The role of dopamine in motivation for food in humans: Implications for obesity

Expert Opinion on Therapeutic Targets

Volumn 6, Issue 5, 2002, Pages 601-609

  Wang, Gene Jack ^a   Volkow, Nora D ^a   Fowler, Joanna S ^a  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Dopamine (DA) D2 receptor; Dorsal striatum; Imaging; Reward

Indexed keywords

4 AMINOBUTYRIC ACID; ALCOHOL; AMYLIN; BROMOCRIPTINE; CHOLECYSTOKININ; COCAINE; DIAMORPHINE; DOPAMINE; DOPAMINE RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; GHRELIN; LEPTIN; METHAMPHETAMINE; METHYLPHENIDATE; MORPHINE; NEUROPEPTIDE Y; NEUROPEPTIDE Y RECEPTOR ANTAGONIST; NEUROTRANSMITTER; NICOTINE; PLACEBO; PROOPIOMELANOCORTIN; RACLOPRIDE; RECEPTOR SUBTYPE;

BODY WEIGHT; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; DIET RESTRICTION; DOPAMINE BRAIN LEVEL; DOPAMINERGIC SYSTEM; DRUG ABUSE; DRUG BINDING SITE; DRUG MECHANISM; DRUG METABOLISM; EATING DISORDER; ENERGY EXPENDITURE; ENERGY METABOLISM; FEEDING BEHAVIOR; FOOD INTAKE; HUMAN; MORBIDITY; MORTALITY; MOTIVATION; NONHUMAN; OBESITY; PREVALENCE; PUBLIC HEALTH; REVIEW; SATIETY; UNITED STATES;

ANIMALS; APPETITE; BRAIN CHEMISTRY; CORPUS STRIATUM; DOPAMINE; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; EATING DISORDERS; FEEDING BEHAVIOR; HUMANS; HYPOTHALAMUS; LIMBIC SYSTEM; METHYLPHENIDATE; OBESITY; RATS; RECEPTORS, DOPAMINE; RECEPTORS, DOPAMINE D2; REWARD; SATIATION; SUBSTANCE-RELATED DISORDERS;

EID: 0036400336     PISSN: 14728222     EISSN: None     Source Type: Journal    
DOI: 10.1517/14728222.6.5.601     Document Type: Review

References (110)

1. MOKDAD AH, SERDULA MK, DIETZ WH, BOWMAN BA, MARKS JS, KOPLAN JP: The spread of the obesity epidemic in the United States, 1991-1998. JAMA (1999) 282:1519-1522.
2. COMUZZIE AG, ALLISSON DB: The search for human obesity genes. Science (1998) 280:1374-1377.
3. BARSH GS, FAROOQI IS, O'RAHILLY S: Genetics of body-weight regulation. Nature (2000) 404:644-651.
4. ERICSSON M, POSTON WS II, FOREYT JP: Common biological pathways in eating disorders and obesity. Addict. Behav. (1996) 21:733-743.
5. SERDULA MK, MOKDAD AH, WILLIAMSON DF, GALUSKA DA, MENDLEIN JM, HEATH GW. Prevalence of attempting weight loss and strategies for controlling weight. JAMA (1999) 282:1353-1358.
6. CHAGNON YC, PERUSSE L, WEISNAGEL J, RANKINEN T, BOUCHARD C: The human obesity gene map: the 1999 update. Obes. Res. (2000) 8:89-117.
7. HILL JO, PETERS JC: Environmental contributions to the obesity epidemic. Science (1998) 280:1371-1374.
8. SMITH GP, SCHNEIDER LH: Relationships between mesolimbic dopamine function and eating behavior. Ann. NY Acad. Sci. (1988) 537:254-261.
9. GREENO CG, WING RR: Stress-induced eating. Psychol. Bull. (1994) 115:444-464.
10. BRAY GA, TARTAGLIA LA: Medicinal strategies in the treatment of obesity. Nature (2000) 404:672-677.
11. BLUM K, BRAVERMAN ER, HOLDER JM et al.: Reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive, and compulsive behaviors. J. Psychoactive Drugs (2000) 32(Suppl.):1-112.
12. CUMMINGS DE, WEIGLE DS, FRAYO RS et al.: Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N. Engl. J. Med. (2002) 346:1623-1630.
13. BLUNDELL JE, GILLETT A: Control of food intake in the obese. Obes. Res. (2001) 9:263S-270S.
14. SCHWARTZ GJ, MORAN TH: Sub-diaphragmatic vagal afferent integration of meal-related gastrointestinal signals. Neurosci. Biobehav. Rev. (1996) 20:47-56.
15. KEESEY RE, HIRVONEN MD: Body weight set-points: determination and adjustment. J. Nutr. (1997) 127:1875S-1883S.
16. HARRIS RB, KASSER TR, MARTIN RJ: Dynamics of recovery of body composition after overfeeding, food restriction or starvation of mature female rats. J. Nutr. (1986) 116:2536-2546.
17. BAGDADE JD, BIERMAN EL, PORTE D Jr: The significance of basal insulin levels in the evaluation of the insulin response to glucose in diabetic and nondiabetic subjects. J. Clin. Invest. (1967) 46:1549-1557.
18. CONSIDINE RV, SINHA MK, HEIMAN ML et al.: Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N. Engl. J. Med. (1996) 334:292-295.
19. BUARA GD, FOSTER DM, PORTE D Jr et al.: Saturable transport of insulin from plasma into the central nervous system of dogs in vivo. A mechanism for regulated insulin delivery to the brain. J. Clin. Invest. (1993) 92:1824-1830.
20. SCHWARTZ MW, PESKIND E, RASKIND M, BOYKO EJ, PORTE D Jr: Cerebrospinal fluid leptin levels: relationship to plasma levels and to adiposity in humans. Nat. Med. (1996) 2:589-593.
21. ELIAS CF, LEE C, KELLY J et al.: Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron (1998) 21:1375-1385.
22. SCHWARTZ MW, SEELEY RJ, WOODS SC et al.: Leptin increases hypothalamic pro-opiomelanocortin mRNA expression in the rostral acuate nucleus. Diabetes (1997) 46:2119-2123.
23. HAHN TM, BREININGER JF, BASKIN DG, SCHWARTZ MW: Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat. Neurosci. (1998) 1:271-272.
24. BROBERGER C, JOHANSEN J, JOHANSSON C, SCHALLING M, HOKFELT T: The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc. Natl. Acad. Sci. USA (1998) 95:15043-15048.
25. SIPOLS AJ, BASKIN DG, SCHWARTZ MW: Effect of intracerebroventricular insulin infusion on diabetic hyperphagia and hypothalamic neuropeptide gene expression. Diabetes (1995) 44:147-151.
26. TRAVERS JB, TRAVERS SP, NORGREN R: Gustatory neural processing in the hindbrain. Ann. Rev. Neurosci. (1987) 10:595-632.
27. CAMPFIELD LA, SMITH FJ, GUISEZ Y, DEVOS R, BURN P: Recombinant mouse ob protein: evidence for a peripheral signal linking adiposity and central neural networks. Science (1995) 269:546-549.
28. CHUA SC JR, CHUNG WK, WU-PENG XS et al.: Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor. Science (1996) 271: 994-996.
29. WILSON BD, BAGNOL D, KAELIN CB et al.: Physiological and anatomical circuitry between Agouti-related protein and leptin signaling. Endocrinology (1999) 140:2387-2397.
30. MARSH DJ, HOLLOPETER G, HUSZAR D et al.: Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat. Genet. (1999) 21:119-122.
31. MAFFEI M, HALLAAS J, RAVUSSIN E et al.: Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med. (1995) 1:1155-1161.
32. CLEMENT K, VAISSE C, LAHLOU N et al.: A mutation in the human leptin receptor gene causes obesity and pituitary dysfunction. Nature (1998) 392:398-401.
33. YEO GS, FARCOOQI IS, AMINIAN S, HALSALL DJ, STANHOPE RG, O'RAHILLY S: A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat. Genet. (1998) 20:111-112.
34. VAISSSE C, CLEMENT K, GUY-GRAND B, FROGUEL P: A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat. Genet. (1998) 20:113-114.
35. SCHWARTZ MW, WOODS SC, PORTE D JR, SEELEY RJ, BASKIN DG: Central nervous system control of food intake. Nature (2000) 404:661-671.
36. LEONHARDT M, HRUPKA B, LANGHANS W. New approaches in the pharmacological treatment of obesity. Eur. J. Nutr. (1999) 38:1-13.
37. BLUNDELL JE: Is there a role for serotonin (5-hydroxytryptamine) in feeding? Int. J. Obes. (1977) 1:15-42.
38. CAMPFIELD LA, SMITH FJ, BURN P: Strategies and potential molecular targets for obesity treatment. Science (1998) 280:1383-1387.
39. LEIBOWITZ SF: The role of serotonin in eating disorders. Drugs (1990) 39(Suppl. 3):33-48.
40. SALAMONE JD, KURTH PA, MCCULLOUGH LD, SOKOLOWSKI JD, COUSINS MS: The role of brain dopamine in response initiation: effects of haloperidol and regionally specific dopamine depletions on the local rate of instrumental responding. Brain Res. (1993) 628:218-226.
41. SZCZYPKA MS, RAINEY MA, KIM DS et al.: Feeding behavior in dopamine-deficient mice. Proc. Natl. Acad. Sci. USA (1999) 96:12138-12143.
42. SALAMONE JD, COUSINS MS, SNYDER BJ: Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci. Biobehav. Rev. (1997) 21:341-359.
43. MEGUID MM, FETISSOV SO, VARMA M et al.: Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition (2000) 16:843-857.
44. TONG Y, PELLETIER G: Role of dopamine in the regulation of proopiomelanocortin (pomc) mRNA levels in the arcuate nucleus and pituitary gland of the female rat as studied by in situ hybridization. Brain Res. Mol. Brain Res. (1992) 15:27-32.
45. GILLARD ER, DANG DQ, STANLEY BG: Evidence that neuropeptide Y and dopamine in the perifornical hypothalamus interact antagonistically in the control of food intake. Brain Res. (1993) 628:128-136.
46. BASKIN DG, FIGLEWICZ LATTEMANN D et al.: Insulin and leptin: dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Res. (1999) 848:114-123.
47. MEGUID MM, FETISSOV SO, BLAHA V, YANG ZJ: Dopamine and serotonin VMN release is related to feeding status in obese and lean Zucker rats. Neuroreport (2000) 11:2069-2072.
48. WILLNER P, TOWELL A, MUSCAT R: Apomorphine anorexia: a behavioural and neuropharmacological analysis. Psychopharmacology (1985) 87:351-356.
49. CINCOTTA AH, MACEACHERN TA, MEIER AH: Bromocriptine redirects metabolism and prevents seasonal onset of obese hyperinsulinemic state in Syrian hamsters. Am. J Physiol. (1993) 264:E285-E293.
50. SCISLOWSKI PW, TOZZO E, ZHANG Y, PHANEUF S, PREVELIGE R, CINCOTTA AH: Biochemical mechanisms responsible for the attenuation of diabetic and obese conditions in ob/ob mice treated with dopaminergic agonists. Int. J. Obes. Relat. Metab. Disord. (1999) 23:425-431.
51. CINCOTTA AH, MEIER AH, CINCOTTA JR M: Bromocriptine improves glycaemic control and serum lipid profile in obese Type 2 diabetic subjects: a new approach in the treatment of diabetes. Expert Opin. Investig. Drugs (1999) 8:1683-1707.
52. PIJL H, OHASHI S, MATSUDA M et al.: Bromocriptine: a novel approach to the treatment of Type 2 diabetes. Diabetes Care (2000) 23:1154-1161.
53. BINA KG, CINCOTTA AH: Dopaminergic agonists normalize elevated hypothalamic neuropeptide Y and corticotropin-releasing hormone, body weight gain, and hyperglycemia in ob/ob mice. Neuroendocrinology (2000) 71:68-78.
54. LUO S, MEIER AH, CINCOTTA AH: Bromocriptine reduces obesity; glucose intolerance and extracellular monoamine metabolite levels in the ventromedial hypothalamus of Syrian hamsters. Neuroendocrinology (1998) 68:1-10.
55. CLINTON PG, RUSK IN, COOPER SJ: Effects of dopamine D1 and dopamine D2 antagonists on the free feeding and drinking patterns of rats. Behav. Neurosci. (1991) 105:272-281.
56. BAPTISTA T, PARADA M, HERNANDEZ L: Long term administration of some antipsychotic drugs increases body weight and feeding in rats. Are D2 dopamine receptors involved? Pharmacol. Biochem. Behav. (1987) 27:399-405.
57. ALLISON DB, CASEY DE: Antipsychotic-induced weight gain: a review of the literature. J. Clin. Psychiatry (2001) 62(Suppl. 7):22-31.
58. WETTERLING T: Bodyweight gain with atypical antipsychotics. A comparative review. Drug Saf. (2001) 24:59-73.
59. LUTZ TA, TSCHUDY S, MOLLET A, GEARY N, SCHARRER E: Dopamine D2 receptors mediate amylin's acute satiety effect. Am. J. Physiol. Regul. Integr. Comp. Physiol. (2001) 280:R1697-R1703.
60. CHEN J: Dopamine D2 receptor and obesity. Lancet (2001) 357:1883.
61. GOUDIE AJ, SMITH JA, HALFORD JCG: Characterisation of olanzapine-induced weight gain in rats. J. Psychopharmacol. In press.
62. MARTEL P, FANTINO M: Mesolimbic dopaminergic system activity as a function of food reward: a microdialysis study. Pharmacol. Biochem. Behav. (1996) 53:221-226.
63. POTHOS E, CREESE I, HOEBEL B: Restricted eating with weight loss selectively decreases extracellular dopamine in the nucleus accumbens and alters dopamine response to amphetamine, morphine, and food intake. J. Neurosci. (1995) 15:6640-6650.
64. BERRIDGE KC, ROBINSON TE: What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. (1998) 28:309-369.
65. SCHWARTZ MW, BASKIN DG, KAIYALA KJ, WOODS SC: Model for the regulation of energy balance and adiposity by the central nervous system. Am. J. Clin. Nutr. (1999) 69:584-596.
66. BERRIDGE KC, ROBINSON TE: What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. (1998) 28:309-369.
67. KOOB GF, BLOOM FE: Cellular and molecular mechanisms of drug dependence. Science (1988) 242:715-723.
68. WISE RA, BOZARTH MA: A psychosomatic stimulant theory of addiction. Psychol. Rev. (1987) 94:469-492.
69. VOLKOW ND, WANG G-J, FOWLER JS et al.: 'Nonhedonic' food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect. Synapse (2002) 44:175-180.
70. VOLKOW ND, WANG G-J, FOWLER JS et al.: Relationship between blockade of dopamine transporters by oral methylphenidate and the increases in extracellular dopamine: therapeutic implications. Synapse (2002) 43:181-187.
71. 11C-methyl]-(l)-cocaine PET studies in human subjects. J. Cereb. Blood Flow Metab. (1990) 10:740-747.
72. HERNANDEZ L, HOEBEL BG: Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by dialysis. Life Sci. (1988) 42:1705-1712.
73. PHILLIPS AG, ATKINSON LJ, BLACKBURN JR, BLAHA CD: Increased extracellular dopamine in the nucleus accumbens of the rat elicited by a conditioned stimulus for food: an electrochemical study. Can. J. Physiol. Pharmacol. (1993) 71:387-393.
74. RICHARDSON NR, GRATTON A: Behavior-relevant changes in nucleus accumbens dopamine transmission elicited by food reinforcement: an electrochemical study in rat. J. Neurosci. (1996) 16:8160-8169.
75. 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) 11:4389-4397.
76. SZCZYPKA MS, KWOK K, BROT MD et al.: Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron (2001) 30:819-828.
77. BINA KG, CINCOTTA AH: Dopaminergic agonist normalize elevated hypothalamic neuropeptide Y and corticotropin-releasing hormone, body weight gain, and hyperglycemia in ob/ob mice. Neuroendocrinology (2000) 71:68-78.
78. NOBLE EP, NOBLE RE, RITCHIE T et al. D2 dopamine receptor gene and obesity. Int. J. Eat. Disord. (1994) 15:205-217.
79. LARUELLE M, GELERNTER J, INNIS RB: D2 receptors binding potential is not affected by Taq1 polymorphism at the D2 receptor gene. Mol. Psychiatry (1998) 3:261-265.
80. NOBLE EP, BLUM K, RITCHIE T, MONTGOMERY A, SHERIDAN PJ: Allelic association of the D2 dopamine receptor gene with receptor-binding characteristics in alcoholism. Arch. Gen. Psychiatry (1991) 48:648-654.
81. COMINGS DE, GADE R, MACMURRAY JP, MUHLEMAN D, PETERS WR: Genetic variants of the human obesity (OB) gene: association with body mass index in young women, psychiatric symptoms, and interaction with the dopamine D2 receptor (DRD2) gene. Mol. Psychiatry (1996) 1:325-335.
82. NOBLE EP, FITCH RJ, RITCHIE T, BRUNNER RL, ZHANG Y, STJEOR SC: The D2 dopamine receptor gene: obesity, smoking and mood. In: Obesity Assessment. St Jeor ST (Ed.), Chapman and Hall, New York (1997):522-533.
83. JIMERSON DC, LESEM MD, KAYE WH, BREWERTON TD: Low serotonin and dopamine metabolite concentrations in cerebrospinal fluid from bulimic patients with frequent binge episodes. Arch. Gen. Psychiatry (1992) 49:132-138.
84. WANG G-J, VOLKOW ND, LOGAN J et al.: Brain dopamine and obesity. Lancet (2001) 357:354-357.
85. VOLKOW ND, FOWLER JS, WANG G-J et al.: Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse (1993) 14:169-177.
86. VOLKOW ND, FOWLER JS, WOLF AP: Effects of chronic cocaine abuse on postsynaptic dopamine receptors. Am. J. Psychiatry (1990) 147:719-724.
87. VOLKOW ND, CHANG L, WANG G-J et al.: Decreased brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in orbitofrontal cortex. Am. J. Psychiatry. In press.
88. VOLKOW ND, WANG G-J, FOWLER JS et al.: Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol. Clin. Exp. Res. (1996) 20:1594-1598.
89. WANG G-J, VOLKOW ND, FOWLER JS et al.: Dopamine D2 receptors availability in opiate-dependent subjects before and after naloxone-precipitated withdrawal. Neuropsychopharmacology (1997) 16:174-182.
90. WANG G-J, VOLKOW ND, FOWLER JS, PAPPAS NR, WONG CT, NETUSIL N: Evaluation of brain dopamine systems in obese subjects using PET. J. Nucl. Med. (2000) 41:139P.
91. PHILLIPS TJ, BROWN KJ, BURKHART-KASCH S. et al.: Alcohol preference and sensitivity are markedly reduced in mice lacking D2 receptors. Nat. Neurosci. (1998) 1:610-615.
92. MALDONADO R, SAIARDI A, VALVERDE O, SAMAD TA, ROQUES BP, BORRELLI E: Absence of opiate rewarding effects in mice lacking dopamine D2 receptors. Nature (1997) 388:586-589.
93. CAINE SB, NEGUS SS, MELLO NK et al.: Role of dopamine D2-like receptors in cocaine self-administration: studies with D2 receptor mutant mice and novel D2 receptor antagonists. J Neurosci. (2002) 22:2977-2988.
94. WEISSENBORN R, DEROCHE V, KOOB GF, WEISS F: Effects of dopamine agonists and antagonists on cocaine-induced operant responding for a cocaine-associated stimulus. Pychopharmacology (Berl.) (1996) 126:311-322.
95. BERGER SP, HALL S, MICKALIAN JD et al.: Haloperidol antagonism of cue-elicited cocaine craving. Lancet (1996) 347:504-508.
96. SHERER MA, KUMOR KM, JAFFE JH: Effects of intravenous cocaine are partially attenuated by haloperidol. Psychiatry Res. (1989) 27:117-125.
97. GOSNELL BA: Sucrose intake predicts rate of acquisition of cocaine self-administration. Psychopharmacology (2000) 149:286-292.
98. VOLKOW ND, WANG G-J, FOWLER JS et al.: Prediction of reinforcing responses to psychostimulants in humans by brain dopamine D2 receptor levels. Am. J. Psychiatry (1999) 156:1440-1443.
99. TOWELL A, MUSCAT R, WILLNER P: Behavioural microanalysis of the role of dopamine in amphetamine anorexia. Pharmacol. Biochem. Behav. (1988) 30:641-648.
100. FOLTIN RW, FISCHMAN MW, NAUTIYAL C: The effects of cocaine on food intake of baboons before, during, and after a period of repeated desipramine. Pharmacol. Biochem. Behav. (1990) 36:869-874.
101. WANG G-J, VOLKOW ND, WONG CT et al.: Behavior and cardiovascular effects of intravenous methylphenidate in normal subjects and cocaine abusers. Eur. Addict. Res. (1997) 3:49-54.
102. PLATTE P, PIRKE KM, WADE SE, TRIMBORN P, FICHTER MM: Physical activity, total energy expenditure, and food intake in grossly obese and normal weight women. Int. J. Eat. Disord. (1995) 17:51-57.
103. BANDINI LG, SCHOELLER DA, CYR HN, DIETZ WH: Validity of reported energy intake in obese and nonobese adolescents. Am. J. Clin. Nutr. (1990) 52:421-425.
104. PRENTICE AM, BLACK AE, COWARD WA et al.: High levels of energy expenditure in obese women. Br. Med. J. (Clin. Res. Ed.) (1986) 292:983-987.
105. TRYON WW, GOLDBERG JL, MORRISON DF: Activity decreases as percentage overweight increases. Int. J. Obes. Relat. Metab. Disord. (1992) 16:591-595.
106. SPECILAE SG, MILLER JD, MCMILLEN BA, GERMAN DC: Activation of specific central dopamine pathways: locomotion and footshock. Brain Res. Bull. (1986) 16:33-38.
107. HEYES M, GARNETT E, COATES G: Nigrostriatal dopaminergic activity is increased during exhaustive exercise stress in rats. Life Sci. (1988) 42:1537-1542.
108. HATTORI S, NAOI M, NISHINO H: Striatal dopamine turnover during treadmill running in the rat: relation to the speed of running. Brain Res. Bull. (1994) 35:41-49.
109. WILSON WM, MARSDEN CA: Extracellular dopamine in the nucleus accumbens of the rat during treadmill running. Acta Physiol. Scand. (1995) 155:465-466.
110. MACRAE PG, SPIRDUSO WW, CARTEE GD, FARRAR RP, WILCOX RE: Endurance training effects on striatal D2 dopamine receptor binding and striatal dopamine metabolite levels. Neurosci. Lett. (1987) 79:138-144.