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The role of the opioid system in binge eating disorder

Published online by Cambridge University Press:  26 October 2015

Chiara Giuliano  and
Pietro Cottone
Chiara Giuliano*
Affiliation:
Behavioral and Clinical Neuroscience Institute and Department of Psychology, University of Cambridge, Downing Street, Cambridge, UK
Pietro Cottone
Affiliation:
Laboratory of Addictive Disorders, Departments of Pharmacology and Experimental Therapeutics and Psychiatry, Boston University School of Medicine, Boston, Massachusetts, USA
*
*Address for correspondence: Dr. Chiara Giuliano, Department of Psychology, University of Cambridge, Downing St, Cambridge CB2 3EB, UK. (Email: [email protected])
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Abstract

Binge eating disorder is characterized by excessive, uncontrollable consumption of palatable food within brief periods of time. Excessive intake of palatable food is thought to be driven by hedonic, rather than energy homeostatic, mechanisms. However, reward processing does not only comprise consummatory actions; a key component is represented by the anticipatory phase directed at procuring the reward. This phase is highly influenced by environmental food-associated stimuli, which can robustly enhance the desire to eat even in the absence of physiological needs. The opioid system (endogenous peptides and their receptors) has been strongly linked to the rewarding aspects of palatable food intake, and perhaps represents the key system involved in hedonic overeating. Here we review evidence suggesting that the opioid system can also be regarded as one of the systems that regulates the anticipatory incentive processes preceding binge eating hedonic episodes.

Keywords

Animal modelsbinge eatingincentive salienceopioidspalatable food
Type
Review Articles
Information
CNS Spectrums , Volume 20 , Special Issue 6: Binge Eating Disorder Differentiating from General Obesity , December 2015 , pp. 537 - 545
Copyright
© Cambridge University Press 2015 

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Footnotes

The authors would like to thank Prof. Barry Everitt for constructive and helpful comments on the manuscript and Dr. David Belin for the generous contribution of generating the illustration.

References

1. Stein, RI, Kenardy, J, Wiseman, CV, Dounchis, JZ, Arnow, BA, Wilfley, DE. What’s driving the binge in binge eating disorder? A prospective examination of precursors and consequences. Int J Eat Disord. 2007; 40(3): 195–203.Google Scholar
2. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Arlington, VA: American Psychiatric Publishing; 2013.Google Scholar
3. Hudson, JI, Hiripi, E, Pope, HG, Kessler, RC. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry. 2007; 61(3): 348–358.Google Scholar
4. Swanson, SA, Crow, SJ, Le Grange, D, Swendsen, J, Merikangas, KR. Prevalence and correlates of eating disorders in adolescents: results from the national comorbidity survey replication adolescent supplement. Arch Gen Psychiatry. 2011; 68(7): 714–723.Google Scholar
5. Devlin, MJ. Is there a place for obesity in DSM-V? Int J Eat Disord. 2007; 40(Suppl): S83–S88.Google Scholar
6. Pacanowski, CR, Senso, MM, Oriogun, K, Crain, AL, Sherwood, NE. Binge eating behavior and weight loss maintenance over a 2-year period. J Obes. 2014; 2014: e249315.Google Scholar
7. TODAY Study Group, Wilfley, D, Berkowitz, R, et al. Binge eating, mood, and quality of life in youth with type 2 diabetes: baseline data from the today study. Diabetes Care. 2011; 34(4): 858–860.Google Scholar
8. Striegel-Moore, RH, Franko, DL. Epidemiology of binge eating disorder. Int J Eat Disord. 2003; 34(Suppl): S19–S29.Google Scholar
9. Striegel-Moore, RH, Franko, DL. Should binge eating disorder be included in the DSM-V? A critical review of the state of the evidence. Annu Rev Clin Psychol. 2008; 4(1): 305–324.Google Scholar
10. U.S. Food and Drug Administration. FDA expands uses of Vyvanse to treat binge-eating disorder. January 30, 2015. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm432543.htm. Accessed June 11, 2015.Google Scholar
11. McElroy, SL, Guerdjikova, AI, Martens, B, Keck, PE, Pope, HG, Hudson, JI. Role of antiepileptic drugs in the management of eating disorders. CNS Drugs. 2009; 23(2): 139–156.Google Scholar
12. McElroy, SL, Hudson, JI, Capece, JA, et al. Topiramate for the treatment of binge eating disorder associated with obesity: a placebo-controlled study. Biol Psychiatry. 2007; 61(9): 1039–1048.Google Scholar
13. Yager, J. Binge eating disorder: the search for better treatments. Am J Psychiatry. 2008; 165(1): 4–6.Google Scholar
14. Polivy, J, Herman, CP. Dieting and binging: a causal analysis. Am Psychol. 1985; 40(2): 193–201.Google Scholar
15. Mela, DJ. Determinants of food choice: relationships with obesity and weight control. Obes Res. 2001; 9(Suppl 4): 249S–255S.Google Scholar
16. Yeomans, MR, Blundell, JE, Leshem, M. Palatability: response to nutritional need or need-free stimulation of appetite? Br J Nutr. 2004; 92(Suppl 1): S3–S14.Google Scholar
17. Cottone, P, Sabino, V, Steardo, L, Zorrilla, EP. Opioid-dependent anticipatory negative contrast and binge-like eating in rats with limited access to highly preferred food. Neuropsychopharmacology. 2008; 33(3): 524–535.CrossRefGoogle ScholarPubMed
18. de Zwaan, M. Binge eating disorder and obesity. Int J Obes Relat Metab Disord. 2001; 25(Suppl 1): S51–S55.CrossRefGoogle ScholarPubMed
19. Blasio, A, Steardo, L, Sabino, V, Cottone, P. Opioid system in the medial prefrontal cortex mediates binge-like eating. Addict Biol. 2014; 19(4): 652–662.Google Scholar
20. Yanovski, SZ, Leet, M, Yanovski, JA, et al. Food selection and intake of obese women with binge-eating disorder. Am J Clin Nutr. 1992; 56(6): 975–980.CrossRefGoogle ScholarPubMed
21. Polivy, J. The effects of behavioral inhibition: integrating internal cues, cognition, behavior, and affect. Psychological Inquiry. 1998; 9(3): 181–204.Google Scholar
22. Boggiano, MM, Turan, B, Maldonado, CR, Oswald, KD, Shuman, ES. Secretive food concocting in binge eating: test of a famine hypothesis. Int J Eat Disord. 2013; 46(3): 212–225.Google Scholar
23. Witt, AA, Lowe, MR. Hedonic hunger and binge eating among women with eating disorders. Int J Eat Disord. 2014; 47(3): 273–280.Google Scholar
24. Nathan, PJ, Bullmore, ET. From taste hedonics to motivational drive: central μ-opioid receptors and binge-eating behaviour. Int J Neuropsychopharmacol. 2009; 12(7): 995–1008.Google Scholar
25. Kelley, AE. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev. 2004; 27(8): 765–776.CrossRefGoogle ScholarPubMed
26. Peciña, S, Berridge, KC. Dopamine or opioid stimulation of nucleus accumbens similarly amplify cue-triggered “wanting” for reward: entire core and medial shell mapped as substrates for PIT enhancement. Eur J Neurosci. 2013; 37(9): 1529–1540.Google Scholar
27. Flagel, SB, Watson, SJ, Robinson, TE, Akil, H. Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology (Berl). 2007; 191(3): 599–607.CrossRefGoogle ScholarPubMed
28. Dagher, A. The neurobiology of appetite: hunger as addiction. Int J Obes (Lond). 2009; 33(Suppl 2): S30–S33.Google Scholar
29. Robinson, MJF, Burghardt, PR, Patterson, CM, et al. Individual differences in cue-induced motivation and striatal systems in rats susceptible to diet-induced obesity. Neuropsychopharmacology. 2015; 40(9): 2113–2123.Google Scholar
30. Ng, L, Davis, C. Cravings and food consumption in binge eating disorder. Eat Behav. 2013; 14(4): 472–475.Google Scholar
31. Greeno, CG, Wing, RR, Shiffman, S. Binge antecedents in obese women with and without binge eating disorder. J Consult Clin Psychol. 2000; 68(1): 95–102.Google Scholar
32. Berridge, KC. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci Biobehav Rev. 2000; 24(2): 173–198.CrossRefGoogle ScholarPubMed
33. Peciña, S, Berridge, KC. Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci. 2005; 25(50): 11777–11786.Google Scholar
34. Smith, KS, Berridge, KC. Opioid limbic circuit for reward: interaction between hedonic hotspots of nucleus accumbens and ventral pallidum. J Neurosci. 2007; 27(7): 1594–1605.CrossRefGoogle ScholarPubMed
35. Castro, DC, Berridge, KC. Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness “liking” and “wanting.”. J Neurosci. 2014; 34(12): 4239–4250.CrossRefGoogle ScholarPubMed
36. Woolley, JD, Lee, BS, Fields, HL. Nucleus accumbens opioids regulate flavor-based preferences in food consumption. Neuroscience. 2006; 143(1): 309–317.Google Scholar
37. Giuliano, C, Robbins, TW, Nathan, PJ, Bullmore, ET, Everitt, BJ. Inhibition of opioid transmission at the μ-opioid receptor prevents both food seeking and binge-like eating. Neuropsychopharmacology. 2012; 37(12): 2643–2652.Google Scholar
38. Cambridge, VC, Ziauddeen, H, Nathan, PJ, et al. Neural and behavioral effects of a novel mu opioid receptor antagonist in binge-eating obese people. Biol Psychiatry. 2013; 73(9): 887–894.Google Scholar
39. Ziauddeen, H, Chamberlain, SR, Nathan, PJ, et al. Effects of the mu-opioid receptor antagonist GSK1521498 on hedonic and consummatory eating behaviour: a proof of mechanism study in binge-eating obese subjects. Mol Psychiatry. 2013; 18(12): 1287–1293.Google Scholar
40. Gual, A, Bruguera, P, López-Pelayo, H. Nalmefene and its use in alcohol dependence. Drugs Today (Barc). 2014; 50(5): 347–355.Google Scholar
41. Petrovich, GD, Ross, CA, Gallagher, M, Holland, PC. Learned contextual cue potentiates eating in rats. Physiol Behav. 2007; 90(2–3): 362–367.Google Scholar
42. Castro, DC, Berridge, KC. Advances in the neurobiological bases for food “liking” versus “wanting.”. Physiol Behav. 2014; 136: 22–30.Google Scholar
43. Dickinson, A, Mackintosh, NJ. Classical conditioning in animals. Annu Rev Psychol. 1978; 29: 587–612.Google Scholar
44. Crombag, HS, Galarce, EM, Holland, PC. Pavlovian influences on goal-directed behavior in mice: the role of cue-reinforcer relations. Learn Mem. 2008; 15(5): 299–303.Google Scholar
45. Weingarten, HP. Conditioned cues elicit feeding in sated rats: a role for learning in meal initiation. Science. 1983; 220(4595): 431–433.Google Scholar
46. Petrovich, GD, Ross, CA, Gallagher, M, Holland, PC. Learned contextual cue potentiates eating in rats. Physiol Behav. 2007; 90(2–3): 362–367.Google Scholar
47. Hall, J, Parkinson, JA, Connor, TM, Dickinson, A, Everitt, BJ. Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur J Neurosci. 2001; 13(10): 1984–1992.Google Scholar
48. Everitt, BJ, Robbins, TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci. 2005; 8(11): 1481–1489.Google Scholar
49. Everitt, BJ, Robbins, TW. Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology (Berl). 2000; 153(1): 17–30.Google Scholar
50. Smith, KL, Rao, RR, Velázquez-Sánchez, C, et al. The uncompetitive N-methyl-D-aspartate antagonist memantine reduces binge-like eating, food-seeking behavior, and compulsive eating: role of the nucleus accumbens shell. Neuropsychopharmacology. 2015; 40(5): 1163–1171.Google Scholar
51. Flaherty, CF, Coppotelli, C, Grigson, PS, Mitchell, C, Flaherty, JE. Investigation of the devaluation interpretation of anticipatory negative contrast. J Exp Psychol Anim Behav Process. 1995; 21(3): 229–247.CrossRefGoogle ScholarPubMed
52. Pliner, P, Peter, C, Polivy, J. Palatability as a determinant of eating: finickiness as a function of taste, hunger, and the prospect of good food. In: Capaldi ED, Powley TL, eds. Taste, Experience, and Feeding. Washington, DC: American Psychological Association; 1990: 210–226.Google Scholar
53. Katsuura, Y, Taha, SA. Mu opioid receptor antagonism in the nucleus accumbens shell blocks consumption of a preferred sucrose solution in an anticipatory contrast paradigm. Neuroscience. 2014; 261: 144–152.Google Scholar
54. Flagel, SB, Clark, JJ, Robinson, TE, et al. A selective role for dopamine in stimulus-reward learning. Nature. 2011; 469(7328): 53–57.Google Scholar
55. Smith, KS, Berridge, KC, Aldridge, JW. Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc Natl Acad Sci U S A. 2011; 108(27): E255–E264.CrossRefGoogle ScholarPubMed
56. Tindell, AJ, Berridge, KC, Zhang, J, Peciña, S, Aldridge, JW. Ventral pallidal neurons code incentive motivation: amplification by mesolimbic sensitization and amphetamine. Eur J Neurosci. 2005; 22(10): 2617–2634.Google Scholar
57. Zhang, M, Balmadrid, C, Kelley, AE. Nucleus accumbens opioid, GABaergic, and dopaminergic modulation of palatable food motivation: contrasting effects revealed by a progressive ratio study in the rat. Behav Neurosci. 2003; 117(2): 202–211.Google Scholar
58. Fernando, ABP, Murray, JE, Milton, AL. The amygdala: securing pleasure and avoiding pain. Front Behav Neurosci. 2013; 7: 190.Google Scholar
59. Cardinal, RN, Parkinson, JA, Hall, J, Everitt, BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev. 2002; 26(3): 321–352.Google Scholar
60. Holland, PC, Hsu, M. Role of amygdala central nucleus in the potentiation of consuming and instrumental lever-pressing for sucrose by cues for the presentation or interruption of sucrose delivery in rats. Behav Neurosci. 2014; 128(1): 71–82.Google Scholar
61. Corbit, LH, Balleine, BW. Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer. J Neurosci. 2005; 25(4): 962–970.Google Scholar
62. Berridge, KC. From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur J Neurosci. 2012; 35(7): 1124–1143.Google Scholar
63. Holland, PC, Petrovich, GD. A neural systems analysis of the potentiation of feeding by conditioned stimuli. Physiol Behav. 2005; 86(5): 747–761.Google Scholar
64. Petrovich, GD, Ross, CA, Mody, P, Holland, PC, Gallagher, M. Central, but not basolateral, amygdala is critical for control of feeding by aversive learned cues. J Neurosci. 2009; 29(48): 15205–15212.CrossRefGoogle Scholar
65. Mahler, SV, Berridge, KC. Which cue to “want?” Central amygdala opioid activation enhances and focuses incentive salience on a prepotent reward cue. J Neurosci. 2009; 29(20): 6500–6513.Google Scholar
66. DiFeliceantonio, AG, Berridge, KC. Which cue to “want”? Opioid stimulation of central amygdala makes goal-trackers show stronger goal-tracking, just as sign-trackers show stronger sign-tracking. Behav Brain Res. 2012; 230(2): 399–408.Google Scholar
67. Mahler, SV, Berridge, KC. What and when to “want”? Amygdala-based focusing of incentive salience upon sugar and sex. Psychopharmacology (Berl). 2012; 221(3): 407–426.Google Scholar
68. Petrovich, GD, Holland, PC, Gallagher, M. Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J Neurosci. 2005; 25(36): 8295–8302.Google Scholar
69. Petrovich, GD, Ross, CA, Holland, PC, Gallagher, M. Medial prefrontal cortex is necessary for an appetitive contextual conditioned stimulus to promote eating in sated rats. J Neurosci. 2007; 27(24): 6436–6441.Google Scholar
70. Mena, JD, Sadeghian, K, Baldo, BA. Induction of hyperphagia and carbohydrate intake by μ-opioid receptor stimulation in circumscribed regions of frontal cortex. J Neurosci. 2011; 31(9): 3249–3260.Google Scholar
71. Browning, M, Holmes, EA, Murphy, SE, Goodwin, GM, Harmer, CJ. Lateral prefrontal cortex mediates the cognitive modification of attentional bias. Biol Psychiatry. 2010; 67(10): 919–925.CrossRefGoogle ScholarPubMed
72. Chamberlain, SR, Mogg, K, Bradley, BP, et al. Effects of mu opioid receptor antagonism on cognition in obese binge-eating individuals. Psychopharmacology (Berl). 2012; 224(4): 501–509.Google Scholar
73. Murray, E, Brouwer, S, McCutcheon, R, Harmer, CJ, Cowen, PJ, McCabe, C. Opposing neural effects of naltrexone on food reward and aversion: implications for the treatment of obesity. Psychopharmacology (Berl). 2014; 231(22): 4323–4335.Google Scholar
74. Van den Eynde, F, Guillaume, S, Broadbent, H, et al. Neurocognition in bulimic eating disorders: a systematic review. Acta Psychiatr Scand. 2011; 124(2): 120–140.Google Scholar
75. Manasse, SM, Espel, HM, Forman, EM, et al. The independent and interacting effects of hedonic hunger and executive function on binge eating. Appetite. 2015; 89: 16–21.Google Scholar
76. Robinson, TE, Berridge, KC. Incentive-sensitization and addiction. Addict Abingdon Engl. 2001; 96(1): 103–114. doi:10.1080/09652140020016996.Google Scholar
77. Davis, C, Strachan, S, Berkson, M. Sensitivity to reward: implications for overeating and overweight. Appetite. 2004; 42(2): 131–138.Google Scholar
78. Goldfein, JA, Walsh, BT, LaChaussee, JL, Kissileff, HR, Devlin, MJ. Eating behavior in binge eating disorder. Int J Eat Disord. 1993; 14(4): 427–431.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
79. Avena, NM, Rada, P, Hoebel, BG. Sugar bingeing in rats. Curr Protoc Neurosci. 2006; Chapter 9:Unit9.23C.Google ScholarPubMed
80. Avena, NM, Rada, P, Hoebel, BG. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev. 2008; 32(1): 20–39.Google Scholar
81. Boggiano, MM, Chandler, PC, Viana, JB, Oswald, KD, Maldonado, CR, Wauford, PK. Combined dieting and stress evoke exaggerated responses to opioids in binge-eating rats. Behav Neurosci. 2005; 119(5): 1207–1214.Google Scholar
82. Boggiano, MM, Chandler, PC. Binge eating in rats produced by combining dieting with stress. Curr Protoc Neurosci. 2006; Chapter 9:Unit9.23A.CrossRefGoogle ScholarPubMed
83. Micioni Di Bonaventura, MV, Ciccocioppo, R, Romano, A, et al. Role of bed nucleus of the stria terminalis corticotrophin-releasing factor receptors in frustration stress-induced binge-like palatable food consumption in female rats with a history of food restriction. J Neurosci. 2014; 34(34): 11316–11324.CrossRefGoogle ScholarPubMed
84. Hagan, MM, Chandler, PC, Wauford, PK, Rybak, RJ, Oswald, KD. The role of palatable food and hunger as trigger factors in an animal model of stress induced binge eating. Int J Eat Disord. 2003; 34(2): 183–197.Google Scholar
85. Hagan, MM, Wauford, PK, Chandler, PC, Jarrett, LA, Rybak, RJ, Blackburn, K. A new animal model of binge eating: key synergistic role of past caloric restriction and stress. Physiol Behav. 2002; 77(1): 45–54.Google Scholar
86. Piccoli, L, Micioni Di Bonaventura, MV, Cifani, C, et al. Role of orexin-1 receptor mechanisms on compulsive food consumption in a model of binge eating in female rats. Neuropsychopharmacology. 2012; 37(9): 1999–2011.Google Scholar
87. Corwin, RL, Wojnicki, FH, Fisher, JO, Dimitriou, SG, Rice, HB, Young, MA. Limited access to a dietary fat option affects ingestive behavior but not body composition in male rats. Physiol Behav. 1998; 65(3): 545–553.Google Scholar
88. Dimitriou, SG, Rice, HB, Corwin, RL. Effects of limited access to a fat option on food intake and body composition in female rats. Int J Eat Disord. 2000; 28(4): 436–445.Google Scholar
89. Berner, LA, Avena, NM, Hoebel, BG. Bingeing, self-restriction, and increased body weight in rats with limited access to a sweet-fat diet. Obesity (Silver Spring). 2008; 16(9): 1998–2002.Google Scholar
90. Berner, LA, Bocarsly, ME, Hoebel, BG, Avena, NM. Baclofen suppresses binge eating of pure fat but not a sugar-rich or sweet-fat diet. Behav Pharmacol. 2009; 20(7): 631–634.Google Scholar
91. Cottone, P, Wang, X, Park, JW, et al. Antagonism of sigma-1 receptors blocks compulsive-like eating. Neuropsychopharmacology. 2012; 37(12): 2593–2604.Google Scholar