Advertisement

Binge Eating pp 121-135 | Cite as

Neuroimaging to Study Brain Reward Processing and Reward-Based Learning in Binge Eating Pathology

  • Marisa DeGuzmanEmail author
  • Guido K. W. Frank
Chapter
  • 68 Downloads

Abstract

This chapter reviews human neuroimaging studies that investigate the neurobiology of reward processing in eating disorders associated with binge eating. Across the relatively small research literature on binge-eating disorder (BED) and bulimia nervosa (BN) using food and nonfood stimuli, neuroimaging studies consistently suggest alterations in brain reward circuit response. Studies tend to identify heightened brain response to visual presentation of reward cues, while reward receipt, including unexpected receipt, is associated with lower brain activation. Those results point toward specific neurotransmitter alterations associated with binge eating pathophysiology. However, there is still extensive heterogeneity across studies due to different study designs and analytic approaches, and research that systematically translates and studies basic science models in humans will have the best chance of identifying neurocircuitry that is specific to this pathology.

Keywords

Reward processing Reward-based learning Neuroimaging 

References

  1. American Psychiatric Association (2013) Desk reference to the diagnostic criteria from DSM-5. American Psychiatric Publishing, Washington, DCGoogle Scholar
  2. Avena NM (2013) Animal models of eating disorders. In: Avena NM (ed) Neuromethods, vol 74. Humana Press, Totowa, NJ, pp 281–290Google Scholar
  3. Bailer UF, Frank GK, Price JC, Meltzer CC, Becker C, Mathis CA, Wagner A, Barbarich-Marsteller NC, Bloss CS, Putnam K, Schork NJ, Gamst A, Kaye WH (2013) Interaction between serotonin transporter and dopamine D2/D3 receptor radioligand measures is associated with harm avoidant symptoms in anorexia and bulimia nervosa. Psychiatry Res 211(2):160–168.  https://doi.org/10.1016/j.pscychresns.2012.06.010CrossRefPubMedGoogle Scholar
  4. Balodis IM, Kober H, Worhunsky PD, White MA, Stevens MC, Pearlson GD, Sinha R, Grilo CM, Potenza MN (2013) Monetary reward processing in obese individuals with and without binge eating disorder. Biol Psychiatry 73(9):877–886.  https://doi.org/10.1016/j.biopsych.2013.01.014CrossRefPubMedPubMedCentralGoogle Scholar
  5. Balodis IM, Grilo CM, Kober H, Worhunsky PD, White MA, Stevens MC, Pearlson GD, Potenza MN (2014) A pilot study linking reduced fronto-striatal recruitment during reward processing to persistent bingeing following treatment for binge-eating disorder. Int J Eat Disord 47(4):376–384.  https://doi.org/10.1002/eat.22204CrossRefPubMedGoogle Scholar
  6. Berridge KC (2009a) ‘Liking’ and ‘wanting’ food rewards: brain substrates and roles in eating disorders. Physiol Behav 97(5):537–550.  https://doi.org/10.1016/j.physbeh.2009.02.044CrossRefPubMedPubMedCentralGoogle Scholar
  7. Berridge KC (2009b) Wanting and liking: observations from the neuroscience and psychology laboratory. Inquiry (Oslo) 52(4):378.  https://doi.org/10.1080/00201740903087359CrossRefGoogle Scholar
  8. Bodell LP, Wildes JE, Goldschmidt AB, Lepage R, Keenan KE, Guyer AE, Hipwell AE, Stepp SD, Forbes EE (2018) Associations between neural reward processing and binge eating among adolescent girls. J Adolesc Health 62(1):107–113.  https://doi.org/10.1016/j.jadohealth.2017.08.006CrossRefPubMedGoogle Scholar
  9. Bohon C, Stice E (2011) Reward abnormalities among women with full and subthreshold bulimia nervosa: a functional magnetic resonance imaging study. Int J Eat Disord 44(7):585–595.  https://doi.org/10.1002/eat.20869CrossRefPubMedGoogle Scholar
  10. Boswell RG, Kober H (2016) Food cue reactivity and craving predict eating and weight gain: a meta-analytic review. Obes Rev 17(2):159–177.  https://doi.org/10.1111/obr.12354CrossRefPubMedGoogle Scholar
  11. Broft A, Shingleton R, Kaufman J, Liu F, Kumar D, Slifstein M, Abi-Dargham A, Schebendach J, Van Heertum R, Attia E, Martinez D, Walsh BT (2012) Striatal dopamine in bulimia nervosa: a PET imaging study. Int J Eat Disord 45(5):648–656.  https://doi.org/10.1002/eat.20984CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cambridge VC, Ziauddeen H, Nathan PJ, Subramaniam N, Dodds C, Chamberlain SR, Koch A, Maltby K, Skeggs AL, Napolitano A, Farooqi IS, Bullmore ET, Fletcher PC (2013) Neural and behavioral effects of a novel mu opioid receptor antagonist in binge-eating obese people. Biol Psychiatry 73(9):887–894.  https://doi.org/10.1016/j.biopsych.2012.10.022CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chase HW, Fournier JC, Bertocci MA, Greenberg T, Aslam H, Stiffler R, Lockovich J, Graur S, Bebko G, Forbes EE, Phillips ML (2017) A pathway linking reward circuitry, impulsive sensation-seeking and risky decision-making in young adults: identifying neural markers for new interventions. Transl Psychiatry 7(4):e1096.  https://doi.org/10.1038/tp.2017.60CrossRefPubMedPubMedCentralGoogle Scholar
  14. Craig AD (2009) How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70.  https://doi.org/10.1038/nrn2555CrossRefPubMedGoogle Scholar
  15. Cuthbert BN (2014) Translating intermediate phenotypes to psychopathology: the NIMH research domain criteria. Psychophysiology 51(12):1205–1206.  https://doi.org/10.1111/psyp.12342CrossRefPubMedGoogle Scholar
  16. Cyr M, Wang Z, Tau GZ, Zhao G, Friedl E, Stefan M, Terranova K, Marsh R (2016) Reward-based spatial learning in teens with bulimia nervosa. J Am Acad Child Adolesc Psychiatry 55(11):962–971.e3.  https://doi.org/10.1016/j.jaac.2016.07.778CrossRefPubMedPubMedCentralGoogle Scholar
  17. de Araujo IE, Kringelbach ML, Rolls ET, Hobden P (2003) Representation of umami taste in the human brain. J Neurophysiol 90(1):313–319.  https://doi.org/10.1152/jn.00669.2002CrossRefPubMedGoogle Scholar
  18. Dodds CM, O’Neill B, Beaver J, Makwana A, Bani M, Merlo-Pich E, Fletcher PC, Koch A, Bullmore ET, Nathan PJ (2012) Effect of the dopamine D3 receptor antagonist GSK598809 on brain responses to rewarding food images in overweight and obese binge eaters. Appetite 59(1):27–33.  https://doi.org/10.1016/j.appet.2012.03.007CrossRefPubMedGoogle Scholar
  19. Filbey FM, Myers US, Dewitt S (2012) Reward circuit function in high BMI individuals with compulsive overeating: similarities with addiction. NeuroImage 63(4):1800–1806.  https://doi.org/10.1016/j.neuroimage.2012.08.073CrossRefPubMedGoogle Scholar
  20. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, Akers CA, Clinton SM, Phillips PE, Akil H (2011) A selective role for dopamine in stimulus-reward learning. Nature 469(7328):53–57.  https://doi.org/10.1038/nature09588CrossRefPubMedGoogle Scholar
  21. Frank GK (2011) Reward and neurocomputational processes. Curr Top Behav Neurosci 6:95–110.  https://doi.org/10.1007/7854_2010_81
  22. Frank GK (2013) Altered brain reward circuits in eating disorders: chicken or egg? Curr Psychiatry Rep 15(10):396.  https://doi.org/10.1007/s11920-013-0396-xCrossRefPubMedPubMedCentralGoogle Scholar
  23. Frank GK (2015) Advances from neuroimaging studies in eating disorders. CNS Spectr 20:1–10.  https://doi.org/10.1017/S1092852915000012CrossRefGoogle Scholar
  24. Frank GK (2016) The perfect storm—a bio-psycho-social risk model for developing and maintaining eating disorders. Front Behav Neurosci 10:44.  https://doi.org/10.3389/fnbeh.2016.00044CrossRefPubMedPubMedCentralGoogle Scholar
  25. Frank GK, Kaye WH (2005) Positron emission tomography studies in eating disorders: multireceptor brain imaging, correlates with behavior and implications for pharmacotherapy. Nucl Med Biol 32(7):755–761.  https://doi.org/10.1016/j.nucmedbio.2005.06.011CrossRefPubMedGoogle Scholar
  26. Frank GK, Reynolds JR, Shott ME, O’Reilly RC (2011) Altered temporal difference learning in bulimia nervosa. Biol Psychiatry 70(8):728–735.  https://doi.org/10.1016/j.biopsych.2011.05.011CrossRefPubMedPubMedCentralGoogle Scholar
  27. Frank GK, Shott ME, Riederer J, Pryor TL (2016) Altered structural and effective connectivity in anorexia and bulimia nervosa in circuits that regulate energy and reward homeostasis. Transl Psychiatry 6(11):e932.  https://doi.org/10.1038/tp.2016.199CrossRefPubMedPubMedCentralGoogle Scholar
  28. Frank GKW, DeGuzman MC, Shott ME, Laudenslager ML, Rossi B, Pryor T (2018a) Association of brain reward learning response with harm avoidance, weight gain, and hypothalamic effective connectivity in adolescent anorexia nervosa. JAMA Psychiatry 75(10):1071–1080.  https://doi.org/10.1001/jamapsychiatry.2018.2151CrossRefPubMedPubMedCentralGoogle Scholar
  29. Frank GKW, Favaro A, Marsh R, Ehrlich S, Lawson EA (2018b) Toward valid and reliable brain imaging results in eating disorders. Int J Eat Disord 51(3):250–261.  https://doi.org/10.1002/eat.22829CrossRefPubMedGoogle Scholar
  30. Frank GKW, Shott ME, DeGuzman MC, Smolen A (2018c) Dopamine D2 -141C Ins/Del and Taq1A polymorphisms, body mass index, and prediction error brain response. Transl Psychiatry 8(1):102.  https://doi.org/10.1038/s41398-018-0147-1CrossRefPubMedPubMedCentralGoogle Scholar
  31. Geliebter A, Ladell T, Logan M, Schneider T, Sharafi M, Hirsch J (2006) Responsivity to food stimuli in obese and lean binge eaters using functional MRI. Appetite 46(1):31–35.  https://doi.org/10.1016/j.appet.2005.09.002CrossRefPubMedGoogle Scholar
  32. Geliebter A, Benson L, Pantazatos SP, 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.  https://doi.org/10.1016/j.appet.2015.08.009CrossRefPubMedGoogle Scholar
  33. Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35(1):4–26.  https://doi.org/10.1038/npp.2009.129CrossRefPubMedGoogle Scholar
  34. Hayes DJ, Greenshaw AJ (2011) 5-HT receptors and reward-related behaviour: a review. Neurosci Biobehav Rev 35(6):1419–1449.  https://doi.org/10.1016/j.neubiorev.2011.03.005CrossRefPubMedGoogle Scholar
  35. Karhunen LJ, Vanninen EJ, Kuikka JT, Lappalainen RI, Tiihonen J, Uusitupa MI (2000) Regional cerebral blood flow during exposure to food in obese binge eating women. Psychiatry Res 99(1):29–42CrossRefGoogle Scholar
  36. Kelley AE, Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22(9):3306–3311.  https://doi.org/10.1523/JNEUROSCI.22-09-03306.2002CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86(5):773–795.  https://doi.org/10.1016/j.physbeh.2005.08.066CrossRefPubMedGoogle Scholar
  38. Kessler RM, Hutson PH, Herman BK, Potenza MN (2016) The neurobiological basis of binge-eating disorder. Neurosci Biobehav Rev 63:223–238.  https://doi.org/10.1016/j.neubiorev.2016.01.013CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lee JE, Namkoong K, Jung YC (2017) Impaired prefrontal cognitive control over interference by food images in binge-eating disorder and bulimia nervosa. Neurosci Lett 651:95–101.  https://doi.org/10.1016/j.neulet.2017.04.054CrossRefPubMedGoogle Scholar
  40. Lloyd EC, Steinglass JE (2018) What can food-image tasks teach us about anorexia nervosa? A systematic review. J Eat Disord 6:31.  https://doi.org/10.1186/s40337-018-0217-zCrossRefPubMedPubMedCentralGoogle Scholar
  41. Michaelides M, Thanos PK, Volkow ND, Wang GJ (2012) Dopamine-related frontostriatal abnormalities in obesity and binge-eating disorder: emerging evidence for developmental psychopathology. Int Rev Psychiatry 24(3):211–218.  https://doi.org/10.3109/09540261.2012.679918CrossRefPubMedPubMedCentralGoogle Scholar
  42. Monteleone AM, 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. Prog Neuropsychopharmacol Biol Psychiatry 80(Pt B):132–142.  https://doi.org/10.1016/j.pnpbp.2017.02.020. Epub 2017 Mar 1
  43. Mueller SV, Morishima Y, Schwab S, Wiest R, Federspiel A, Hasler G (2018) Neural correlates of impaired reward-effort integration in remitted bulimia nervosa. Neuropsychopharmacology 43(4):868–876.  https://doi.org/10.1038/npp.2017.277CrossRefPubMedGoogle Scholar
  44. Ohmura Y, Tsutsui-Kimura I, Sasamori H, Nebuka M, Nishitani N, Tanaka KF, Yamanaka A, Yoshioka M (2019) Different roles of distinct serotonergic pathways in anxiety-like behavior, antidepressant-like, and anti-impulsive effects. Neuropharmacology:107703.  https://doi.org/10.1016/j.neuropharm.2019.107703
  45. Reiter AM, Heinze HJ, Schlagenhauf F, Deserno L (2017) Impaired flexible reward-based decision-making in binge eating disorder: evidence from computational modeling and functional neuroimaging. Neuropsychopharmacology 42(3):628–637.  https://doi.org/10.1038/npp.2016.95CrossRefPubMedGoogle Scholar
  46. Rolls ET (2016) Functions of the anterior insula in taste, autonomic, and related functions. Brain Cogn 110:4–19.  https://doi.org/10.1016/j.bandc.2015.07.002CrossRefPubMedGoogle Scholar
  47. Rolls BJ, Rolls ET, Rowe EA, Sweeney K (1981) Sensory specific satiety in man. Physiol Behav 27(1):137–142CrossRefGoogle Scholar
  48. Schafer A, Vaitl D, Schienle A (2010) Regional grey matter volume abnormalities in bulimia nervosa and binge-eating disorder. NeuroImage 50(2):639–643.  https://doi.org/10.1016/j.neuroimage.2009.12.063CrossRefPubMedGoogle Scholar
  49. Schag K, Schonleber J, Teufel M, Zipfel S, Giel KE (2013) Food-related impulsivity in obesity and binge eating disorder—a systematic review. Obes Rev 14(6):477–495.  https://doi.org/10.1111/obr.12017CrossRefGoogle Scholar
  50. Schienle A, Schafer A, Hermann A, Vaitl D (2009) Binge-eating disorder: reward sensitivity and brain activation to images of food. Biol Psychiatry 65(8):654–661.  https://doi.org/10.1016/j.biopsych.2008.09.028CrossRefPubMedGoogle Scholar
  51. Setsu R, Hirano Y, Tokunaga M, Takahashi T, Numata N, Matsumoto K, Masuda Y, Matsuzawa D, Iyo M, Shimizu E, Nakazato M (2017) Increased subjective distaste and altered insula activity to umami Tastant in patients with bulimia nervosa. Front Psychiatry 8:172.  https://doi.org/10.3389/fpsyt.2017.00172CrossRefPubMedPubMedCentralGoogle Scholar
  52. Simon JJ, Skunde M, Walther S, Bendszus M, Herzog W, Friederich HC (2016) Neural signature of food reward processing in bulimic-type eating disorders. Soc Cogn Affect Neurosci 11(9):1393–1401.  https://doi.org/10.1093/scan/nsw049CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tomasi D, Volkow ND (2013) Striatocortical pathway dysfunction in addiction and obesity: differences and similarities. Crit Rev Biochem Mol Biol 48(1):1–19.  https://doi.org/10.3109/10409238.2012.735642CrossRefPubMedGoogle Scholar
  54. Uddin LQ, Nomi JS, Hebert-Seropian B, Ghaziri J, Boucher O (2017) Structure and function of the human insula. J Clin Neurophysiol 34(4):300–306.  https://doi.org/10.1097/WNP.0000000000000377CrossRefPubMedPubMedCentralGoogle Scholar
  55. Vitousek K, Manke F (1994) Personality variables and disorders in anorexia nervosa and bulimia nervosa. J Abnorm Psychol 103(1):137–147CrossRefGoogle Scholar
  56. Voon V, Morris LS, Irvine MA, Ruck C, Worbe Y, Derbyshire K, Rankov V, Schreiber LR, Odlaug BL, Harrison NA, Wood J, Robbins TW, Bullmore ET, Grant JE (2015) Risk-taking in disorders of natural and drug rewards: neural correlates and effects of probability, valence, and magnitude. Neuropsychopharmacology 40(4):804–812.  https://doi.org/10.1038/npp.2014.242CrossRefPubMedGoogle Scholar
  57. Wagner A, Barbarich-Marsteller NC, Frank GK, Bailer UF, Wonderlich SA, Crosby RD, Henry SE, Vogel V, Plotnicov K, McConaha C, Kaye WH (2006) Personality traits after recovery from eating disorders: do subtypes differ? Int J Eat Disord 39(4):276–284.  https://doi.org/10.1002/eat.20251CrossRefPubMedGoogle Scholar
  58. Wang GJ, Geliebter A, Volkow ND, Telang FW, Logan J, Jayne MC, Galanti K, Selig PA, Han H, Zhu W, Wong CT, Fowler JS (2011) Enhanced striatal dopamine release during food stimulation in binge eating disorder. Obesity (Silver Spring) 19(8):1601–1608.  https://doi.org/10.1038/oby.2011.27CrossRefGoogle Scholar
  59. Weygandt M, Schaefer A, Schienle A, Haynes JD (2012) Diagnosing different binge-eating disorders based on reward-related brain activation patterns. Hum Brain Mapp 33(9):2135–2146.  https://doi.org/10.1002/hbm.21345CrossRefPubMedGoogle Scholar
  60. Wierenga CE, Ely A, Bischoff-Grethe A, Bailer UF, Simmons AN, Kaye WH (2014) Are extremes of consumption in eating disorders related to an altered balance between reward and inhibition? Front Behav Neurosci 8:410.  https://doi.org/10.3389/fnbeh.2014.00410CrossRefPubMedPubMedCentralGoogle Scholar
  61. Wonderlich JA, Breithaupt L, Thompson JC, Crosby RD, Engel SG, Fischer S (2018) The impact of neural responses to food cues following stress on trajectories of negative and positive affect and binge eating in daily life. J Psychiatr Res 102:14–22.  https://doi.org/10.1016/j.jpsychires.2018.03.005. Epub 2018 Mar 14.PMID: 29558632CrossRefPubMedGoogle Scholar
  62. Wu M, Brockmeyer T, Hartmann M, Skunde M, Herzog W, Friederich HC (2016) Reward-related decision making in eating and weight disorders: a systematic review and meta-analysis of the evidence from neuropsychological studies. Neurosci Biobehav Rev 61:177–196.  https://doi.org/10.1016/j.neubiorev.2015.11.017CrossRefGoogle Scholar
  63. Xia L, Gu R, Zhang D, Luo Y (2017) Anxious individuals are impulsive decision-makers in the delay discounting task: an ERP study. Front Behav Neurosci 11:5.  https://doi.org/10.3389/fnbeh.2017.00005CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of the Incarnate WordSan AntonioUSA
  2. 2.Department of PsychiatryUniversity of California San DiegoSan DiegoUSA

Personalised recommendations