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| Neural mechanisms of binge eating from a reward-inhibition dual-system perspective |
| CHEN Ximei1, LI Wei1, YANG Yingkai1,2, CHEN Hong1,2,3 |
1 School of Psychology, Southwest University, Chongqing 400715; 2 Key Laboratory of Cognition and Personality (Ministry of Education), Southwest University,Chongqing 400715; 3 Research Center of Psychology and Social Development, Faculty of Psychology, Southwest University, Chongqing 400715 |
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Abstract As an important risk factor for overweight and obesity, binge eating has recently gained increasing attention in the field of health psychology. At the behavioral level, binge eating has been linked to enhanced reward sensitivity and altered inhibitory control in non-clinical individuals. At the neural level, the decreased functional synchrony between the brain’s reward and cognitive control systems (i.e., the brain dual-system) represents the crucial neural substrates that could explain the potential interactions of dysfunctional reward sensitivity with inhibitory control in binge eating. These non-clinical findings are consistent with previous clinical studies involved in children and adults with binge-eating disorder. From a reward-inhibition dual-system perspective, the evidence reviewed in this study suggests that future research needs to systematically investigate the crucial role of the brain dual-system interactions (e.g., “correlation” and “causality”) in binge eating in the general population. From a developmental perspective of binge eating, it is important to further reveal the full range of neuromarkers of the dual-system interaction, from childhood to adulthood.
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[1] 吕振勇, 郑盼盼, Jackson. T. (2016). 暴食症的影响因素及其机制.心理科学进展, 24(1), 55-65. [2] 郑琰, 郭佳鑫, 张方屹. (2020). 生活事件和情绪性进食的关系:功能失调性态度的调节作用.心理研究, 13(1), 76-81. [3] Abdo N., Boyd E., Baboumian S., Pantazatos S. P., & Geliebter A. (2020). Relationship between binge eating and associated eating behaviors with subcortical brain volumes and cortical thickness.Journal of Affective Disorders, 274, 1201-1205. [4] Adise S., Geier C. F., Roberts N. J., White C. N., & Keller K. L. (2018). Is brain response to food rewards related to overeating? A test of the reward surfeit model of overeating in children. Appetite, 128, 167-179. [5] Adise S., Geier C. F., Roberts N. J., White C. N., & Keller K. L. (2019). Food or money? Children’s brains respond differently to rewards regardless of weight status. Pediatric Obesity, 14(2), Article e12469. [6] American Psychiatric Association.(2013). Diagnostic and statistical manual of mental disorders (DSM-5) (5th ed.). Washington, DC: American Psychiatric Publishing. [7] Ames S. L., Kisbu-Sakarya Y., Reynolds K. D., Boyle S., Cappelli C., Cox M. G., .. Stacy A. W. (2014). Inhibitory control effects in adolescent binge eating and consumption of sugar-sweetened beverages and snacks.Appetite, 81, 180-192. [8] Balodis I. M., Kober H., Worhunsky P. D., White M. A., Stevens M. C., Pearlson G. D., .. Potenza M. N. (2013a). Monetary reward processing in obese individuals with and without binge eating disorder.Biological Psychiatry, 73(9), 877-886. [9] Balodis I. M., Molina N. D., Kober H., Worhunsky P. D., White M. A., Rajita Sinha, Grilo, C. M., & Potenza M. N. (2013b). Divergent neural substrates of inhibitory control in binge eating disorder relative to other manifestations of obesity.Obesity, 21(2), 367-377. [10] Bari, A., & Robbins, T. W. (2013). Inhibition and impulsivity: Behavioral and neural basis of response control.Progress in Neurobiology, 108, 44-79. [11] Bartholdy S., O’Daly O. G., Campbell I. C., Banaschewski T., Barker G., Bokde A., .. IMAGEN Consortium. (2019). Neural correlates of failed inhibitory control as an early marker of disordered dating in adolescents.Biological Psychiatry, 85(11), 956-965. [12] Best J. R., Miller P. H., & Jones L. L. (2009). Executive functions after age 5: Changes and correlates.Developmental Review, 29(3), 180-200. [13] Bodell L. P., Wildes J. E., Goldschmidt A. B., Lepage R., Keenan K. E., Guyer A. E., .. Forbes E. E. (2018). Associations between neural reward processing and binge eating among adolescent girls.Journal of Adolescent Health, 62(1), 107-113. [14] Carver, C. S., & White, T. L. (1994). Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS scales.Journal of Personality and Social Psychology, 67(2), 319-333. [15] Chen X., Gao X., Qin J., Wang C., Xiao M., Tian Y., .. Chen H. (2021). Resting-state functional network connectivity underlying eating disorder symptoms in healthy young adults. NeuroImage: Clinical, 30, Article 102671. [16] Chen X., Li W., Liu Y., Xiao M., & Chen H. (2023). Altered effective connectivity between reward and inhibitory control networks in people with binge eating episodes: A spectral dynamic causal modeling study.Appetite, 188, 106763. [17] Cosme, D., & Lopez, R. B. (2020). Neural indicators of food cue reactivity, regulation, and valuation and their associations with body composition and daily eating behavior. Social Cognitive and Affective Neuroscience. Advance online publication. [18] Cuthbert, B. N. (2015). Research Domain Criteria: Toward future psychiatric nosologies.Dialogues in Clinical Neuroscience, 17(1), 89-97. [19] Cyr M., Wang Z., Tau G. Z., Zhao G., Friedl E., Stefan M., .. Marsh R. (2016). Reward-based spatial learning in teens with bulimia nervosa.Journal of the American Academy of Child and Adolescent Psychiatry, 55(11), 962-971. [20] Eneva K. T., Murray S., O'Garro-Moore J., Yiu A., Alloy L. B., Avena N. M., & Chen E. Y. (2017). Reward and punishment sensitivity and disordered eating behaviors in men and women.Journal of Eating Disorders, 5, 6. [21] Farr O. M., Li C. R., & Mantzoros C. S. (2016). Central nervous system regulation of eating: Insights from human brain imaging.Metabolism: Clinical and Experimental, 65(5), 699-713. [22] Filbey F. M., Myers U. S., & Dewitt S. (2012). Reward circuit function in high BMI individuals with compulsive overeating: Similarities with addiction.NeuroImage, 63(4), 1800-1806. [23] Fisher, J. O., & Birch, L. L. (1999). Restricting access to foods and children’s eating.Appetite, 32(3), 405-419. [24] Flegal K. M., Kruszon-Moran D., Carroll M. D., Fryar C. D., & Ogden C. L. (2016). Trends in obesity among adults in the United States, 2005 to 2014.JAMA, 315(21), 2284-2291. [25] Forbush K. T., Wildes J. E., Pollack L. O., Dunbar D., Luo J., Patterson K., .. Watson D. (2013). Development and validation of the eating pathology symptoms inventory (EPSI).Psychological Assessment, 25(3), 859-878. [26] Frank G. K. (2013). Altered brain reward circuits in eating disorders: Chicken or egg? Current Psychiatry Reports, 15(10), 396. [27] Garner, D. M. (2004). Eating Disorder Inventory-3. Psychological Assessment Resources Inc: Professional Manual. [28] Geliebter A., Benson L., Pantazatos S. P., Hirsch J., & Carnell S. (2016). Greater anterior cingulate activation and connectivity in response to visual and auditory high-calorie food cues in binge eating: Preliminary findings.Appetite, 96, 195-202. [29] Goldschmidt A. B., Wall M. M., Zhang J., Loth K. A., & Neumark-Sztainer D. (2016). Overeating and binge eating in emerging adulthood: 10-year stability and risk factors.Developmental Psychology, 52(3), 475-483. [30] Gormally J., Black S., Daston S., & Rardin D. (1982). The assessment of binge eating severity among obese persons.Addictive Behaviors, 7(1), 47-55. [31] Hagan, K. E., & Bohon, C. (2021). Subcortical brain volume and cortical thickness in adolescent girls and women with binge eating.International Journal of Eating Disorders, 54(8), 1527-1536. [32] Haynos A. F., Camchong J., Pearson C. M., Lavender J. M., Mueller B. A., Peterson C. B., .. Lim K. O. (2021). Resting state hypoconnectivity of reward networks in binge eating disorder.Cerebral Cortex, 31(5), 2494-2504. [33] Keith S. W., Redden D. T., Katzmarzyk P. T., Boggiano M. M., Hanlon E. C., Benca R. M., .. Allison D. B. (2006). Putative contributors to the secular increase in obesity: Exploring the roads less traveled.International Journal of Obesity, 30, 1585-1594. [34] Kessler R. C., Berglund P. A., Chiu W. T., Deitz A. C., Hudson J. I., Shahly V., .. Xavier M. (2013). The prevalence and correlates of binge eating disorder in the World Health Organization World Mental Health Surveys.Biological Psychiatry, 73, 904-914. [35] Knutson B., Westdorp A., Kaiser E., & Hommer D. (2000). FMRI visualization of brain activity during a monetary incentive delay task.NeuroImage, 12(1), 20-27. [36] Li W., Chen X., Luo Y., Luo L., & Chen H. (2022). Orbitofrontal neural dissociation of healthy and unhealthy food reward sensitivity in normal-weight binge eaters. Psychiatry Research, 316, 114736. Advance online publication. [37] Liu X., Turel O., Xiao Z., Lv C., & He Q. (2023). Neural differences of food-specific inhibitory control in people with healthy vs higher BMI. Appetite, 188, 106759. [38] Lowe C. J., Morton J. B., & Reichelt A. C. (2020). Adolescent obesity and dietary decision making-A brain-health perspective.Lancet Child & Adolescent Health, 4(5), 388-396. [39] Lyu Z., Zheng P., Chen H., & Jackson T. (2017). Approach and inhibition responses to external food cues among average-weight women who binge eat and weight-matched controls.Appetite, 108, 367-374. [40] Manasse S. M., Goldstein S. P., Wyckoff E., Forman E. M., Juarascio A. S., Butryn M. L., .. Nederkoorn C. (2016). Slowing down and taking a second look: Inhibitory deficits associated with binge eating are not food-specific.Appetite, 96, 555-559. [41] Mele G., Alfano V., Cotugno A., & Longarzo M. (2020). A broad-spectrum review on multimodal neuroimaging in bulimia nervosa and binge eating disorder.Appetite, 151, 104712. [42] Monteleone A. M., Castellini G., Volpe U., Ricca V., Lelli L., Monteleone P., & Maj M. (2018). Neuroendocrinology and brain imaging of reward in eating disorders: A possible key to the treatment of anorexia nervosa and bulimia nervosa.Progress in Neuro-Psychopharmacology & Biological Psychiatry, 80(Pt B), 132-142. [43] Murray S. B., Alba C., Duval C. J., Nagata J. M., Cabeen R. P., Lee D. J., .. Jann K. (2022). Aberrant functional connectivity between reward and inhibitory control networks in pre-adolescent binge eating disorder. Psychological Medicine, 1-10. Advance online publication. [44] Ogden C. L., Carroll M. D., Lawman H. G., Fryar C. D., Kruszon-Moran D., Kit B. K., & Flegal K. M. (2016). Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014.JAMA, 315(21), 2292-2299. [45] Oliva R., Budisavljevi S., Castiello U., & Begliomini C. (2021). Neuroanatomical correlates of binge-eating behavior: At the roots of unstoppable eating.Brain Sciences, 11(9), 1162. [46] Oliva R., Morys F., Horstmann A., Castiello U., & Begliomini C. (2019). The impulsive brain: Neural underpinnings of binge eating behavior in normal-weight adults.Appetite, 136, 33-49. [47] Oliva R., Morys F., Horstmann A., Castiello U., & Begliomini C. (2020). Characterizing impulsivity and resting-state functional connectivity in normal-weight binge eaters.International Journal of Eating Disorders, 53(3), 478-488. [48] Olivo G., Gaudio S., & Schi?th H. B. (2019). Brain and cognitive development in adolescents with anorexia nervosa: A systematic review of fMRI studies. Nutrients, 11(8), Article 1907. [49] Shapiro A., Johnson S. L., Sutton B., Legget K. T., Dabelea D., & Tregellas J. R. (2019). Eating in the absence of hunger in young children is related to brain reward network hyperactivity and reduced functional connectivity in executive control networks. Pediatric Obesity, 14(6), Article e12502. [50] Simon J. J., Skunde M., Walther S., Bendszus M., Herzog W., & Friederich H. C. (2016). Neural signature of food reward processing in bulimic-type eating disorders.Social Cognitive and Affective Neuroscience, 11(9), 1393-1401. [51] Smith, D. G., & Robbins, T. W. (2013). The neurobiological underpinnings of obesity and binge eating: A rationale for adopting the food addiction model.Biological Psychiatry, 73(9), 804-810. [52] Smith K. E., Luo S., & Mason T. B. (2021). A systematic review of neural correlates of dysregulated eating associated with obesity risk in youth.Neuroscience and Biobehavioral Reviews, 124, 245-266. [53] Steward T., Menchón J. M., Jiménez-Murcia S., Soriano-Mas C., & Fernández-Aranda F. (2018). Neural network alterations across eating disorders: A narrative review of fMRI studies.Current Neuropharmacology, 16(8), 1150-1163. [54] Stice E., Marti C. N., Shaw H., & Jaconis M. (2009). An 8-year longitudinal study of the natural history of threshold, subthreshold, and partial eating disorders from a community sample of adolescents.Journal of Abnormal Psychology, 118(3), 587-597. [55] Stice E., Presnell K., & Spangler D. (2002). Risk factors for binge eating onset in adolescent girls: A 2-year prospective investigation.Health Psychology, 21(2), 131-138. [56] Stice E., Telch C. F., & Rizvi S. L. (2000). Development and validation of the Eating Disorder Diagnostic Scale: A brief self-report measure of anorexia, bulimia, and binge-eating disorder.Psychological Assessment, 12(2), 123-131. [57] Sutton C. A., L’Insalata A. M., & Fazzino T. L. (2022). Reward sensitivity, eating behavior, and obesity-related outcomes: A systematic review.Physiology & Behavior, 252, 113843. [58] Swanson S. A., Crow S. J., Le Grange D., Swendsen J., & Merikangas K. R. (2011). Prevalence and correlates of eating disorders in adolescents. Results from the national comorbidity survey replication adolescent supplement.Archives of General Psychiatry, 68, 714-723. [59] Tanofsky-Kraff M., Schvey N. A., & Grilo C. M. (2020). A developmental framework of binge-eating disorder based on pediatric loss of control eating.American Psychologist, 75(2), 189-203. [60] Udo, T., & Grilo, C. M. (2018). Prevalence and correlates of DSM-5-defined eating disorders in a nationally representative sample of U.S. adults.Biological Psychiatry, 84, 345-354. [61] Weafer J., Crane N. A., Gorka S. M., Phan K. L., & de Wit H. (2019). Neural correlates of inhibition and reward are negatively associated.NeuroImage, 196, 188-194. [62] Zhang R., Geng X., & Lee T. (2017). Large-scale functional neural network correlates of response inhibition: An fMRI meta-analysis.Brain Structure & Function, 222(9), 3973-3990. [63] Zhang X., Wen K., Han J., & Chen H. (2023). The neural processes in food decision-making and their effect on daily diet management in successful and unsuccessful restrained eaters.Neuroscience, 517, 1-17. [64] Zhang Z., Robinson L., Jia T., Quinlan E. B., Tay N., Chu C., .. Desrivières S. (2020). Development of disordered eating behaviors and comorbid depressive symptoms in adolescence: Neural and psychopathological predictors.Biological Psychiatry, 90(12), 853-862. |
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