Animal Models of Sugar and Fat Bingeing: Relationship to Food Addiction and Increased Body Weight

  • Nicole M. Avena
  • Miriam E. Bocarsly
  • Bartley G. Hoebel
Part of the Methods in Molecular Biology book series (MIMB, volume 829)

Abstract

Binge eating is a behavior that occurs in some eating disorders, as well as in obesity and in nonclinical populations. Both sugars and fats are readily consumed by human beings and are common components of binges. This chapter describes animal models of sugar and fat bingeing, which allow for a detailed analysis of these behaviors and their concomitant physiological effects. The model of sugar bingeing has been used successfully to elicit behavioral and neurochemical signs of dependence in rats; e.g., indices of opiate-like withdrawal, increased intake after abstinence, cross-sensitization with drugs of abuse, and the repeated release of dopamine in the nucleus accumbens following repeated bingeing. Studies using the model of fat bingeing suggest that it can produce some, but not all, of the signs of dependence that are seen with sugar binge eating, as well as increase body weight, potentially leading to obesity.

Key words

Binge eating Dopamine Fat Food addiction Nucleus accumbens Sugar Body weight 

References

  1. 1.
    Hudson, J. I., Hiripi, E., Pope, H. G., Jr., and Kessler, R. C. (2007) The prevalence and correlates of eating disorders in the national comorbidity survey replication. Biol Psychiatry 61, 348–58.PubMedCrossRefGoogle Scholar
  2. 2.
    Ogden, C. L., Yanovski, S. Z., Carroll, M. D., and Flegal, K. M. (2007) The epidemiology of obesity. Gastroenterology 132, 2087–102.PubMedCrossRefGoogle Scholar
  3. 3.
    Stunkard, A. J. (1959) Eating patterns and obesity. Psychiatr Q 33, 284–95.PubMedCrossRefGoogle Scholar
  4. 4.
    Tanofsky-Kraff, M., Cohen, M. L., Yanovski, S. Z., Cox, C., Theim, K. R., Keil, M., Reynolds, J. C., and Yanovski, J. A. (2006) A prospective study of psychological predictors of body fat gain among children at high risk for adult obesity. Pediatrics 117, 1203–9.PubMedCrossRefGoogle Scholar
  5. 5.
    Ramacciotti, C. E., Coli, E., Paoli, R., Gabriellini, G., Schulte, F., Castrogiovanni, S., Dell’Osso, L., and Garfinkel, P. E. (2005) The relationship between binge eating disorder and non-purging bulimia nervosa. Eat Weight Disord 10, 8–12.PubMedGoogle Scholar
  6. 6.
    Grucza, R. A., Przybeck, T. R., and Cloninger, C. R. (2007) Prevalence and correlates of binge eating disorder in a community sample. Compr Psychiatry 48, 124–31.PubMedCrossRefGoogle Scholar
  7. 7.
    Galanti, K., Gluck, M. E., and Geliebter, A. (2007) Test meal intake in obese binge eaters in relation to impulsivity and compulsivity. Int J Eat Disord 40, 727–32.PubMedCrossRefGoogle Scholar
  8. 8.
    Yudkin, J. (1972) Sweet and Dangerous, Peter H. Wyden, Inc, New York.Google Scholar
  9. 9.
    Bray, G. A., York, B., and DeLany, J. (1992) A survey of the opinions of obesity experts on the causes and treatment of obesity. Am J Clin Nutr 55, 151S–54S.PubMedGoogle Scholar
  10. 10.
    Bray, G. A., and Popkin, B. M. (1998) Dietary fat intake does affect obesity! Am J Clin Nutr 68, 1157–73.PubMedGoogle Scholar
  11. 11.
    Avena, N., Rada, P., and Hoebel, B. (2006) Unit 9.23C Sugar bingeing in rats, in “Current Protocols in Neuroscience” (Crawley, J., Gerfen, C., Rogawski, M., Sibley, D., Skolnick, P., and Wray, S., Eds.), John Wiley & Sons, Inc., Indianapolis pp. 9.23C.1–9.23C.6.Google Scholar
  12. 12.
    Avena, N. M., Rada, P., and Hoebel, B. G. (2008) Evidence of sugar addiction: Behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32, 20–39.Google Scholar
  13. 13.
    Hoebel, B. G. (1985) Brain neurotransmitters in food and drug reward. Am J Clin Nutr 42, 1133–50.PubMedGoogle Scholar
  14. 14.
    Hernandez, L., and Hoebel, B. G. (1988) Feeding and hypothalamic stimulation increase dopamine turnover in the accumbens. Physiol Behav 44, 599–606.PubMedCrossRefGoogle Scholar
  15. 15.
    Kelley, A. E., Bakshi, V. P., Haber, S. N., Steininger, T. L., Will, M. J., and Zhang, M. (2002) Opioid modulation of taste hedonics within the ventral striatum. Physiol Behav 76, 365–77.PubMedCrossRefGoogle Scholar
  16. 16.
    Le Magnen, J. (1990) A role for opiates in food reward and food addiction, in “Taste, Experience, and Feeding” (Capaldi, P. T., Ed.), American Psychological Association, Washington, D. C. pp. 241–52.CrossRefGoogle Scholar
  17. 17.
    Volkow, N. D., and Wise, R. A. (2005) How can drug addiction help us understand obesity? Nat Neurosci 8, 555–60.PubMedCrossRefGoogle Scholar
  18. 18.
    Wise, R. A. (1989) Opiate reward: sites and substrates. Neurosci Biobehav Rev 13, 129–33.PubMedCrossRefGoogle Scholar
  19. 19.
    Ahmed, S. H., and Koob, G. F. (1998) Transition from moderate to excessive drug intake: change in hedonic set point. Science 282, 298–300.PubMedCrossRefGoogle Scholar
  20. 20.
    Heyser, C. J., Schulteis, G., and Koob, G. F. (1997) Increased ethanol self-administration after a period of imposed ethanol deprivation in rats trained in a limited access paradigm. Alcohol Clin Exp Res 21, 784–91.PubMedCrossRefGoogle Scholar
  21. 21.
    Avena, N. M., Carrillo, C. A., Needham, L., Leibowitz, S. F., and Hoebel, B. G. (2004) Sugar-dependent rats show enhanced intake of unsweetened ethanol. Alcohol 34, 203–9.PubMedCrossRefGoogle Scholar
  22. 22.
    Avena, N. M., and Hoebel, B. G. (2003) A diet promoting sugar dependency causes behavioral cross-sensitization to a low dose of amphetamine. Neuroscience 122, 17–20.PubMedCrossRefGoogle Scholar
  23. 23.
    Avena, N. M., and Hoebel, B. G. (2003) Amphetamine-sensitized rats show sugar-induced hyperactivity (cross-sensitization) and sugar hyperphagia. Pharmacol Biochem Behav 74, 635–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Colantuoni, C., Rada, P., McCarthy, J., Patten, C., Avena, N. M., Chadeayne, A., and Hoebel, B. G. (2002) Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res 10, 478–88.PubMedCrossRefGoogle Scholar
  25. 25.
    Colantuoni, C., Schwenker, J., McCarthy, J., Rada, P., Ladenheim, B., Cadet, J. L., Schwartz, G. J., Moran, T. H., and Hoebel, B. G. (2001) Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. Neuroreport 12, 3549–52.PubMedCrossRefGoogle Scholar
  26. 26.
    Gosnell, B. A. (2005) Sucrose intake enhances behavioral sensitization produced by cocaine. Brain Res 1031, 194–201.PubMedCrossRefGoogle Scholar
  27. 27.
    Grimm, J. W., Fyall, A. M., and Osincup, D. P. (2005) Incubation of sucrose craving: effects of reduced training and sucrose pre-loading. Physiol Behav 84, 73–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Rada, P., Avena, N. M., and Hoebel, B. G. (2005) Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 134, 737–44.PubMedCrossRefGoogle Scholar
  29. 29.
    Wideman, C. H., Nadzam, G. R., and Murphy, H. M. (2005) Implications of an animal model of sugar addiction, withdrawal and relapse for human health. Nutr Neurosci 8, 269–76.PubMedCrossRefGoogle Scholar
  30. 30.
    Spangler, R., Wittkowski, K. M., Goddard, N. L., Avena, N. M., Hoebel, B. G., and Leibowitz, S. F. (2004) Opiate-like effects of sugar on gene expression in reward areas of the rat brain. Brain Res Mol Brain Res 124, 134–42.PubMedCrossRefGoogle Scholar
  31. 31.
    Hernandez, L., and Hoebel, B. G. (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42, 1705–12.PubMedCrossRefGoogle Scholar
  32. 32.
    Hoebel, B. G., Hernandez, L., Schwartz, D. H., Mark, G. P., and Hunter, G. A. (1989) Microdialysis studies of brain norepinephrine, serotonin, and dopamine release during ingestive behavior: theoretical and clinical implications, in “The Psychobiology of Human Eating Disorders: Preclinical and Clinical Perspectives” (Schneider, L. H., Cooper, S. J., and Halmi, K. A., Eds.), Annals of the New York Academy of Sciences, New York. pp.171–91.Google Scholar
  33. 33.
    Koob, G. F. (1999) Drug reward and addiction, in “Fundamental Neuroscience” (Zigmond, M., Bloom, F. E., Landis, S. C., Roberts, J. L., and Squire, L. R., Eds.), Academic Press, San Diego pp. 1254–79.Google Scholar
  34. 34.
    Wise, R. A. (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend 51, 13–22.PubMedCrossRefGoogle Scholar
  35. 35.
    Wise, R. A. (1997) Drug self-administration viewed as ingestive behaviour. Appetite 28, 1–5.PubMedCrossRefGoogle Scholar
  36. 36.
    Avena, N. M., Rada, P., Moise, N., and Hoebel, B. G. (2006) Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 139, 813–20.PubMedCrossRefGoogle Scholar
  37. 37.
    Bassareo, V., and Di Chiara, G. (1997) Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum. J Neurosci 17, 851–61.PubMedGoogle Scholar
  38. 38.
    Avena, N. M., Bocarsly, M. E., Kim, A., Rada, P., and Hoebel, B. G. (2008) After daily bingeing on a sucrose solution, prolonged food deprivation induces anxiety and accumbens dopamine/acetylcholine imbalance. Physiol Behav 94, 309–15.Google Scholar
  39. 39.
    Rada, P., Jensen, K., and Hoebel, B. G. (2001) Effects of nicotine and mecamylamine-induced withdrawal on extracellular dopamine and acetylcholine in the rat nucleus accumbens. Psychopharmacology (Berl) 157, 105–10.CrossRefGoogle Scholar
  40. 40.
    Rada, P., Johnson, D. F., Lewis, M. J., and Hoebel, B. G. (2004) In alcohol-treated rats, naloxone decreases extracellular dopamine and increases acetylcholine in the nucleus accumbens: evidence of opioid withdrawal. Pharmacol Biochem Behav 79, 599–605.PubMedCrossRefGoogle Scholar
  41. 41.
    Rada, P., Pothos, E., Mark, G. P., and Hoebel, B. G. (1991) Microdialysis evidence that acetylcholine in the nucleus accumbens is involved in morphine withdrawal and its treatment with clonidine. Brain Res 561, 354–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Rada, P. V., Mark, G. P., Taylor, K. M., and Hoebel, B. G. (1996) Morphine and naloxone, i.p. or locally, affect extracellular acetylcholine in the accumbens and prefrontal cortex. Pharmacol Biochem Behav 53, 809–16.PubMedCrossRefGoogle Scholar
  43. 43.
    Avena, N. M., Long, K. A., and Hoebel, B. G. (2005) Sugar-dependent rats show enhanced responding for sugar after abstinence: evidence of a sugar deprivation effect. Physiol Behav 84, 359–62.PubMedCrossRefGoogle Scholar
  44. 44.
    American Psychiatric Association (2000) Diag­nostic and Statistical Manual of Mental Disorders Fourth Edition Text Revision (DSM-IV-TR), American Psychiatric Association, Washington, DC.Google Scholar
  45. 45.
    Corwin, R. L., Wojnicki, F. H., Fisher, J. O., Dimitriou, S. G., Rice, H. B., and Young, M. A. (1998) Limited access to a dietary fat option affects ingestive behavior but not body composition in male rats. Physiol Behav 65, 545–53.PubMedCrossRefGoogle Scholar
  46. 46.
    Dimitriou, S. G., Rice, H. B., and Corwin, R. L. (2000) Effects of limited access to a fat option on food intake and body composition in female rats. Int J Eat Disord 28, 436–45.PubMedCrossRefGoogle Scholar
  47. 47.
    Boggiano, M. M., Chandler, P. C., Viana, J. B., Oswald, K. D., Maldonado, C. R., and Wauford, P. K. (2005) Combined dieting and stress evoke exaggerated responses to opioids in binge-eating rats. Behav Neurosci 119, 1207–14.PubMedCrossRefGoogle Scholar
  48. 48.
    Boggiano, M. M., and Chandler, P. C. (2006) Binge eating in rats produced by combining dieting with stress. Curr Protoc Neurosci Chapter 9, Unit9 23A.Google Scholar
  49. 49.
    Berner, L. A., Avena, N. M., and Hoebel, B. G. (2008) Bingeing, Self-restriction, and Increased Body Weight in Rats With Limited Access to a Sweet-fat Diet. Obesity (Silver Spring) 16, 1998–2002.Google Scholar
  50. 50.
    Berner, L. A., Bocarsly, M. E., Hoebel, B. G., and Avena, N. M. (2009) Baclofen suppresses binge eating of pure fat but not a sugar-rich or sweet-fat diet. Behav Pharmacol 20, 631–4.Google Scholar
  51. 51.
    Allison, S., and Timmerman, G. M. (2007) Anatomy of a binge: food environment and characteristics of nonpurge binge episodes. Eat Behav 8, 31–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Guertin, T. L., and Conger, A. J. (1999) Mood and forbidden foods’ influence on perceptions of binge eating. Addict Behav 24, 175–93.PubMedCrossRefGoogle Scholar
  53. 53.
    Hadigan, C. M., Kissileff, H. R., and Walsh, B. T. (1989) Patterns of food selection during meals in women with bulimia. Am J Clin Nutr 50, 759–66.PubMedGoogle Scholar
  54. 54.
    Kales, E. F. (1990) Macronutrient analysis of binge eating in bulimia. Physiol Behav 48, 837–40.PubMedCrossRefGoogle Scholar
  55. 55.
    Kelley, A. E., Will, M. J., Steininger, T. L., Zhang, M., and Haber, S. N. (2003) Restricted daily consumption of a highly palatable food (chocolate Ensure(R)) alters striatal enkephalin gene expression. Eur J Neurosci 18, 2592–8.PubMedCrossRefGoogle Scholar
  56. 56.
    Liang, N. C., Hajnal, A., and Norgren, R. (2006) Sham feeding corn oil increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 291, R1236–9.Google Scholar
  57. 57.
    Teegarden, S. L., and Bale, T. L. (2007) Decreases in dietary preference produce increased emotionality and risk for dietary relapse. Biol Psychiatry 61, 1021–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Teegarden, S. L., Nestler, E. J., and Bale, T. L. (2008) Delta FosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol Psychiatry 64, 941–50.PubMedCrossRefGoogle Scholar
  59. 59.
    Johnson, P. M., and Kenny, P. J. (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13, 635–41.Google Scholar
  60. 60.
    Cottone, P., Sabino, V., Steardo, L., and Zorrilla, E. P. (2009) Consummatory, anxiety-related and metabolic adaptations in female rats with alternating access to preferred food. Psychoneuroendocrinology 34, 38–49.PubMedCrossRefGoogle Scholar
  61. 61.
    Corwin, R. L., and Buda-Levin, A. (2004) Behavioral models of binge-type eating. Physiol Behav 82, 123–30.PubMedCrossRefGoogle Scholar
  62. 62.
    Mazda, T., Yamamoto, H., Fujimura, M., and Fujimiya, M. (2004) Gastric distension-induced release of 5-HT stimulates c-fos expression in specific brain nuclei via 5-HT3 receptors in conscious rats. Am J Physiol Gastrointest Liver Physiol 287, G228–35.PubMedCrossRefGoogle Scholar
  63. 63.
    Avena, N. M., Rada, P., and Hoebel, B. G. (2008) Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose. Neuroscience 156, 865–71.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Nicole M. Avena
    • 1
    • 2
  • Miriam E. Bocarsly
    • 2
  • Bartley G. Hoebel
    • 2
  1. 1.Department of Psychiatry, McKnight Brain InstituteUniversity of FloridaGainesvilleUSA
  2. 2.Department of Psychology, Princeton Neuroscience InstitutePrinceton UniversityPrincetonUSA

Personalised recommendations