Hostname: page-component-745bb68f8f-d8cs5 Total loading time: 0 Render date: 2025-01-23T09:30:33.281Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional and effective connectivity between reward and inhibitory control networks underlying subclinical binge eating

Published online by Cambridge University Press:  21 January 2025

Ximei Chen ,
Wei Li ,
Yijun Luo ,
Yong Liu ,
Xiaofei Xu ,
Xiao Gao  and
Hong Chen Open the ORCID record for Hong Chen [Opens in a new window]
Ximei Chen
Affiliation:
Key Laboratory of Cognition and Personality, Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, China
Wei Li
Affiliation:
Key Laboratory of Cognition and Personality, Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, China
Yijun Luo
Affiliation:
Key Laboratory of Cognition and Personality, Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, China
Yong Liu
Affiliation:
Key Laboratory of Cognition and Personality, Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, China
Xiaofei Xu
Affiliation:
School of Computing Technologies, RMIT University, Melbourne, Australia
Xiao Gao
Affiliation:
Key Laboratory of Cognition and Personality, Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, China
Hong Chen*
Affiliation:
Key Laboratory of Cognition and Personality, Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, China Research Center of Psychology and Social Development, Faculty of Psychology, Southwest University, Chongqing, China
*
Correspondence: Hong Chen. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Knowledge is growing on the essential role of neural circuits involved in aberrant cognitive control and reward sensitivity for the onset and maintenance of binge eating.

Aims

To investigate how the brain's reward (bottom-up) and inhibition control (top-down) systems potentially and dynamically interact to contribute to subclinical binge eating.

Method

Functional magnetic resonance imaging data were acquired from 30 binge eaters and 29 controls while participants performed a food reward Go/NoGo task. Dynamic causal modelling with the parametric empirical Bayes framework, a novel brain connectivity technique, was used to examine between-group differences in the directional influence between reward and executive control regions. We explored the proximal risk factors for binge eating and its neural basis, and assessed the predictive ability of neural indices on future disordered eating and body weight.

Results

The binge eating group relative to controls displayed fewer reward-inhibition undirectional and directional synchronisations (i.e. medial orbitofrontal cortex [mOFC]–superior parietal gyrus [SPG] connectivity, mOFC → SPG excitatory connectivity) during food reward_nogo condition. Trait impulsivity is a key proximal factor that could weaken the mOFC–SPG connectivity and exacerbate binge eating. Crucially, this core mOFC–SPG connectivity successfully predicted binge eating frequency 6 months later.

Conclusions

These findings point to a particularly important role of the bottom-up interactions between cortical reward and frontoparietal control circuits in subclinical binge eating, which offers novel insights into the neural hierarchical mechanisms underlying problematic eating, and may have implications for the early identification of individuals suffering from strong binge eating-associated symptomatology in the general population.

Keywords

Binge eatingreward sensitivityinhibitory controldynamic causal modellingfunctional magnetic resonance imaging
Type
Original Article
Information
The British Journal of Psychiatry , First View , pp. 1 - 14
Check for updates
Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press on behalf of Royal College of Psychiatrists.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Deloitte Access Economics. The Social and Economic Cost of Eating Disorders in the United States of America: A Report for the Strategic Training Initiative for the Prevention of Eating Disorders and the Academy for Eating Disorders. Deloitte Access Economics, 2020 (https://www.hsph.harvard.edu/striped/report-economic-costs-of-eating-disorders/).Google Scholar
Santomauro, DF, Melen, S, Mitchison, D, Vos, T, Whiteford, H, Ferrari, AJ. The hidden burden of eating disorders: an extension of estimates from the global burden of disease study 2019. Lancet 2021; 8(4): 320.Google ScholarPubMed
Tong, J, Miao, S, Wang, J, Yang, F, Lai, H, Zhang, C, et al. A two-stage epidemiologic study on prevalence of eating disorders in female university students in Wuhan, China. Soc Psychiatry Psychiatr Epidemiol 2014; 49(3): 499–505.CrossRefGoogle ScholarPubMed
Goldschmidt, AB, Wall, MM, Loth, KA, Neumark-Sztainer, D. Risk factors fordisordered eating in overweight adolescents and young adults. J Pediatr Psychol 2015; 40(10): 1048–55.CrossRefGoogle ScholarPubMed
Sparti, C, Santomauro, D, Cruwys, T, Burgess, P, Harris, M. Disordered eating among Australian adolescents: prevalence, functioning, and help received. Int J Eat Disord 2019; 52(3): 246–54.CrossRefGoogle ScholarPubMed
Tanofsky-Kraff, M, Schvey, NA, Grilo, CM. A developmental framework of binge-eating disorder based on pediatric loss of control eating. Am Psychol 2020; 75(2): 189–203.CrossRefGoogle ScholarPubMed
Stice, E, Yokum, S. Neural vulnerability factors that increase risk for future weight gain. Psychol Bull 2016; 142(5): 447–71.CrossRefGoogle ScholarPubMed
Wu, M, Brockmeyer, T, Hartmann, M, Skunde, M, Herzog, W, Friederich, HC. Reward-related decision making in eating and weight disorders: a systematic review and meta-analysis of the evidence from neuropsychological studies. Neurosci Biobehav Rev 2016; 61: 177–96.CrossRefGoogle ScholarPubMed
Bodell, LP, Wildes, JE, Goldschmidt, AB, Lepage, R, Keenan, KE, Guyer, AE, et al. Associations between neural reward processing and binge eating among adolescent girls. J Adolesc Health 2018; 62(1): 107–13.CrossRefGoogle ScholarPubMed
Monteleone, AM, Castellini, G, Volpe, U, Ricca, V, Lelli, L, Monteleone, P, et al. Neuroendocrinology and brain imaging of reward in eating disorders: a possible key to the treatment of anorexia nervosa and bulimia nervosa. Prog Neuro-Psychopharmacol Biol Psychiatry 2018; 80(Pt B): 132–42.CrossRefGoogle Scholar
Bartholdy, S, O'Daly, OG, Campbell, IC, Banaschewski, T, Barker, G, Bokde, A, Neural correlates of failed inhibitory control as an early marker of disordered dating in adolescents. Biol Psychiatry 2019; 85(11): 956–65.CrossRefGoogle Scholar
Oliva, R, Morys, F, Horstmann, A, Castiello, U, Begliomini, C. The impulsive brain: neural underpinnings of binge eating behavior in normal-weight adults. Appetite 2019; 136: 33–49.CrossRefGoogle ScholarPubMed
Stice, E, Burger, K. Neural vulnerability factors for obesity. Clin Psychol Rev 2019; 68: 38–53.CrossRefGoogle ScholarPubMed
Sutton, CA, L'Insalata, AM, Fazzino, TL. Reward sensitivity, eating behavior, and obesity-related outcomes: a systematic review. Physiol Behav 2022; 252: 113843.CrossRefGoogle ScholarPubMed
Schmidt, R, Wandrer, H, Boutelle, KN, Kiess, W, Hilbert, A. Associations between eating in the absence of hunger and executive functions in adolescents with binge-eating disorder: an experimental study. Appetite 2023; 186: 106573.CrossRefGoogle ScholarPubMed
Vrieze, E, Leenaerts, N. Neuronal activity and reward processing in relation to binge eating. Curr Opin Psychiatry 2023; 36(6): 443–8.CrossRefGoogle ScholarPubMed
Forester, G, Schaefer, LM, Johnson, JS, Amponsah, T, Dvorak, RD, Wonderlich, SA. Neurocognitive reward processes measured via event-related potentials are associated with binge-eating disorder diagnosis and ecologically-assessed behavior. Appetite 2024; 193: 107151.CrossRefGoogle ScholarPubMed
Murray, SB, Zhang, R, Duval, CJ, Nagata, JM, Jann, K. Task-evoked neural activity during reward anticipation and inhibitory control in preadolescent binge eating disorder. J Adolesc Health 2024; 74(5): 958–63.CrossRefGoogle ScholarPubMed
Chen, X, Dong, D, Zhou, F, Gao, X, Liu, Y, Wang, J, et al. Connectome-based prediction of eating disorder-associated symptomatology. Psychol Med 2023; 53(12): 5786–99.CrossRefGoogle ScholarPubMed
Chen, X, Li, W, Liu, Y, Xiao, M, Chen, H. Altered effective connectivity between reward and inhibitory control networks in people with binge eating episodes: a spectral dynamic causal modeling study. Appetite 2023; 188: 106763.CrossRefGoogle ScholarPubMed
Li, W, Chen, X, Luo, Y, Luo, L, Chen, H. Orbitofrontal neural dissociation of healthy and unhealthy food reward sensitivity in normal-weight binge eaters. Psychiatry Res 2022; 316: 114736.CrossRefGoogle ScholarPubMed
Lowe, CJ, Morton, JB, Reichelt, AC. Adolescent obesity and dietary decision making–a brain-health perspective. Lancet Child Adolesc Health 2020; 4(5): 388–96.CrossRefGoogle ScholarPubMed
Oliva, R, Morys, F, Horstmann, A, Castiello, U, Begliomini, C. Characterizing impulsivity and resting-state functional connectivity in normal-weight binge eaters. Int J Eat Disord 2020; 53(3): 478–88.CrossRefGoogle ScholarPubMed
Chen, X, Gao, X, Qin, J, Wang, C, Xiao, M, Tian, Y, et al. Resting-state functional network connectivity underlying eating disorder symptoms in healthy young adults. NeuroImage 2021; 30: 102671.CrossRefGoogle ScholarPubMed
Li, W, Chen, X, Luo, Y, Xiao, M, Liu, Y, Chen, H. Altered connectivity patterns of medial and lateral orbitofrontal cortex underlie the severity of bulimic symptoms. Int J Clin Health Psychol 2024; 24(1): 100439.CrossRefGoogle ScholarPubMed
Friston, KJ, Harrison, L, Penny, W. Dynamic causal modeling. NeuroImage 2003; 19: 1273–302.CrossRefGoogle Scholar
Friston, KJ, Litvak, V, Oswal, A, Razi, A, Stephan, KE, Van Wijk, BC, et al. Bayesian model reduction and empirical Bayes for group (DCM) studies. NeuroImage 2016; 128: 413–31.CrossRefGoogle Scholar
Friston, KJ, Preller, KH, Mathys, C, Cagnan, H, Heinzle, J, Razi, A, et al. Dynamic causal modelling revisited. NeuroImage 2019; 199: 730–44.CrossRefGoogle ScholarPubMed
Zeidman, P, Jafarian, A, Corbin, N, Seghier, ML, Razi, A, Price, CJ, et al. A guide to group effective connectivity analysis, part 1: first level analysis with DCM for fMRI. NeuroImage 2019; 200: 174–90.CrossRefGoogle ScholarPubMed
Zeidman, P, Jafarian, A, Seghier, ML, Litvak, V, Cagnan, H, Price, CJ, et al. A guide to group effective connectivity analysis, part 2: second level analysis with PEB. NeuroImage 2019; 200: 12–25.CrossRefGoogle ScholarPubMed
Friston, KJ, Penny, W. Posterior probability maps and SPMs. NeuroImage 2003; 19(3): 1240–9.CrossRefGoogle ScholarPubMed
Labonté, K, Nielsen, DE. Measuring food-related inhibition with go/no-go tasks: critical considerations for experimental design. Appetite 2023; 185: 106497.CrossRefGoogle ScholarPubMed
Gormally, J, Black, S, Daston, S, Rardin, D. The assessment of binge eating severity among obese persons. Addict Behav 1982; 7(1): 47–55.CrossRefGoogle ScholarPubMed
Li, X, Pan, Y, Han, Y, Liang, Q, Yang, X, Meng, X, et al. Chinese food image database for eating and appetite studies. Nutrients 2022; 14(14): 2916.CrossRefGoogle ScholarPubMed
Gholamipourbarogh, N, Ghin, F, Mückschel, M, Frings, C, Stock, AK, Beste, C. Evidence for independent representational contents in inhibitory control subprocesses associated with frontoparietal cortices. Hum Brain Mapp 2023; 44(3): 1046–61.CrossRefGoogle ScholarPubMed
Tozzi, L, Goldstein-Piekarski, AN, Korgaonkar, MS, Williams, LM. Connectivity of the cognitive control network during response inhibition as a predictive and response biomarker in major depression: evidence from a randomized clinical trial. Biol Psychiatry 2020; 87(5): 462–72.CrossRefGoogle ScholarPubMed
Li, G, Liu, Y, Zheng, Y, Li, D, Liang, X, Chen, Y, et al. Large-scale dynamic causal modeling of major depressive disorder based on resting-state functional magnetic resonance imaging. Hum Brain Mapp 2020; 41(4): 865–81.CrossRefGoogle ScholarPubMed
Koussis, NC, Burgher, B, Jeganathan, J, Scott, JG, Cocchi, L, Breakspear, M. Cognitive control system gates insula processing of affective stimuli in early psychosis. Schizophr Bull 2023; 49(4): 987–96.CrossRefGoogle ScholarPubMed
Kass, RE, Raftery, AE. Bayes factors. J Am Stat Assoc 1995; 90(430): 773–95.CrossRefGoogle Scholar
Haynos, AF, Camchong, J, Pearson, CM, Lavender, JM, Mueller, BA, Peterson, CB, et al. Resting state hypoconnectivity of reward networks in binge eating disorder. Cereb Cortex 2021; 31(5): 2494–504.CrossRefGoogle ScholarPubMed
Murray, SB, Alba, C, Duval, CJ, Nagata, JM, Cabeen, RP, Lee, DJ, et al. Aberrant functional connectivity between reward and inhibitory control networks in pre-adolescent binge eating disorder. Psychol Med 2023; 53(9): 3869–78.Google ScholarPubMed
Zhang, Z, Bo, Q, Li, F, Zhao, L, Wang, Y, Liu, R, et al. Altered effective connectivity among core brain networks in patients with bipolar disorder. J Psychiatr Res 2022; 152: 296–304.CrossRefGoogle ScholarPubMed
Fitzsimmons-Craft, EE, Bardone-Cone, AM, Brownstone, LM, Harney, MB. Evaluating the roles of anxiety and dimensions of perfectionism in dieting and binge eating using weekly diary methodology. Eat Behav 2012; 13(4): 418–22.CrossRefGoogle ScholarPubMed
Kenny, B, Fuller-Tyszkiewicz, M, Moodie, M, Brown, V, Williams, J. Bi-directional associations between depressive symptoms and eating disorder symptoms in early adolescence. Body Image 2022; 42: 246–56.CrossRefGoogle ScholarPubMed
Wang, JN, Wang, M, Wu, GW, Li, WH, Lv, Z, Chen Q, et al. Uncovering neural pathways underlying bulimia nervosa: resting-state neural connectivity disruptions correlate with maladaptive eating behaviors. Eat Weight Disord 2023; 28(1): 91.CrossRefGoogle ScholarPubMed
Mele, G, Alfano, V, Cotugno, A, Longarzo, M. A broad-spectrum review on multimodal neuroimaging in bulimia nervosa and binge eating disorder. Appetite 2020; 151: 104712.CrossRefGoogle ScholarPubMed
Han, Y, Yan, H, Shan, X, Li, H, Liu, F, Li, P, et al. Disrupted functional connectivity associated with cognitive impairment in generalized anxiety disorder (GAD) and comorbid GAD and depression: a follow-up fMRI study. J Psychiatry Neurosci 2023; 48(6): E439–51.CrossRefGoogle ScholarPubMed
Murray, SB, Alba, C, Duval, CJ, Nagata, JM, Ganson, KT, Jann, K. Sex differences in functional connectivity from reward-based regions in pre-adolescent binge eating disorder. Psychiatry Res 2023; 324: 115186.CrossRefGoogle ScholarPubMed
Battistella, G, Simonyan, K. Top-down alteration of functional connectivity within the sensorimotor network in focal dystonia. Neurology 2019; 92(16): e1843–51.CrossRefGoogle ScholarPubMed
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material
Download Chen et al. supplementary material(File)
File 658.7 KB
Submit a response

eLetters

No eLetters have been published for this article.