Dopamine-based reward circuitry responsivity, genetics, and overeating

Current Topics in Behavioral Neurosciences

Volumn 6, Issue 1, 2011, Pages 81-93

  Stice, Eric ^a   Yokum, Sonja ^a   Zald, David ^b   Dagher, Alain ^c  

^a OREGON RESEARCH INSTITUTE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Dopamine; Food reward; Genetics; Obesity; Overeating

Indexed keywords

CATECHOL METHYLTRANSFERASE; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; PROTEIN KINASE B; DOPAMINE 4 RECEPTOR; DRD4 PROTEIN, HUMAN; GHRELIN;

ARTICLE; BODY WEIGHT; CATHECOL O METHYLTRANSFERASE GENE; DNA POLYMORPHISM; DOPAMINE BRAIN LEVEL; DOPAMINE D2 RECEPTOR GENE; DOPAMINE RELEASE; EATING HABIT; FOOD INTAKE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE; GENETIC VARIABILITY; GENOTYPE; HUMAN; LIPID DIET; NONHUMAN; OBESITY; OVERNUTRITION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REWARD; WEIGHT GAIN; ANIMAL; BRAIN; GENETICS; HYPERPHAGIA; METABOLISM; PATHOLOGY; PSYCHOLOGICAL ASPECT; REVIEW;

ANIMALS; BRAIN; CATECHOL O-METHYLTRANSFERASE; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; GHRELIN; HUMANS; HYPERPHAGIA; OBESITY; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D4; REWARD;

EID: 81455130784     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2010_89     Document Type: Article

References (80)

1. Abizaid A, Liu ZW, Andrews ZB, Shanabrough M, Borok E, Elsworth JD, Roth RH, Sleeman MW, Picciotto MR, Tschop MH, Gao XB, Horvath TL (2006) Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Investig 116:3229-3239.
2. Asghari V, Sanyal S, Buchwaldt S, Paterson A, Jovanovic V, Van Tol HH (1995) Modulation of intracellular cyclic AMP levels by different human dopamine D4 receptor variants. J Neurochem 65:1157-1165.
3. Avena NM, Rada P, Hoebel BG (2008) Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose. Neuroscience 16:865-871.
4. Bayer HM, Glimcher PW (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47(1):129-141.
5. Bello NT, Lucas LR, Hajnal A (2002) Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport 13(12):1575-1578.
6. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28(3):309-369.
7. Bilder R, Volavka J, Lachman H, Grace A (2004) Relations to the tonic-phasic dopamine hypothesis and neuropsychiatric phenotypes. Neuropsychopharmacology 29(11):1943-1961.
8. Blackburn JR, Phillips AG, Jakubovic A, Fibiger HC (1989) Dopamine and preparatory behavior: a neurochemical analysis. Behav Neurosci 103:15-23.
9. Boettiger CA, Mitchell JM, Tavares VC, Robertson M, Joslyn G, D'Esposito M, Fields HL (2007) Immediate reward bias in humans: fronto-parietal networks and a role for the catechol-O methyltransferase 158(Val/Val) genotype. J Neurosci 27(52):14383-14391.
10. Bowirrat A, Oscar-Berman M (2005) Relationship between dopaminergic neurotransmission, alcoholism, and reward deficiency syndrome. Am J Med Genet B Neuropsychiatr Genet 132 (1):29-37.
11. Brody AL, Mandelkern MA, Olmstead RE, Scheibal D, Hahn E, Shiraga S, Zamora-Paja E, Farahi J, Saxena S, London ED, McCracken JT (2006) Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. Arch Gen Psychiatry 63:808-816.
12. Carvelli L, Moron JA, Kahlig KM, Ferrer V (2002) PI 3-kinase regulation of dopamine uptake. J Neurochem 81:859-869.
13. Chen PS, Yang YK, Yeh TL, Lee IH, Yao WJ, Chiu NT, Lu RB (2008) Correlation between body mass index and striatal dopamine transporter availability in healthy volunteers: a SPECT study. Neuroimage 40:275-279.
14. Comings DE, Flanagan SD, Dietz G, Muhleman D, Knell E, Gysin R (1993) The dopamine D2 receptor (DRD2) as a major gene in obesity and height. Biochem Med Metab Biol 50(2): 176-185.
15. Cota D, Barrera JG, Seeley RJ (2006) Leptin in energy balance and reward: two faces of the same coin? Neuron 51:678-680.
16. Davis JF, Tracy AL, Schurdak JD, Tschöp MH, Lipton JW, Clegg DJ, Benoit SC (2008) Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav Neurosci 122(6):1257-1263.
17. Epstein LH, Jaroni JL, Paluch RA, Leddy JJ, Vahue HE, Hawk L, Pl W, Shields PG, Lerman C (2002) Dopamine transport genotype as a risk factor for obesity in smokers. Obesity 10: 1232-1240.
18. Epstein LH, Wright SM, Paluch RA, Leddy JJ, Hawk LW, Jaroni JL, Saad FG, Crystal-Mansour S, Shields PG, Lerman C (2004) Relation between food reinforcement and dopamine genotypes and its effect on food intake in smokers. Am J Clin Nutr 80:82-88.
19. Epstein LJ, Leddy JJ, Temple JL, Faith MS (2007) Food reinforcment and eating: a multilevel analysis. Psychol Bull 133:884-906.
20. Erblich J, Lerman C, Self DW, Diaz GA, Bovbjerg DH (2005) Effects of dopamine D2 receptor (DRD2) and transporter (SLC6A3) polymorphisms on smoking cue-induced cigarette craving among African American smokers. Mol Psychiatry 10:407-414.
21. Fetissov SO, Meguid MM, Sato T, Zhang LH (2002) Expression of dopaminergic receptors in the hypothalamus of lean and obese Zucker rates and food intake. Am J Physiol Regul Integr Comp Physiol 283:905-910.
22. Figlewicz DP, Evans SB, Murphy J, Hoen M, Baskin DG (2003) Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat. Brain Res 964(1):107-115.
23. Filbey FM, Ray L, Smolen A, Claus ED, Audette A, Hutchison K (2008) Differential neural response to alcohol priming and alcohol taste cues is associated with DRD4. VNTR and OPRM1 genotypes. Alcohol Clin Exp Res 32:1-11.
24. Floresco SB, West AR, Ash B, Moore H, Grace AA (2003) Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6:968-973.
25. Fossella J, Green AE, Fan J (2006) Evaluation of a structural polymorphism in the ankyrin repeat and kinase domain containing 1 (ANKK1) gene and the activation of executive attention networks. Cogn Affect Behav Neurosci 6:71-78.
26. Fulton S, Woodside B, Shizgal P (2000) Modulation of brain reward circuitry by leptin. Science 287:125-128.
27. Fulton S, Richard D, Woodside B, Shizgal P (2004) Food restriction and leptin impact brain reward circuitry in lean and obese Zucker rats. Behav Brain Res 155:319-329.
28. Garcia BG, Wei Y, Moron JA, Lin RZ, Javitch JA, Galli A (2005) Akt is essential for insulin modulation of amphetamine-induced human dopamine transporter cell-surface redistribution. Mol Pharmacol 68:102-109.
29. Geiger BM, Haburcak M, Avena NM, Moeyer MC, Hoebel BG, Photos EN (2009) Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 159(4): 1193-1199.
30. Gogos JA, Morgan M, Luine V, Santha M, Ogawa S, Pfaff D et al (1998) Catechol-O-methyltransferase- deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior. Proc Natl Acad Sci U S A 95:9991-9996.
31. Goldstein R, Klein A, Tomasi D, Zhang L, Cottone L, Maloney T et al (2007) Is decreased prefrontal cortical sensitivity to monetary reward associated with impaired motivation and selfcontrol in cocaine addiction? Am J Psychiatry 164:43-51.
32. Guo G, North KE, Gorden-Larsen P, Bulik CM, Choi S (2007) Body mass, DRD4, physical activity, sedentary behavior, and family socioeconomic status. Obesity 15:1199-1206.
33. Hamarman S, Fossella J, Ulger C, Brimacombe M, Dermody J (2004) Dopamine receptor 4 (DRD4) 7-repeat allele predicts methylphenidate dose response in children with attention deficit hyperactivity disorders: a pharmacogenetic study. J Child Adolesc Psychopharmacol 14:564-574.
34. Hao J, Cabeza DV, Carr KD (2004) Effects of chronic ICV leptin infusion on motor-activating effects of D-amphetamine in food-restricted and ad libitum fed rats. Physiol Behav 83:377-381.
35. Hare TA, O'Doherty J, Camerer CF, Schultz W, Rangel A (2008) Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J Neurosci 28(22):5623-5630.
36. Huang XF, Zavitsanou K, Huang X, Yu Y, Wang H, Chen F, Lawrence AJ, Deng C (2006) Dopamine transporter and D2 receptor binding densities in mice prone or resistant to chronic high fat diet-incuded obesity. Behav Brain Res 175:415-419.
37. Hutchison KE, McGeary J, Smolen A, Bryan A, Swift RM (2002) The DRD4. VNTR polymorphism moderates craving after alcohol consumption. Health Psychol 21:139-146.
38. Kaplan AS, Levitan RD, Yilmaz Z, Davis C, Tharmalingam S, Kennedy JL (2008) A DRD4/ BDNF gene-gene interaction associated with maximum BMI in women with bulimia nervosa. Int J Eat Disord 41:22-28.
39. Kelley AE, Will MJ, Steininger TL, Zhang M, Haber SN (2003) Restricted daily consumption of a highly palatable food (chocolate Ensure(R)) alters striatal enkephalin gene expression. Eur J Neurosci 18(9):2592-2598.
40. Kirsch P, Reuter M, Mier D, Lonsdorf T, Stark R, Gallhofer B et al (2006) Imaging gene-substance interactions: the effect of the DRD2. TaqIA polymorphism and the dopamine agonists bromocriptine on the brain activation during the anticipation of reward. Neurosci Lett 405:196-201.
41. Kiyatkin EA, Gratton A (1994) Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food. Brain Res 652:225-234.
42. Knutson B, Gibbs SE (2007) Linking nucleus accumbens dopamine and blood oxygenation. Psychopharmacology (Berl) 191(3):813-822.
43. Korotkova TM, Brown RE, Sergeeva OA, Ponomarenko AA, Haas HL (2006) Effects of arousal and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur J Neurosci 23:2677-2685.
44. Levin BE, Meynell AA (2002) Defense of body weight depends on dietary composition and palatability in rats with diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 282: R46-54.
45. Levitan RD, Masellis M, Lam RW, Muglia P, Basile VS, Jain U, Kaplan AS, Tharmakingam S, Kennedy SH, Kennedy JL (2004) Childhood in-attention and dysphoria and adult obesity associated with the dopamine D4 receptor gene in overeating women with seasonal affective disorder. Neuropsychopharmacology 29:179-186.
46. Li Y, Shao C, Zhang D, Zhao M, Lin L, Yan P, Xie Y, Jiang K, Jin L (2006) The effect of dopamine D2, D5 receptor and transporter (SLC6A3) polymorphisms on the cue-elicited heroin craving in Chinese. Am J Med Genet B Neuropsychiatr Genet 141B:269-273.
47. Matsumoto M, Weickert C, Beltaifa S, Kolachana B, Chen J, Hyde TM, Herman MM, Weinberger DR, Kleinman JE (2003) Catechol 0-methyltransferase (COMT) mRNA expression in the dorsolateral prefrontal cortex of patients with schizophrenia. Neuropsychopharmacology 28(8):1521-30.
48. McClernon FJ, Hutchison KE, Rose JE, Kozink RV (2007) DRD4. VNTR polymorphism is associated with transient fMRI-BOLD responses to smoking cues. Psychopharmacology (Berl) 194:433-441.
49. Mikolajczyk E, Smiarowska M, Grzywacz A, Samochowiec J (2006) Association of eating disorders with catechol-O-methyltransferase gene functional polymorphism. Neuropsychobiology 54(1):82-86.
50. Narita M, Nagumo Y, Hashimoto S, Narita M, Khotib J, Miyatake M et al (2006) Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J Neurosci 26:398-405.
51. Nascimento EBM, Fodor M, van der Zon GCM, Jazet IM, Meinders AE, Voshol PJ, Vlasblom R, Baan B, Eckel J, Maassen JA, Diamant M, Ouwens DM (2007) Insulin-mediated phosphorylation of the proline-rich AKT substrate PRAS40 is impaired in insulin target tissues of high-fat diet-fed rats. Diabetes Nutr Metab 55(12):3221-3228.
52. Noain D, Avale ME, Wedemeyer C, Calvo D, Peper M, Rubinstein M (2006) Identification of brain neurons expressin the dopamine D4 receptor gene using BAC transgenic mice. Eur J Neurosci 24:2429-2438.
53. Orosco M, Rouch C, Nicolaidis S (1996) Rostromedial hypothalamic monoamine changes in response to intravenous infusions of insulin and glucose in freely feeding obese Zucker rats: a microdialysis study. Appetite 26:1-20.
54. Patterson TA, Brot MD, Zavosh A, Schenk JO, Szot P, Figlewicz DP (1998) Food deprivation decreases mRNA and activity of the rat dopamine transporter. Neuroendocrinology 68:11-20.
55. Pecina S, Cagniard B, Berridge KC, Aldrigde JW, Zhuang X (2003) Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards. J Neurosci 23:9395-9402.
56. Ritchie T, Noble EP (2003) Association of seven polymorphisms of the D2 dopamine receptor gene with brain receptor-binding characteristics. Neurochem Res 28:73-82.
57. Robinson TE, Berridge KC (2000) Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci 20:s91-s117.
58. Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13(3):900-913.
59. Shalev U, Yap J, Shaham Y (2001) Leptin attenuates acute food deprivation-induced relapse to heroin seeking. J Neurosci 21:RC129.
60. Shao C, Li Y, Jiang K, Zhang D, Xu Y, Lin L, Wang Q, Zhao M, Jin L (2006) Dopamine D4 receptor polymorphism modulates cue-elicited heroin craving in Chinese. Psychopharmacology (Berl) 186:185-190.
61. Simon G, von Korff M, Saunders K, Miglioretti D, Crane P et al (2006) Association between obesity and psychiatric disorders in the US population. Arch Gen Psychiatry 63:824-830.
62. Small DM, Jones-Gotman M, Dagher A (2003) Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage 19:1709-15.
63. Sobik L, Hutchison K, Craighead L (2005) Cue-elicited craving for food: a fresh approach to the study of binge eating. Appetite 44:253-61.
64. South T, Huang XF (2008) High-fat diet exposure increases dopamine D2 receptor and decreases dopamine transporter receptor binding density in the nucleus accumbens and caudate putamen of mice. Neurochem Res 33:598-605.
65. Southon AWK, Sanigorski AM, Zimmet P, Nicholson GC, Kotowicz MA, Collier G (2003) The Taq IA and Ser311. Cys polymorphisms in the dopamine D2 receptor gene and obesity. Diabetes Nutr Metab 16:72-76.
66. Spitz MR, Detry MA, Pillow P, Hu YH, Amos CI, Hong WK, Wu X (2000) Variant alleles of the D2 dopamine receptor gene and obesity. Nutr Res 20:371-380.
67. Stice E, Spoor S, Bohon C, Small DM (2008a) Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322:449-452.
68. Stice E, Spoor S, Bohon C, Veldhuizen M, Small DM (2008b) Relation of reward from food intake and anticipated intake to obesity: a functional magnretic resonance imaging study. J Abnorm Psychol 117:924-935.
69. Stice E, Yokum S, Bohon C, Marti N, Smolen A (2010) Reward circuitry responsivity to food predicts future increases in body mass: moderating effects of DRD2 and DRD4. Neuroimage 50(4):1618-1625.
70. Thanos PK, Volkow ND, Freimuth P, Umegaki H, Ikari H, Roth G, Ingram DK, Hitzemann R (2001) Overexpression of dopamine receptors reduces alcohol self-administration. J Neurochem 78(5):1094-1103.
71. Thomas GN, Critchley JA, Tomlinson B, Cockram CS, Chan JC (2001) Relationships between the TaqI polymorphism of the dopamine D2 receptor and blood pressure in hyperglycemic and normoglycemic Chinese subjects. Clin Endocrinol 55:605-611.
72. Tupala E, Hall H, Bergström K, Mantere T, Räsänen P, Särkioja T, Tiihonen J (2003) Dopamine D2 receptors and transporters in type 1 and 2 alcoholics measured with human whole hemisphere autoradiography. Hum Brain Mapp 20(2):91-102.
73. Vittoz NM, Berridge CW (2006) Hypocretin/orexin selectively increases dopamine efflux within the prefrontal cortex: involvement of the ventral tegmental area. Neuropsychopharmacology 31:384-395.
74. Volkow ND, Fowler JS, Wang GJ (2002) Role of dopamine in drug reinforcement and addiction in humans: results from imaging studies. Behav Pharmacol 13:355-366.
75. Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J, Alexoff D, Ding YS, Wong C, Ma Y, Pradhan K (2008) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. Neuroimage 42(4):1537-1543.
76. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W, Netusil N, Fowler JS (2001) Brain dopamine and obesity. Lancet 357(9253):354-357.
77. Warren M, Frost-Pineda K, Gold M (2005) Body mass index and marijuana use. J Addict Dis 24:95-100.
78. Wellman PJ, Nation JR, Davis KW (2007) Impairment of cocaine self-administration in rats maintained on a high fat diet. Pharmacol Biochem Behav 88:89-93.
79. Williams JM, Owens WA, Turner GH, Saunders C, Dipace C, Blakely RD, France CP, Gore JC, Daws LC, Avison MJ, Galli A (2007) Hypoinsulinemia regulates amphetamine-induced reverse transport of dopamine. PLoS Biol 5(10):e274.
80. Yamamoto T (2006) Neural substrates for the processing of cognitive and affective aspects of taste in the brain. Arch Histol Cytol 69:243-255