The Relationship Between Drugs of Abuse and Palatable Foods: Pre-clinical Evidence Towards a Better Understanding of Addiction-Like Behaviors

  • Renata B. M. Duarte
  • Aline Caron Borges
  • Marilia Barros
Chapter

Abstract

Food is essential for the survival of all animals, yet ingestive behavior varies significantly between species. In humans, obesity and related pathologies are currently considered a public health issue, having attained global epidemic proportions. Therefore, a better understanding of its etiology may help improve treatment strategies, as well as promote large-scale social changes. In this sense, this chapter discusses mainly “food addiction” within the current framework of eating-related disorders. We first review the two main neurophysiological mechanisms that regulate ingestive behaviors: (i) the homeostatic drive, which, via activation of specific hormones, increases or inhibits food intake according to endogenous energy deposits; and (ii) the hedonic drive, which is related to the subjective pleasurable experiences associated with food and acts independent of the body’s energy stores. We then focus on the main concepts and characteristics of “food addiction,” with the development of food-related binge-like and craving behaviors that may be induced when the hedonic drive “overrides” the homeostatic system. Several behavioral criteria currently used to define drug addiction can be readily transposed to those related to eating disorders. At the neurobiological level, similar underlying neural pathways are activated and/or altered by compulsive-like drug and food intake. The behavioral and neurobiological overlap is discussed, with an emphasis on pre-clinical evidence, particularly between binge-eating disorders and drug addiction. Different animal models, their advantages and translational limitations to human pathologies are then discussed.

Keywords

Food addiction Binge eating Reward Animal models 

Notes

Acknowledgments

The writing of this chapter was supported by CNPq (478930/2012-7) and FAP-DF (193.001.026/2015). R.B.M.D. received a doctoral fellowship from CNPq and M.B. a research fellowship from CNPq (304041/2015-7).

References

  1. 1.
    Volkow ND, Wise RA. How can drug addiction help us understand obesity? Nat Neurosci. 2005;8:555–60.PubMedCrossRefGoogle Scholar
  2. 2.
    Saper CB, Chou TC, Elmquist JK. The need to feed: homeostatic and hedonic control of eating. Neuron. 2002;36:199–211.PubMedCrossRefGoogle Scholar
  3. 3.
    Sternson SM, Nicholas Betley J, Cao ZF. Neural circuits and motivational processes for hunger. Curr Opin Neurobiol. 2013;23:353–60.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Mustajoki P. Obesegenic food environment explains most of the obesity epidemic. Duodecim. 2015;131:1345–52.Google Scholar
  5. 5.
    Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends in obesity among US adults, 1999-2008. JAMA. 2010;303:235–41.PubMedCrossRefGoogle Scholar
  6. 6.
    Rodin J, Mancuso J, Granger J, Nelbach E. Food cravings in relation to body mass index, restraint, and estradiol levels: a repeated measures study in healthy women. Appetite. 1991;17:177–85.PubMedCrossRefGoogle Scholar
  7. 7.
    Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93:359–404.PubMedCrossRefGoogle Scholar
  8. 8.
    Finkelstein EA, Trogdon JG, Cohen JW, Dietz W. Annual medical spending attributable to obesity: payer- and service-specific estimates. Health Aff. 2009;28:822–31.CrossRefGoogle Scholar
  9. 9.
    Fontaine KR, Redden DT, Wang C, Westfall AO, Allison DB. Years of life lost due to obesity. JAMA. 2003;289:187–93.PubMedCrossRefGoogle Scholar
  10. 10.
    Berridge KC, Ho CY, Richard JM, DiFeliceantonio AG. The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res. 2010;1350:43–64.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Gasbarri A, Pompili A, Packard MG, Tomaz C. Habit learning and memory in mammals: behavioral and neural characteristics. Neurobiol Learn Mem. 2014;114:198–208.PubMedCrossRefGoogle Scholar
  12. 12.
    APA – American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-V). 5th ed. Washington, DC: American Psychiatric Association; 2013.CrossRefGoogle Scholar
  13. 13.
    Avena NM, Rada P, Hoebel BG. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev. 2008;32:20–39.PubMedCrossRefGoogle Scholar
  14. 14.
    Davis C, Carter JC. Compulsive overeating as an addiction disorder. A review of theory and evidence. Appetite. 2009;53:1–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Gold MS, Frost-Pineda K, Jacobs WS. Overeating, binge eating, and eating disorders as addictions. Psychiatr Ann. 2003;33:117–22.CrossRefGoogle Scholar
  16. 16.
    Jong JW, Vanderschuren LJ, Adan RA. Towards an animal model of food addiction. Obes Facts. 2012;5:180–95.PubMedCrossRefGoogle Scholar
  17. 17.
    Volkow ND, Wang GJ, Fowler JS, Telang F. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci. 2008;363:3191–200.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Wilson GT. Eating disorders, obesity and addiction. Eur Eat Disord Rev. 2010;18:341–51.PubMedCrossRefGoogle Scholar
  19. 19.
    Benoit SC, Tracy AL. Behavioral controls of food intake. Peptides. 2008;29:139–47.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Woods SC. The control of food intake: behavioral versus molecular perspectives. Cell Metab. 2009;9:489–98.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Fulton S. Appetite and reward. Front Neuroendocrinol. 2010;31:85–103.PubMedCrossRefGoogle Scholar
  22. 22.
    Dagher A. Functional brain imaging of appetite. Trends Endocrinol Metab. 2012;23:250–60.PubMedCrossRefGoogle Scholar
  23. 23.
    Strubbe JH, Woods SC. The timing of meals. Psychoanal Rev. 2004;111:128–41.CrossRefGoogle Scholar
  24. 24.
    Woods SC, Lutz TA, Geary N, Langhans W. Pancreatic signals controlling food intake, insulin, glucagon and amylin. Philos Trans R Soc B Biol Sci. 2006;361:1219–35.CrossRefGoogle Scholar
  25. 25.
    Schneeberger M, Gomis R, Claret M. Hypothalamic and brainstem neuronal circuits controlling homeostatic energy balance. J Endocrinol. 2014;220:25–46.CrossRefGoogle Scholar
  26. 26.
    Volkow ND, Wang GJ, Tomasi D, Baler RD. Obesity and addiction: neurobiological overlaps. Obes Rev. 2013;14:2–18.PubMedCrossRefGoogle Scholar
  27. 27.
    Vainik U, Dagher A, Dube L, Fellows LK. Neurobehavioural correlates of body mass index and eating behaviours in adults: a systematic review. Neurosci Biobehav Rev. 2013;37:279–99.PubMedCrossRefGoogle Scholar
  28. 28.
    Dalley JW, Everitt BJ, Robbins TW. Impulsivity, compulsivity, and top-down cognitive control. Neuron. 2011;69:680–94.PubMedCrossRefGoogle Scholar
  29. 29.
    Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley J, Robbins TW. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci. 2008;363:3125–35.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Gautier JF, Chen K, Salbe AD, Bandy D, Pratley RE, Heiman M, Ravussin E, Reiman EM, Tataranni PA. Differential brain responses to satiation in obese and lean men. Diabetes. 2000;49:838–46.PubMedCrossRefGoogle Scholar
  31. 31.
    Gearhardt AN, Yokum S, Orr PT, Stice E, Corbin WR, Brownell KD. Neural correlates of food addiction. Arch Gen Psychiatry. 2011;68:808–16.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Volkow ND, Wang GJ, Baler RD. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci. 2011;15:37–46.PubMedCrossRefGoogle Scholar
  33. 33.
    Morton GJ, Cummings DE, Baskins DG, Barsh GS, Schwartz MV. Central nervous system control of food intake and body weight. Nature. 2006;21:289–95.CrossRefGoogle Scholar
  34. 34.
    Morton GJ, Meek TH, Schwartz MW. Neurobiology of food intake in health and disease. Nat Rev Neurosci. 2014;15:367–78.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Schwartz MW, Woods SC, Porte Jr D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000;404:661–71.PubMedGoogle Scholar
  36. 36.
    Zigman JM, Elmquist JK. From anorexia to obesity — the yin and yang of body weight control. Endocrinology. 2003;144:3749–56.PubMedCrossRefGoogle Scholar
  37. 37.
    Cummings DE, Shannon MH. Roles for ghrelin in the regulation of appetite and body weight. Arch Surg. 2003;138:389–96.PubMedCrossRefGoogle Scholar
  38. 38.
    Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Letters Nature. 1999;402:656–60.CrossRefGoogle Scholar
  39. 39.
    Shigemura N, Ohta R, Kusakabe Y, Miura H, Hino A, Koyano K, Nakashima K, Ninomiya Y. Leptin modulates behavioral responses to sweet substances by influencing peripheral taste structures. Endocrinology. 2004;145:839–47.PubMedCrossRefGoogle Scholar
  40. 40.
    Berridge KC, Kringelbach ML. Pleasure systems in the brain. Neuron. 2015;86:646–64.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Egecioglu E, Skibicka KP, Hansson C, Alvarez-Crespo M, Friberg PA, Jerlhag E, Engel JA, Dickson LS. Hedonic and incentive signals for body weight control. Rev Endocr Metab Disord. 2011;12:141–51.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Castro DC, Berridge KC. Advances in the neurobiological bases for food ‘liking’ versus ‘wanting’. Physiol Behav. 2014;136:22–30.PubMedCrossRefGoogle Scholar
  43. 43.
    Berridge KC, Robinson TE. Parsing reward. Trends Neurosci. 2003;26:507–13.PubMedCrossRefGoogle Scholar
  44. 44.
    Richard JM, Castro DC, Difeliceantonio AG, Robinson MJ, Berridge KC. Mapping brain circuits of reward and motivation: in the footsteps of Ann Kelley. Neurosci Biobehav Rev. 2013;37:1919–31.PubMedCrossRefGoogle Scholar
  45. 45.
    Berthoud HR, Lenard NR, Shin AC. Food reward, hyperphagia, and obesity. Am J Physiol Regul Integr Comp Physiol. 2011;300:1266–77.CrossRefGoogle Scholar
  46. 46.
    Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev. 1998;28:309–69.PubMedCrossRefGoogle Scholar
  47. 47.
    Wise RO. Dopamine, learning and motivation. Nat Rev Neurosci. 2004;5:483–94.PubMedCrossRefGoogle Scholar
  48. 48.
    Zhang M, Gosnell BA, Kelley AE. Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens. J Pharmacol Exp Ther. 1998;285:908–14.PubMedGoogle Scholar
  49. 49.
    Hajnal A, Acharya NK, Grigson PS, Covasa M, Twining RC. Obese OLETF rats exhibit increased operant performance for palatable sucrose solutions and differential sensitivity to D2 receptor antagonism. Am J Physiol Reg Integ Compar Physiol. 2007;293:1846–54.CrossRefGoogle Scholar
  50. 50.
    Westerink BH, Teisman A, De Vries JB. Increase in dopamine release from the nucleus accumbens in response to feeding: a model to study interactions between drugs and naturally activated dopaminergic neurons in the rat brain. Naunyn Schmiedeberg's Arch Pharmacol. 1994;349:230–5.CrossRefGoogle Scholar
  51. 51.
    Volkow ND, Morales M. The brain on drugs: from reward to addiction. Cell. 2015;162:712–25.PubMedCrossRefGoogle Scholar
  52. 52.
    Olsen CM. Natural rewards, neuroplasticity, and non-drug addictions. Neuropharmacology. 2011;61:​1109–22.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Pitchers K, Balfour M, Lehman M. Neuroplasticity in the mesolimbic system induced by natural reward and subsequent reward abstinence. Biol Psychiatry. 2010;67:872–9.PubMedCrossRefGoogle Scholar
  54. 54.
    Weatherford SC, Greenberg D, Gibbs J, Smith GP. The potency of D-1 and D-2 receptor antagonists is inversely related to the reward value of sham-fed corn oil and sucrose in rats. Pharmacol Biochem Behav. 1990;37:317–23.Google Scholar
  55. 55.
    Brownell KD, Gold MS. Food and addiction: a comprehensive handbook. Oxford: Oxford University Press; 2012.CrossRefGoogle Scholar
  56. 56.
    Kenny PJ. Common cellular and molecular mechanisms in obesity and drug addiction. Nat Rev Neurosci. 2011;12:638–51.PubMedCrossRefGoogle Scholar
  57. 57.
    Shafat A, Murray B, Rumsey D. Energy density in cafeteria diet induced hyperphagia in the rat. Appetite. 2009;52:34–8.PubMedCrossRefGoogle Scholar
  58. 58.
    Randolph TG. The descriptive features of food addiction: addictive eating and drinking. Q J Stud Alcohol. 1956;17:198–224.PubMedGoogle Scholar
  59. 59.
    Rogers PJ, Smit HJ. Food craving and food “addiction”: a critical review of the evidence from a biopsychosocial perspective. Pharmacol Biochem Behav. 2000;66:3–14.Google Scholar
  60. 60.
    Meule A. Back by popular demand: a narrative review on the history of food addiction research. Yale J Biol Med. 2015;88:295–302.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Hoebel BG, Hernandez L, Schwartz DH, Mark GP, Hunter GA. Microdialysis studies of brain norepinephrine, serotonin, and dopamine release during ingestive behavior. Theoretical and clinical implications. Ann N Y Acad Sci. 1989;575:171–91.PubMedCrossRefGoogle Scholar
  62. 62.
    Avena NM, Rada P, Hoebel BG. Sugar and fat bingeing have notable differences in addictive-like behavior. J Nutr. 2009;139:623–8.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    APA – American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-IV). 4th ed. Washington DC: American Psychiatric Association; 1994.Google Scholar
  64. 64.
    Gearhardt AN, Corbin WR, Brownell KD. Food addiction: an examination of the diagnostic criteria for dependence. J Add Med. 2009;3:1–7.CrossRefGoogle Scholar
  65. 65.
    Burmeister JM, Hinman N, Koball A, Hoffmann DA, Carels RA. Food addiction in adults seeking weight loss treatment. Implications for psychosocial health and weight loss. Appetite. 2013;60:103–10.PubMedCrossRefGoogle Scholar
  66. 66.
    Davis C, Curtis C, Levitan RD, Carter JC, Kaplan AS, Kennedy JL. Evidence that ‘food addiction’ is a valid phenotype of obesity. Appetite. 2011;57:711–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Eichen DM, Lent MR, Goldbacher E, Foster GD. Exploration of “food addiction” in overweight and obese treatment-seeking adults. Appetite. 2013;67:22–4.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Flint E, Cummins S, Sacker A. Associations between active commuting, body fat, and body mass index: population based, cross sectional study in the United Kingdom. BMJ. 2014;349:1–9.Google Scholar
  69. 69.
    Gearhardt AN, Corbin WR, Brownell KD. Preliminary validation of the Yale Food Addiction Scale. Appetite. 2009;52:430–6.PubMedCrossRefGoogle Scholar
  70. 70.
    Gearhardt AN, White MA, Masheb RM, Morgan PT, Crosby RD, Grilo CM. An examination of the food addiction construct in obese patients with binge eating disorder. Int J Eat Disord. 2012;45:657–63.PubMedCrossRefGoogle Scholar
  71. 71.
    Gearhardt AN, White MA, Masheb RM, Grilo CM. An examination of food addiction in a racially diverse sample of obese patients with binge eating disorder in primary care settings. Compr Psychiatry. 2013;54:500–5.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Lent MR, Eichen DM, Goldbacher E, Wadden TA, Foster GD. Relationship of food addiction to weight loss and attrition during obesity treatment. Obesity. 2014;22:52–5.PubMedCrossRefGoogle Scholar
  73. 73.
    Mason SM, Flint AJ, Field AE, Austin SB, Rich-Edwards JW. Abuse victimization in childhood or adolescence and risk of food addiction in adult women. Obesity. 2013;21:775–81.CrossRefGoogle Scholar
  74. 74.
    Meule A, Heckel D, Kübler A. Factor structure and item analysis of the Yale Food Addiction Scale in obese candidates for bariatric surgery. Eur Eat Disord Rev. 2012;20:419–22.PubMedCrossRefGoogle Scholar
  75. 75.
    Davis C. From passive overeating to “food addiction”: a spectrum of compulsion and severity. ISRN Obes. 2013;2013:1–20.Google Scholar
  76. 76.
    Hormes JM, Rozin P. Does ‘craving’ carve nature at the joints? Absence of a synonym for craving in many languages. Addict Behav. 2010;35:459–63.PubMedCrossRefGoogle Scholar
  77. 77.
    Martin CK, Mcclernon FJ, Chellino A, Correa JB. Food cravings: a central construct in food intake behavior, weight loss, and the neurobiology of appetitive behavior. In: Handbook of behavior, food and nutrition. New York: Springer; 2011. p. 741–55.CrossRefGoogle Scholar
  78. 78.
    Weingarten HP, Elston D. Food cravings in a college population. Appetite. 1991;17:167–75.PubMedCrossRefGoogle Scholar
  79. 79.
    Hone-Blanchet A, Fecteau S. Overlap of food addiction and substance use disorders definitions: analysis of animal and human studies. Neuropharmacology. 2014;85:81–90.PubMedCrossRefGoogle Scholar
  80. 80.
    Filbey FM, Schach JP, Meyrs US, Chavez RS, Hutchison KE. Marijuana craving in the brain. Proc Natl Acad Sci U S A. 2009;106:13016–21.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Kober H, Mende-Siedlecki P, Kross EF, Weber J, MischeL W, Hat CL, Ochsner KN. Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A. 2010;107:14811–6.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Wang GJ, Volkow ND, Thanos PK, Fowler JS. Imaging of brain dopamine pathways: implications for understanding obesity. J Addict. 2009;3:8–18.Google Scholar
  83. 83.
    Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD. Images of desire: food-craving activation during fMRI. NeuroImage. 2004;23:1486–93.PubMedCrossRefGoogle Scholar
  84. 84.
    Davis C, Patte K, Curtis C, Reid C. Immediate pleasures and future consequences. A neuropsychological study of binge eating and obesity. Appetite. 2010;54:208–13.PubMedCrossRefGoogle Scholar
  85. 85.
    Miller RE, Mirsky IA, Caul WF, Sakata T. Hyperphagia and polydipsia in socially isolated rhesus monkeys. Science. 1969;165:1027–8.PubMedCrossRefGoogle Scholar
  86. 86.
    Foltin RW, Haney M. Effects of the cannabinoid antagonist SR141716 (rimonabant) and d-amphetamine on palatable food and food pellet intake in non-human primates. Pharmacol Biochem Behav. 2007;86:766–73.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Duarte RBM, Patrono E, Borges AC, César AA, Tomaz C, Ventura R, Gasbarri A, Puglisi-Allegra S, Barros M. Consumption of a highly palatable food induces a lasting place-conditioning memory in marmoset monkeys. Behav Process. 2014;107:163–6.CrossRefGoogle Scholar
  88. 88.
    Duarte RBM, Patrono E, Borges AC, Tomaz C, Ventura R, Gasbarri A, Puglisi-Allegra S, Barros M. High versus low fat/sugar food affects the behavioral, but not the cortisol response of marmoset monkeys in a conditioned-place-preference task. Physiol Behav. 2015;139:442–8.PubMedCrossRefGoogle Scholar
  89. 89.
    Rada P, Avena NM, Hoebel BG. Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience. 2005;134:737–44.PubMedCrossRefGoogle Scholar
  90. 90.
    Cottone P, Sabino V, Steardo L, Zorrilla EP. Consummatory, anxiety-related and metabolic adaptations in female rats with alternating access to preferred food. Psychoneuroendocrinology. 2009;34:38–49.PubMedCrossRefGoogle Scholar
  91. 91.
    Colantuoni C, Schwenker J, Mccarthy J, Rada P, Ladenheim B, Cadet JL, Schwartz GJ, Moran TH, Hoebel BG. Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. Neuroreport. 2001;12:3549–52.PubMedCrossRefGoogle Scholar
  92. 92.
    Mathes CM, Ferrara M, Rowland NE. Cannabinoid-1 receptor antagonists reduce caloric intake by decreasing palatable diet selection in a novel dessert protocol in female rats. Am J Physiol Regul Integr Comp Physiol. 2008;295:67–75.CrossRefGoogle Scholar
  93. 93.
    Colantuoni C, Rada P, Mccarthy J, Patten C, Avena NM, Chadeanye A, Hoebel BG. Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res. 2002;10:478–88.PubMedCrossRefGoogle Scholar
  94. 94.
    Corwin RL. Bingeing rats: a model of intermittent excessive behavior? Appetite. 2006;46:11–5.PubMedCrossRefGoogle Scholar
  95. 95.
    Corwin RL, Buda-Levin A. Behavioral models of binge-type eating. Physiol Behav. 2004;82:123–30.PubMedCrossRefGoogle Scholar
  96. 96.
    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;65:545–53.PubMedCrossRefGoogle Scholar
  97. 97.
    Rada P, Bocarsly ME, Barson JR, Hoebel BG, Leibowitz SF. Reduced accumbens dopamine in Sprague-Dawley rats prone to overeating a fat-rich diet. Physiol Behav. 2010;101:394–400.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Liang NC, Hajnal A, Norgren R. Sham feeding corn oil increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol. 2006;291:1236–9.CrossRefGoogle Scholar
  99. 99.
    de Araujo IE, Oliveira-Maia AJ, Sotnikova TD, Gainetdinov RR, Caron MG, Nicolelis MA, Simon SA. Food reward in the absence of taste receptor signaling. Neuron. 2008;57:930–41.PubMedCrossRefGoogle Scholar
  100. 100.
    Volkow ND, Fowler JS, Wang GJ, Baler R, Telang F. Imaging dopamine’s role in drug abuse and addiction. Neuropharmacology. 2009;56:3–8.PubMedCrossRefGoogle Scholar
  101. 101.
    Bocarsly ME, Berner LA, Hoebel BG, Avena NM. Rats that binge eat fat-rich food do not show somatic signs or anxiety associated with opiate-like withdrawal: implications for nutrient-specific food addiction behaviors. Physiol Behav. 2011;104:865–72.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Kenny PJ. Reward mechanisms in obesity: new insights and future directions. Neuron. 2011;69:664–79.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Heyne A, Kiesselbach C, Sahún I, McDonald J, Gaiffi M, Dierssen M, Wolffgramm J. An animal model of compulsive food-taking behaviour. Addict Biol. 2009;14:373–83.PubMedCrossRefGoogle Scholar
  104. 104.
    Finlayson G, King N, Blundell JE. Is it possible to dissociate ‘liking’ and ‘wanting’ for foods in humans? A novel experimental procedure. Physiol Behav. 2007;90:36–42.PubMedCrossRefGoogle Scholar
  105. 105.
    Kinzig KP, Hargrave SL, Honors MA. Binge-type eating attenuates corticosterone and hypophagic responses to restraint stress. Physiol Behav. 2008;95:108–13.PubMedCrossRefGoogle Scholar
  106. 106.
    Geiger BM, Haburcak M, Avena NM, Moyer MC. Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience. 2009;159:1193–9.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Johnson PM, Kenny PJ. Addiction-like reward dysfunction and compulsive eating in obese rats: role for dopamine D2 receptors. Nat Neurosci. 2010;13:635–41.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Hagan MM, Moss DE. Persistence of binge-eating patterns after a history of restriction with intermittent bouts of refeeding on palatable food in rats: implications for bulimia nervosa. Int J Eat Disord. 1997;22:411–20.PubMedCrossRefGoogle Scholar
  109. 109.
    Avena NM, Long KA, Hoebel BG. Sugar-dependent rats show enhanced responding for sugar after abstinence: evidence of a sugar deprivation effect. Physiol Behav. 2005;84:359–62.PubMedCrossRefGoogle Scholar
  110. 110.
    Pothos EN. The effects of extreme nutritional conditions on the neurochemistry of reward and addiction. Acta Astronaut. 2001;49:391–7.PubMedCrossRefGoogle Scholar
  111. 111.
    Pothos EN, Hernandez L, Hoebel BG. Chronic food deprivation decreases extracellular dopamine in the nucleus accumbens: implications for a possible neurochemical link between weight loss and drug abuse. Obes Res. 1995;3:525–9.CrossRefGoogle Scholar
  112. 112.
    Bello NT, Lucas LR, Hajnal A. Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport. 2002;13:1575–8.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Gosnell BA. Sucrose intake enhances behavioral sensitization produced by cocaine. Brain Res. 2005;1031:194–201.PubMedCrossRefGoogle Scholar
  114. 114.
    Zeeni N, Daher C, Fromentin G, Tome D, Darcel N, Chaumontet C. A cafeteria diet modifies the response to chronic variable stress in rats. Stress. 2013;16:211–9.PubMedCrossRefGoogle Scholar
  115. 115.
    Lenoir M, Serre F, Cantin L, Ahmed SH. Intense sweetness surpasses cocaine reward. PLoS One. 2007;2:1–10.CrossRefGoogle Scholar
  116. 116.
    Manian J, Morris MJ. Palatable cafeteria diet ameliorates anxiety and depression-like symptoms following and adverse early environment. Psychoneuroendocrinology. 2010;35:717–28.CrossRefGoogle Scholar
  117. 117.
    Avena NM, Hoebel BG. Amphetamine-sensitized rats show sugar-induced hyperactivity (cross-sensitization) and sugar hyperphagia. Pharmacol Biochem Behav. 2003;74:635–9.PubMedCrossRefGoogle Scholar
  118. 118.
    Cota D, Tschop MH, Horvath TL, Levine AS. Cannabinoids, opioids and eating behavior: the molecular face of hedonism? Brain Res Rev. 2006;51:85–107.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Renata B. M. Duarte
    • 1
    • 2
  • Aline Caron Borges
    • 1
  • Marilia Barros
    • 1
    • 2
  1. 1.Department of Pharmaceutical Sciences, School of Health SciencesUniversity of BrasiliaBrasiliaBrazil
  2. 2.Primate Center, Institute of BiologyUniversity of BrasiliaBrasiliaBrazil

Personalised recommendations