Hostname: page-component-5db58dd55d-h5th4 Total loading time: 0 Render date: 2026-06-13T03:52:28.988Z Has data issue: false hasContentIssue false
  • English
  • Français

Insights revealed by rodent models of sugar binge eating

Published online by Cambridge University Press:  29 October 2015

Susan M. Murray ,
Alastair J. Tulloch ,
Eunice Y. Chen  and
Nicole M. Avena
Susan M. Murray
Affiliation:
Department of Pharmacology and Systems Therapeutics, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Alastair J. Tulloch
Affiliation:
Department of Pharmacology and Systems Therapeutics, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Eunice Y. Chen
Affiliation:
Department of Clinical Psychology, Temple University, Philadelphia, Pennsylvania, USA
Nicole M. Avena*
Affiliation:
Department of Pharmacology and Systems Therapeutics, Icahn School of Medicine at Mount Sinai, New York, New York, USA
*
*Address for correspondence: Nicole M. Avena, PhD, Mount Sinai-St. Luke’s, 1111 Amsterdam Ave., 10th Floor, New York, NY 10025, USA. (Email: nicole.avena@mssm.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Binge eating is seen across the spectrum of eating disorder diagnoses as well as among individuals who do not meet diagnostic criteria. Analyses of the specific types of foods that are frequently binged upon reveal that sugar-rich items feature prominently in binge-type meals, making the effects of binge consumption of sugar an important focus of study. One avenue to do this involves the use of animal models. Foundational and recent studies of animal models of sugar bingeing, both outlined here, lend insight into the various neurotransmitters and neuropeptides that may participate in or be altered by this behavior. Further, several preclinical studies incorporating sugar bingeing paradigms have explored the utility of pharmacological agents that target such neural systems for reducing sugar bingeing in an effort to enhance clinical treatment. Indeed, the translational implications of findings generated using animal models of sugar bingeing are considered here, along with potential avenues for further study.

Keywords

Animal modelbingeingpharmacological treatmentsugartranslational research

Information

Type
Review Articles
Information
CNS Spectrums , Volume 20 , Special Issue 6: Binge Eating Disorder Differentiating from General Obesity , December 2015 , pp. 530 - 536
Copyright
© Cambridge University Press 2015 

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.)

Article purchase

Temporarily unavailable

Footnotes

The authors acknowledge NIH grant DA-03123 (NMA), Gilead Sciences, Inc. (NMA), and NIH grant 1R21MH093932-01A1 (EYC).

References

1. Coker, EL, von Lojewski, A, Luscombe, GM, Abraham, SF. The difficulty in defining binge eating in obese women: how it affects prevalence levels in presurgical bariatric patients. Eat Behav. 2015; 17: 130–135.CrossRefGoogle ScholarPubMed
2. Abraham, TM, Massaro, JM, Hoffmann, U, Yanovski, JA, Fox, CS. Metabolic characterization of adults with binge eating in the general population: the Framingham Heart Study. Obesity. 2014; 22(11): 2441–2449.Google Scholar
3. Striegel, RH, Bedrosian, R, Wang, C, Schwartz, S. Why men should be included in research on binge eating: results from a comparison of psychosocial impairment in men and women. Int J Eat Disord. 2012; 45(2): 233–240.CrossRefGoogle ScholarPubMed
4. 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.Google Scholar
5. Hadigan, CM, Kissileff, HR, Walsh, BT. Patterns of food selection during meals in women with bulimia. Am J Clin Nutr. 1989; 50(4): 759–766.CrossRefGoogle ScholarPubMed
6. Dalton, M, Blundell, J, Finlayson, G. Effect of BMI and binge eating on food reward and energy intake: further evidence for a binge eating subtype of obesity. Obes Facts. 2013; 6(4): 348–359.Google Scholar
7. 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
8. Corwin, RL, Avena, NM, Boggiano, MM. Feeding and reward: perspectives from three rat models of binge eating. Physiol Behav. 2011; 104(1): 87–97.CrossRefGoogle ScholarPubMed
9. Wojnicki, FH, Stine, JG, Corwin, RL. Liquid sucrose bingeing in rats depends on the access schedule, concentration and delivery system. Physiol Behav. 2007; 92(4): 566–574.CrossRefGoogle ScholarPubMed
10. Boggiano, MM, Chandler, PC. Binge eating in rats produced by combining dieting with stress. Curr Protoc Neurosci. 2006. Chapter 9:Unit9.23A.Google Scholar
11. Colantuoni, C, Schwenker, J, McCarthy, J, et al. Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. Neuroreport. 2001; 12(16): 3549–3552.Google Scholar
12. 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.CrossRefGoogle ScholarPubMed
13. Avena, NM, Bocarsly, ME. Dysregulation of brain reward systems in eating disorders: neurochemical information from animal models of binge eating, bulimia nervosa, and anorexia nervosa. Neuropharmacology. 2012; 63(1): 87–96.Google Scholar
14. Ikemoto, S, Panksepp, J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev. 1999; 31(1): 6–41.Google Scholar
15. Bassareo, V, Cucca, F, Musio, P, Lecca, D, Frau, R, Di Chiara, G. Nucleus accumbens shell and core dopamine responsiveness to sucrose in rats: role of response contingency and discriminative/conditioned cues. Eur J Neurosci. 2015; 41(6): 802–809.CrossRefGoogle ScholarPubMed
16. Rada, P, Avena, NM, Hoebel, BG. Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience. 2005; 134(3): 737–744.Google Scholar
17. Pothos, E, Rada, P, Mark, GP, Hoebel, BG. Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone-precipitated withdrawal and clonidine treatment. Brain Res. 1991; 566(1–2): 348–350.Google Scholar
18. Bassareo, V, Di Chiara, G. Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation to motivational state. Eur J Neurosci. 1999; 11(12): 4389–4397.Google Scholar
19. Avena, NM, Rada, P, Moise, N, Hoebel, BG. Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience. 2006; 139(3): 813–820.CrossRefGoogle ScholarPubMed
20. Spangler, R, Wittkowski, KM, Goddard, NL, Avena, NM, Hoebel, BG, Leibowitz, SF. Opiate-like effects of sugar on gene expression in reward areas of the rat brain. Brain Res Mol Brain Res. 2004; 124(2): 134–142.Google Scholar
21. Spangler, R, Goddard, NL, Avena, NM, Hoebel, BG, Leibowitz, SF. Elevated D3 dopamine receptor mRNA in dopaminergic and dopaminoceptive regions of the rat brain in response to morphine. Brain Res Mol Brain Res. 2003; 111(1–2): 74–83.Google Scholar
22. Georges, F, Stinus, L, Bloch, B, Le Moine, C. Chronic morphine exposure and spontaneous withdrawal are associated with modifications of dopamine receptor and neuropeptide gene expression in the rat striatum. Eur J Neurosci. 1999; 11(2): 481–490.Google Scholar
23. Avena, NM, Rada, PV. Cholinergic modulation of food and drug satiety and withdrawal. Physiol Behav. 2012; 106(3): 332–336.CrossRefGoogle ScholarPubMed
24. Mark, GP, Rada, P, Pothos, E, Hoebel, BG. Effects of feeding and drinking on acetylcholine release in the nucleus accumbens, striatum, and hippocampus of freely behaving rats. J Neurochem. 1992; 58(6): 2269–2274.CrossRefGoogle ScholarPubMed
25. Pratt, WE, Blackstone, K. Nucleus accumbens acetylcholine and food intake: decreased muscarinic tone reduces feeding but not food-seeking. Behav Brain Res. 2009; 198(1): 252–257.Google Scholar
26. Avena, NM, Rada, P, Hoebel, BG. Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose. Neuroscience. 2008; 156(4): 865–871.Google Scholar
27. Colantuoni, C, Rada, P, McCarthy, J, et al. Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res. 2002; 10(6): 478–488.CrossRefGoogle ScholarPubMed
28. Avena, NM, Bocarsly, ME, Rada, P, Kim, A, Hoebel, BG. After daily bingeing on a sucrose solution, food deprivation induces anxiety and accumbens dopamine/acetylcholine imbalance. Physiol Behav. 2008; 94(3): 309–315.Google Scholar
29. Wideman, CH, Nadzam, GR, Murphy, HM. Implications of an animal model of sugar addiction, withdrawal and relapse for human health. Nutr Neurosci. 2005; 8(5–6): 269–276.Google Scholar
30. Rada, P, Johnson, DF, Lewis, MJ, Hoebel, BG. In alcohol-treated rats, naloxone decreases extracellular dopamine and increases acetylcholine in the nucleus accumbens: evidence of opioid withdrawal. Pharmacol Biochem Behav. 2004; 79(4): 599–605.CrossRefGoogle ScholarPubMed
31. Avena, NM, Hoebel, BG. A diet promoting sugar dependency causes behavioral cross-sensitization to a low dose of amphetamine. Neuroscience. 2003; 122(1): 17–20.Google Scholar
32. Avena, NM, Carrillo, CA, Needham, L, Leibowitz, SF, Hoebel, BG. Sugar-dependent rats show enhanced intake of unsweetened ethanol. Alcohol. 2004; 34(2–3): 203–209.Google Scholar
33. Meisch, RA, Thompson, T. Ethanol intake as a function of concentration during food deprivation and satiation. Pharmacol Biochem Behav. 1974; 2(5): 589–596.CrossRefGoogle ScholarPubMed
34. Bello, NT, Sweigart, KL, Lakoski, JM, Norgren, R, Hajnal, A. Restricted feeding with scheduled sucrose access results in an upregulation of the rat dopamine transporter. Am J Physiol Regul Integr Comp Physiol. 2003; 284(5): R1260–R1268.Google Scholar
35. Bello, NT, Lucas, LR, Hajnal, A. Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport. 2002; 13(12): 1575–1578.Google Scholar
36. Bake, T, Duncan, JS, Morgan, DG, Mercer, JG. Arcuate nucleus homeostatic systems are not altered immediately prior to the scheduled consumption of large, binge-type meals of palatable solid or liquid diet in rats and Mice. Journal Neuroendocrinol. 2013; 25(4): 357–371.CrossRefGoogle ScholarPubMed
37. Alcaraz-Iborra, M, Carvajal, F, Lerma-Cabrera, JM, Valor, LM, Cubero, I. Binge-like consumption of caloric and non-caloric palatable substances in ad libitum-fed C57BL/6J mice: pharmacological and molecular evidence of orexin involvement. Behav Brain Res. 2014; 272: 93–99.CrossRefGoogle ScholarPubMed
38. Olney, JJ, Navarro, M, Thiele, TE. Binge-like consumption of ethanol and other salient reinforcers is blocked by orexin-1 receptor inhibition and leads to a reduction of hypothalamic orexin immunoreactivity. Alcohol Clin Exp Res. 2015; 39(1): 21–29.CrossRefGoogle ScholarPubMed
39. 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
40. Yasoshima, Y, Shimura, T. A mouse model for binge-like sucrose overconsumption: contribution of enhanced motivation for sweetener consumption. Physiol Behav. 2015; 138: 154–164.Google Scholar
41. Corwin, RL, Wojnicki, FH. Baclofen, raclopride, and naltrexone differentially affect intake of fat and sucrose under limited access conditions. Behav Pharmacol. 2009; 20(5–6): 537–548.Google Scholar
42. Bello, NT, Hajnal, A. Acute methylphenidate treatments reduce sucrose intake in restricted-fed bingeing rats. Brain Res Bull. 2006; 70(4–6): 422–429.CrossRefGoogle ScholarPubMed
43. Yao, L, Fan, P, Arolfo, M, et al. Inhibition of aldehyde dehydrogenase-2 suppresses cocaine seeking by generating THP, a cocaine use-dependent inhibitor of dopamine synthesis. Nature Med. 2010; 16(9): 1024–1028.Google Scholar
44. Bocarsly, ME, Hoebel, BG, Paredes, D, et al. GS 455534 selectively suppresses binge eating of palatable food and attenuates dopamine release in the accumbens of sugar-bingeing rats. Behav Pharmacol. 2014; 25(2): 147–157.CrossRefGoogle ScholarPubMed
45. Avena, NM, Bocarsly, ME, Murray, S, Gold, MS. Effects of baclofen and naltrexone, alone and in combination, on the consumption of palatable food in male rats. Exp Clin Psychopharmacol. 2014; 22(5): 460–467.CrossRefGoogle ScholarPubMed
46. Marazziti, D, Corsi, M, Baroni, S, Consoli, G, Catena-Dell’Osso, M. Latest advancements in the pharmacological treatment of binge eating disorder. Eur Rev Med Pharmacol Sci. 2012; 16(15): 2102–2107.Google Scholar
47. Hilbert, A, Pike, KM, Goldschmidt, AB, et al. Risk factors across the eating disorders. Psychiatry Res. 2014; 220(1): 500–506.CrossRefGoogle ScholarPubMed
48. Reas, DL, Grilo, CM. Timing and sequence of the onset of overweight, dieting, and binge eating in overweight patients with binge eating disorder. Int J Eat Disord. 2007; 40(2): 165–170.Google Scholar
49. Wang, G-J, Geliebter, A, Volkow, ND, et al. Enhanced striatal dopamine release during food stimulation in binge eating disorder. Obesity (Silver Spring). 2011; 19(8): 1601–1608.Google Scholar
50. Geliebter, A, Ladell, T, Logan, M, Schweider, T, Sharafi, M, Hirsch, J. Responsivity to food stimuli in obese and lean binge eaters using functional MRI. Appetite. 2006; 46(1): 31–35.Google Scholar
51. Grant, JE, Schreiber, LR, Odlaug, BL. Phenomenology and treatment of behavioural addictions. Can J Psychiatry. 2013; 58(5): 252–259.Google Scholar
52. Ivezaj, V, Saules, KK, Wiedemann, AA. “I didn’t see this coming.”: why are postbariatric patients in substance abuse treatment? Patients’ perceptions of etiology and future recommendations. Obes Surg. 2012; 22(8): 1308–1314.Google Scholar
53. Spring, B, Wurtman, J, Gleason, R, Wurtman, R, Kessler, K. Weight gain and withdrawal symptoms after smoking cessation: a preventive intervention using d-fenfluramine. Health Psychol. 1991; 10(3): 216–223.CrossRefGoogle ScholarPubMed
54. Helmers, K, Young, S. The effect of sucrose on acute tobacco withdrawal in women. Psychopharmacology (Berl). 1998; 139(3): 217–221.CrossRefGoogle ScholarPubMed
55. Sysko, R, Devlin, MJ, Walsh, BT, Zimmerli, E, Kissileff, HR. Satiety and test meal intake among women with binge eating disorder. Int J Eat Disord. 2007; 40(6): 554–561.CrossRefGoogle ScholarPubMed
56. Mirch, MC, McDuffie, JR, Yanovski, SZ, et al. Effects of binge eating on satiation, satiety, and energy intake of overweight children. Am J Clin Nutr. 2006; 84(4): 732–738.Google Scholar
57. Geliebter, A, Hashim, SA, Gluck, ME. Appetite-related gut peptides, ghrelin, PYY, and GLP-1 in obese women with and without binge eating disorder (BED). Physiol Behav. 2008; 94(5): 696–699.Google Scholar
58. Munsch, S, Biedert, E, Meyer, AH, Herpertz, S, Beglinger, C. CCK, ghrelin, and PYY responses in individuals with binge eating disorder before and after a cognitive behavioral treatment (CBT). Physiol Behav. 2009; 97(1): 14–20.Google Scholar
59. Herman, CP, Mack, D. Restrained and unrestrained eating. J Pers. 1975; 43(4): 647–660.CrossRefGoogle ScholarPubMed
60. Fairburn, CG, Cooper, Z, Shafran, R. Cognitive behaviour therapy for eating disorders: a “transdiagnostic” theory and treatment. Behav Res Ther. 2003; 41(5): 509–528.Google Scholar
61. Wilson, GT, Wilfley, DE, Agras, WS, Bryson, SW. Psychological treatments of binge eating disorder. Arch Gen Psychiatry. 2010; 67(1): 94–101.Google Scholar
62. Goldschmidt, AB, Crosby, RD, Cao, L, et al. Ecological momentary assessment of eating episodes in obese adults. Psychosom Med. 2014; 76(9): 747–752.Google Scholar
63. Schulz, S, Laessle, R. Stress-induced laboratory eating behavior in obese women with binge eating disorder. Appetite. 2012; 58(2): 457–461.Google Scholar
64. Haedt-Matt, AA, Keel, PK. Revisiting the affect regulation model of binge eating: a meta-analysis of studies using ecological momentary assessment. Psychol Bull. 2011; 137(4): 660–681.Google Scholar