases, Beijing, China

Zhen-chang Wang MD,

Corresponding Author

Zhen-chang Wang MD

[email protected]

Department of Radiology, Beijing Friendship Hospital, Capital Medical University, Beijing, China

First published: 17 January 2019

https://doi.org/10.1002/jmri.26576

Citations: 21

The first two authors contributed equally to this work.

Contract grant sponsor: National Natural Science Foundation of China; Contract grant numbers: 61527807, 81701644, 61801311; Contract grant sponsor: Beijing Municipal Administration of Hospital' Mission Plan; Contract grant number: SML20150101; Beijing Scholars Program; Contract grant number: [2015] 160; Contract grant sponsor: Beijing Natural Science Foundation; Contract grant numbers: 7172064; 7162048; 7182044; Contract grant sponsor: Beijing Municipal Administration of Hospitals (to Han Lv); Contract grant numbers: PX2018001, QML20180103; Contract grant sponsor: Beijing Friendship Hospital, Capital Medical University; Contract grant number: seed project YYZZ2017B01 (to Han Lv).

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Abstract

Background

The reward-related regions have been considered a crucial component in the regulation of eating behavior. Furthermore, appetite-related regions associated with reward can influence eating behaviors through altered functional activity related to food in brain areas associated with emotion, memory, sensory processing, motor function, and cognitive control.

Purpose

To investigate the key nodes in obese females of reward-related regions and, based on key nodes, to evaluate the directionality of functional connectivity between key nodes and appetite-related regions.

Study Type

Prospective.

Population

Twenty-eight obese and 28 normal-weight female controls of similar age.

Field Strength/Sequence

3.0 T MRI and echo planar imaging (EPI) sequence, 3D BRAVO sequence.

Assessment

The fMRI data preprocessing was based on the Data Processing & Analysis of Brain Imaging and Statistical Parametric Mapping 12. Degree centrality calculation was based on the GRETNA toolkit and granger causality analysis were based on the DynamicBC toolbox.

Statistical Tests: Independent two-sample t-tests were used to assess the differences in demographic and clinical data between two groups. Two-sample t-tests were conducted to test the difference in degree centrality and effective connectivity of key nodes between two groups.

Results

Compared with normal-weight controls, obese females showed an increased degree centrality in the left ventral striatum/caudate (t = 2.96808, P < 0.05) and decreased degree centrality in right orbitofrontal cortex (OFC) (t = –3.3558, P < 0.05). The obese females showed directional effective connectivity between left ventral striatum/caudate and several regions (left inferior temporal gyrus, fusiform gyrus, postcentral gyrus, and right precentral gyrus) (P < 0.05). Directional effective connectivity was also observed between the right OFC and several regions (left middle temporal gyrus, cuneus, OFC, superior temporal gyrus, middle frontal gyrus, and right inferior parietal lobule) (P < 0.05).

Data Conclusion

The left ventral striatum/caudate and right OFC are key nodes in reward-related regions. The key nodes with reward processing mainly enhance visual processing of information and further participate in cognitive, attention, and sensorimotor processing.

Level of Evidence: 1.

Technical Efficacy: Stage 4.

J. Magn. Reson. Imaging 2019;50:541–551.

References

1Ng M, Fleming T, Robinson M, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384: 766–781.
10.1016/S0140-6736(14)60460-8
PubMed Web of Science® Google Scholar
2Simon JJ, Wetzel A, Sinno MH, et al. Integration of homeostatic signaling and food reward processing in the human brain. JCI Insight 2017; 2: 92970.
10.1172/jci.insight.92970
PubMed Web of Science® Google Scholar
3Berridge KC. Food reward: Brain substrates of wanting and liking. Neurosci Biobehav Rev 1996; 20: 1–25.
10.1016/0149-7634(95)00033-B
CAS PubMed Web of Science® Google Scholar
4García-García I, Horstmann A, Jurado MA, et al. Reward processing in obesity, substance addiction and non-substance addiction. Obes Rev 2014; 15: 853–869.
10.1111/obr.12221
CAS PubMed Web of Science® Google Scholar
5Bartholdy S, Dalton B, O'Daly OG, Campbell IC, Schmidt U. A systematic review of the relationship between eating, weight and inhibitory control using the stop signal task. Neurosci Biobehav Rev 2016; 64: 35–62.
10.1016/j.neubiorev.2016.02.010
PubMed Web of Science® Google Scholar
6Berridge KC, Ho CY, Richard JM, DiFeliceantonio AG. The tempted brain eats: Pleasure and desire circuits in obesity and eating disorders. Brain Res 2010; 2: 43–64.
10.1016/j.brainres.2010.04.003
Web of Science® Google Scholar
7Rubinov M, Sporns O. Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 2010; 52: 1059–1069.
10.1016/j.neuroimage.2009.10.003
PubMed Web of Science® Google Scholar
8Feldstein Ewing SW, Claus ED, Hudson KA, et al. Overweight adolescents' brain response to sweetened beverages mirrors addiction pathways. Brain Imaging Behav 2017; 11: 925–935.
10.1007/s11682-016-9564-z
PubMed Web of Science® Google Scholar
9Volkow ND, Wang GJ, Tomasi D, Baler RD. Obesity and addiction: Neurobiological overlaps. Obes Rev 2013; 14: 2–18.
10.1111/j.1467-789X.2012.01031.x
CAS PubMed Web of Science® Google Scholar
10Volkow ND, Wang GJ, Baler RD. Reward, dopamine and the control of food intake: Implications for obesity. Trends Cogn Sci 2011; 15: 37–46.
10.1016/j.tics.2010.11.001
CAS PubMed Web of Science® Google Scholar
11Burger KS, Stice E. Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt. Am J Clin Nutr 2013; 97: 1188–1194.
10.3945/ajcn.112.055285
CAS PubMed Web of Science® Google Scholar
12Rolls ET. Sensory processing in the brain related to the control of food intake. Proc Nutr Soc 2007; 66: 96–112.
10.1017/S0029665107005332
PubMed Web of Science® Google Scholar
13Doornweerd S, van Duinkerken E, de Geus EJ, Arbab-Zadeh P, Veltman DJ, IJzerman RG. Overweight is associated with lower resting state functional connectivity in females after eliminating genetic effects: A twin study. Hum Brain Mapp 2017; 38: 5069–5081.
10.1002/hbm.23715
PubMed Web of Science® Google Scholar
14García-García I, Jurado MÁ, Garolera M, et al. Alterations of the salience network in obesity: A resting-state fMRI study. Hum Brain Mapp 2013; 34: 2786–2797.
10.1002/hbm.22104
PubMed Web of Science® Google Scholar
15Carnell S, Gibson C, Benson L, Ochner CN, Geliebter A. Neuroimaging and obesity: Current knowledge and future directions. Obes Rev 2012; 13: 43–56.
10.1111/j.1467-789X.2011.00927.x
CAS PubMed Web of Science® Google Scholar
16van Bloemendaal L, Veltman DJ, Ten Kulve JS, et al. Brain reward-system activation in response to anticipation and consumption of palatable food is altered by glucagon-like peptide-1 receptor activation in humans. Diabetes Obes Metab 2015; 17: 878–886.
10.1111/dom.12506
CAS PubMed Web of Science® Google Scholar
17Hogenkamp PS, Zhou W, Dahlberg LS, et al. Higher resting-state activity in reward-related brain circuits in obese versus normal-weight females independent of food intake. Int J Obes 2016; 40: 1687–1692.
10.1038/ijo.2016.105
CAS PubMed Web of Science® Google Scholar
18Wu GR, Liao W, Stramaglia S, Ding JR, Chen H, Marinazzo D. A blind deconvolution approach to recover effective connectivity brain networks from resting state fMRI data. Med Image Anal 2013; 17: 365–374.
10.1016/j.media.2013.01.003
PubMed Web of Science® Google Scholar
19Gupta A, Mayer EA, Hamadani K, et al. Sex differences in the influence of body mass index on anatomical architecture of brain networks. Int J Obes 2017; 41: 1185–1195.
10.1038/ijo.2017.86
CAS PubMed Web of Science® Google Scholar
20Lee DT, Yip WC, Chen Y, Meng Q, Kleinman A. Ethno-psychometric evaluation of the General Health Questionnaire in rural China. Psychol Med 2006; 36: 249–255.
10.1017/S0033291705006434
PubMed Web of Science® Google Scholar
21van Strien T, Frijters JE, Bergers GP, et al. Dutch eating behavior questionnaire for assessment of restrained, emotional and external eating behaviour. Int J Eat Disord 1986; 5: 21.
Web of Science® Google Scholar
22Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics 2016; 14: 339–351.
10.1007/s12021-016-9299-4
PubMed Web of Science® Google Scholar
23Power JD, Cohen AL, Nelson SM, et al. Functional network organization of the human brain. Neuron 2011; 72: 665–678.
10.1016/j.neuron.2011.09.006
CAS PubMed Web of Science® Google Scholar
24Power JD, Schlaggar BL, Lessov-Schlaggar CN, Petersen SE. Evidence for hubs in human functional brain networks. Neuron 2013; 79: 798–813.
10.1016/j.neuron.2013.07.035
CAS PubMed Web of Science® Google Scholar
25Coveleskie K, Gupta A, Kilpatrick LA, et al. Altered functional connectivity within the central reward network in overweight and obese women. Nutr Diabetes 2015; 19: 148–155.
10.1038/nutd.2014.45
Web of Science® Google Scholar
26Zhang Y, Zhang S, Ide JS, et al. Dynamic network dysfunction in cocaine dependence: Graph theoretical metrics and stop signal reaction time. Neuroimage Clin 2018; 18: 793–801.
10.1016/j.nicl.2018.03.016
PubMed Web of Science® Google Scholar
27Wang J, Wang X, Xia M, Liao X, Evans A, He Y. GRETNA: A graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci 2015; 9: 386.
CAS PubMed Web of Science® Google Scholar
28Li S, Ma X, Huang R, et al. Abnormal degree centrality in neurologically asymptomatic patients with end-stage renal disease: A resting-state fMRI study. Clin Neurophysiol 2016; 127: 602–609.
10.1016/j.clinph.2015.06.022
PubMed Web of Science® Google Scholar
29Liao W, Wu GR, Xu Q, et al. DynamicBC: A MATLAB toolbox for dynamic brain connectome analysis. Brain Connect 2014; 4: 780–790.
10.1089/brain.2014.0253
PubMed Google Scholar
30Zang ZX, Yan CG, Dong ZY, Huang J, Zang YF. Granger causality analysis implementation on MATLAB: A graphic user interface toolkit for fMRI data processing. J Neurosci Methods 2012; 203: 418–426.
10.1016/j.jneumeth.2011.10.006
PubMed Web of Science® Google Scholar
31Stice E, Spoor S, Bohon C, Small DM. Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008; 322: 449–452.
10.1126/science.1161550
CAS PubMed Web of Science® Google Scholar
32Kringelbach ML. The human orbitofrontal cortex: Linking reward to hedonic experience. Nat Rev Neurosci 2005; 6: 691–702.
10.1038/nrn1747
CAS PubMed Web of Science® Google Scholar
33Seeley WW, Menon V, Schatzberg AF, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007; 27: 2349–2356.
10.1523/JNEUROSCI.5587-06.2007
CAS PubMed Web of Science® Google Scholar
34Simon JJ, Becker A, Sinno MH, et al. Neural food reward processing in successful and unsuccessful weight maintenance. Obesity 2018; 26: 895–902.
10.1002/oby.22165
PubMed Web of Science® Google Scholar
35Koch K, Wagner G, Schachtzabel C, et al. Association between white matter fiber structure and reward-related reactivity of the ventral striatum. Hum Brain Mapp 2014; 35: 1469–1476.
10.1002/hbm.22284
CAS PubMed Web of Science® Google Scholar
36Rosenbaum M, Sy M, Pavlovich K, Leibel RL, Hirsch J. Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Invest 2008; 118: 2583–2591.
CAS PubMed Web of Science® Google Scholar
37Moreno-Lopez L, Contreras-Rodriguez O, Soriano-Mas C, Stamatakis EA, Verdejo-Garcia A. Disrupted functional connectivity in adolescent obesity. Neuroimage Clin 2016; 12: 262–268.
10.1016/j.nicl.2016.07.005
PubMed Web of Science® Google Scholar
38Gearhardt AN, Yokum S, Stice E, Harris JL, Brownell KD. Relation of obesity to neural activation in response to food commercials. Soc Cogn Affect Neurosci 2014; 9: 932–938.
10.1093/scan/nst059
PubMed Web of Science® Google Scholar
39Geliebter A, Pantazatos SP, McOuatt H, Puma L, Gibson CD, Atalayer D. Sex-based fMRI differences in obese humans in response to high vs. low energy food cues. Behav Brain Res 2013; 243: 91–96.
10.1016/j.bbr.2012.12.023
PubMed Web of Science® Google Scholar
40Dien J. A tale of two recognition systems: Implications of the fusiform face area and the visual word form area for lateralized object recognition models. Neuropsychologia 2009; 47: 1–16.
10.1016/j.neuropsychologia.2008.08.024
PubMed Web of Science® Google Scholar
41Holsen LM, Zarcone JR, Thompson TI, et al. Neural mechanisms underlying food motivation in children and adolescents. Neuroimage 2005; 27: 669–676.
10.1016/j.neuroimage.2005.04.043
PubMed Web of Science® Google Scholar
42Conway BR. The organization and operation of inferior temporal cortex. Annu Rev Vis Sci 2018; 4: 381–402.
10.1146/annurev-vision-091517-034202
PubMed Web of Science® Google Scholar
43Gupta A, Mayer EA, Sanmiguel CP, et al. Patterns of brain structural connectivity differentiate normal weight from overweight subjects. Neuroimage Clin 2015; 13: 506–517.
10.1016/j.nicl.2015.01.005
Web of Science® Google Scholar

Citing Literature

Volume50, Issue2

August 2019

Pages 541-551

Integration of Neural Reward Processing and Appetite-Related Signaling in Obese Females: Evidence From Resting-State fMRI

Abstract

Background

Purpose

Study Type

Population

Field Strength/Sequence

Assessment

Results

Data Conclusion

References

Citing Literature

References

Information

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