Contribution of the mesolimbic dopamine system in mediating the effects of leptin and ghrelin on feeding

Proceedings of the Nutrition Society

Volumn 71, Issue 4, 2012, Pages 435-445

  Van Zessen, R ^a   Van Der Plasse, G ^a   Adan, R A H ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Dopamine; Feeding behaviour; Ghrelin; Leptin

Indexed keywords

AGOUTI RELATED PROTEIN; DOPAMINE; GHRELIN; JANUS KINASE 2; LEPTIN; LEPTIN RECEPTOR; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN;

ARCUATE NUCLEUS; ASSOCIATION; CONDITIONING; CONFERENCE PAPER; DIET RESTRICTION; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; ENERGY BALANCE; ENZYME ACTIVATION; FEEDING BEHAVIOR; FOOD INTAKE; GENE SILENCING; HUMAN; LATERAL HYPOTHALAMUS; MESOLIMBIC DOPAMINERGIC SYSTEM; MOTIVATION; NONHUMAN; OBESITY; OVERNUTRITION; PLACE PREFERENCE; PROTEIN FUNCTION; REWARD; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VENTRAL TEGMENTUM;

ANOREXIA NERVOSA; APPETITE; DOPAMINE; ENERGY METABOLISM; FEEDING BEHAVIOR; GHRELIN; HUMANS; LEPTIN; MOTIVATION; OBESITY; REWARD; SIGNAL TRANSDUCTION; VENTRAL TEGMENTAL AREA;

EID: 84868265622     PISSN: 00296651     EISSN: 14752719     Source Type: Journal    
DOI: 10.1017/S0029665112000614     Document Type: Conference Paper

References (123)

1. Kelley AE, Baldo BA, Pratt WE et al. (2005) Corticostriatal-hypothalamic circuitry and food motivation: Integration of energy, action and reward. Physiol Behav 86, 773-795.
2. Fields HL, Hjelmstad GO, Margolis EB et al. (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30, 289-316.
3. Narayanan NS, Guarnieri DJ, DiLeone RJ (2010) Metabolic hormones, dopamine circuits, and feeding. Front Neuroendocrinol 31, 104-112.
4. Palmiter RD (2007) Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci 30, 375-381.
5. Margolis EB, Lock H, Hjelmstad GO et al. (2006) The ventral tegmental area revisited: Is there an electrophysiological marker for dopaminergic neurons? J Physiol 577, 907-924.
6. Nair-Roberts RG, Chatelain-Badie SD, Benson E et al. (2008) Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 152, 1024-1031.
7. Yamaguchi T, Wang HL, Li X et al. (2011) Mesocorticolimbic glutamatergic pathway. J Neurosci 31, 8476-8490.
8. Schultz W (2007) Multiple dopamine functions at different time courses. Annu Rev Neurosci 30, 259-288.
9. Wightman RM, Robinson DL (2002) Transient changes in mesolimbic dopamine and their association with 'reward'. J Neurochem 82, 721-735.
10. Gonon F (1997) Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J Neurosci 17, 5972-5978.
11. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275, 1593-1599.
12. Schultz W (2007) Behavioral dopamine signals. Trends Neurosci 30, 203-210.
13. Yun IA, Wakabayashi KT, Fields HL et al. (2004) The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J Neurosci 24, 2923-2933.
14. Schultz W (2010) Multiple functions of dopamine neurons. F1000 Biol Rep 2, 2.
15. Bromberg-Martin ES, Matsumoto M, Hikosaka O (2010) Dopamine in motivational control: Rewarding, aversive, and alerting. Neuron 68, 815-834.
16. Tobler PN, Fiorillo CD, Schultz W (2005) Adaptive coding of reward value by dopamine neurons. Science 307, 1642-1645.
17. Waelti P, Dickinson A, Schultz W (2001) Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43-48.
18. Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299, 1898-1902.
19. Day JJ, Roitman MF, Wightman RM et al. (2007) Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat Neurosci 10, 1020-1028.
20. Beyene M, Carelli RM, Wightman RM (2010) Cue-evoked dopamine release in the nucleus accumbens shell tracks reinforcer magnitude during intracranial self-stimulation. Neuroscience 169, 1682-1688.
21. Roitman MF, Stuber GD, Phillips PE et al. (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24, 1265-1271.
22. Nicola SM, Taha SA, Kim SW et al. (2005) Nucleus accumbens dopamine release is necessary and sufficient to promote the behavioral response to reward-predictive cues. Neuroscience 135, 1025-1033.
23. Roesch MR, Calu DJ, Schoenbaum G (2007) Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nat Neurosci 10, 1615-1624.
24. Cohen JY, Haesler S, Vong L et al. (2012) Neuron-typespecific signals for reward and punishment in the ventral tegmental area. Nature 482, 85-88.
25. Salamone JD, Wisniecki A, Carlson BB et al. (2001) Nucleus accumbens dopamine depletions make animals highly sensitive to high fixed ratio requirements but do not impair primary food reinforcement. Neuroscience 105, 863-870.
26. Cousins MS, Sokolowski JD, Salamone JD (1993) Different effects of nucleus accumbens and ventrolateral striatal dopamine depletions on instrumental response selection in the rat. Pharmacol Biochem Behav 46, 943-951.
27. Ikemoto S, Panksepp J (1996) Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav Neurosci 110, 331-345.
28. Nowend KL, Arizzi M, Carlson BB et al. (2001) D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption. Pharmacol Biochem Behav 69, 373-382.
29. Szczypka MS, Kwok K, Brot MD et al. (2001) Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron 30, 819-828.
30. Ungerstedt U (1971) Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigrostriatal dopamine system. Acta Physiol Scand Suppl 367, 95-122.
31. Salamone JD, Steinpreis RE, McCullough LD et al. (1991) Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology (Berlin) 104, 515-521.
32. Salamone JD, Mahan K, Rogers S (1993) Ventrolateral striatal dopamine depletions impair feeding and food handling in rats. Pharmacol Biochem Behav 44, 605-610.
33. Acosta-Galvan G, Yi CX, van der Vliet J et al. (2011) Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior. Proc Natl Acad Sci USA 108, 5813-5818.
34. Ribeiro AC, LeSauter J, Dupre C et al. (2009) Relationship of arousal to circadian anticipatory behavior: Ventromedial hypothalamus: One node in a hunger-arousal network. Eur J Neurosci 30, 1730-1738.
35. King CM, Hentges ST (2011) Relative number and distribution of murine hypothalamic proopiomelanocortin neurons innervating distinct target sites. PLoS One 6, e25864.
36. Schultz W (2010) Dopamine signals for reward value and risk: Basic and recent data. Behav Brain Funct 6, 24.
37. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5, 483-494.
38. Wise RA (2006) Role of brain dopamine in food reward and reinforcement. Philos Trans R Soc Lond B Biol Sci 361, 1149-1158.
39. Berridge KC (1996) Food reward: Brain substrates of wanting and liking. Neurosci Biobehav Rev 20, 1-25.
40. 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, 309-369.
41. Witten IB, Steinberg EE, Lee SY et al. (2011) Recombinase-driver rat lines: Tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72, 721-733.
42. Adamantidis AR, Tsai HC, Boutrel B et al. (2011) Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J Neurosci 31, 10829-10835.
43. Tsai HC, Zhang F, Adamantidis A et al. (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084.
44. Pothos EN, Creese I, Hoebel BG (1995) 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 15, 6640-6650.
45. Verhagen LA, Luijendijk MC, Korte-Bouws GA et al. (2009) Dopamine and serotonin release in the nucleus accumbens during starvation-induced hyperactivity. Eur Neuropsychopharmacol 19, 309-316.
46. Stuber GD, Evans SB, Higgins MS et al. (2002) Food restriction modulates amphetamine-conditioned place preference and nucleus accumbens dopamine release in the rat. Synapse 46, 83-90.
47. Cadoni C, Solinas M, Valentini V et al. (2003) Selective psychostimulant sensitization by food restriction: Differential changes in accumbens shell and core dopamine. Eur J Neurosci 18, 2326-2334.
48. Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42, 1705-1712.
49. Carr KD (2007) Chronic food restriction: Enhancing effects on drug reward and striatal cell signaling. Physiol Behav 91, 459-472.
50. Fulton S (2010) Appetite and reward. Front Neuroendocrinol 31, 85-103.
51. Sulzer D, Chen TK, Lau YY et al. (1995) Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci 15, 4102-4108.
52. Zhang M, Balmadrid C, Kelley AE (2003) Nucleus accumbens opioid, GABaergic, and dopaminergic modulation of palatable food motivation: Contrasting effects revealed by a progressive ratio study in the rat. Behav Neurosci 117, 202-211.
53. Domingos AI, Vaynshteyn J, Voss HU et al. (2011) Leptin regulates the reward value of nutrient. Nat Neurosci 14, 1562-1568.
54. Aberman JE, Ward SJ, Salamone JD (1998) Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive-ratio performance. Pharmacol Biochem Behav 61, 341-348.
55. Figlewicz DP, Bennett JL, Naleid AM et al. (2006) Intraventricular insulin and leptin decrease sucrose self-administration in rats. Physiol Behav 89, 611-616.
56. la Fleur SE, Vanderschuren LJ, Luijendijk MC et al. (2007) A reciprocal interaction between food-motivated behavior and diet-induced obesity. Int J Obes (Lond) 31, 1286-1294.
57. Alsio J, Olszewski PK, Norback AH et al. (2010) Dopamine D1 receptor gene expression decreases in the nucleus accumbens upon long-term exposure to palatable food and differs depending on diet-induced obesity phenotype in rats. Neuroscience 171, 779-787.
58. Johnson PM, Kenny PJ (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13, 635-641.
59. Wang GJ, Volkow ND, Logan J et al. (2001) Brain dopamine and obesity. Lancet 357, 354-357.
60. Li Y, South T, Han M et al. (2009) High-fat diet decreases tyrosine hydroxylase mRNA expression irrespective of obesity susceptibility in mice. Brain Res 1268, 181-189.
61. Davis JF, Tracy AL, Schurdak JD et al. (2008) Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav Neurosci 122, 1257-1263.
62. Wang GJ, Volkow ND, Fowler JS (2002) The role of dopamine in motivation for food in humans: Implications for obesity. Expert Opin Ther Targets 6, 601-609.
63. Philpot KB, Dallvechia-Adams S, Smith Y et al. (2005) A cocaine-and-amphetamine-regulated-transcript peptide projection from the lateral hypothalamus to the ventral tegmental area. Neuroscience 135, 915-925.
64. Greenwell TN, Zangen A, Martin-Schild S et al. (2002) Endomorphin-1 and -2 immunoreactive cells in the hypothalamus are labeled by fluoro-gold injections to the ventral tegmental area. J Comp Neurol 454, 320-328.
65. Hommel JD, Trinko R, Sears RM et al. (2006) Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51, 801-810.
66. Abizaid A, Liu ZW, Andrews ZB et al. (2006) Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 116, 3229-3239.
67. Yamanaka A, Beuckmann CT, Willie JT et al. (2003) Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38, 701-713.
68. Lawrence CB, Snape AC, Baudoin FM et al. (2002) Acute central ghrelin and GH secretagogues induce feeding and activate brain appetite centers. Endocrinology 143, 155-162.
69. Borgland SL, Chang SJ, Bowers MS et al. (2009) Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neurosci 29, 11215-11225.
70. Leinninger GM, Opland DM, Jo YH et al. (2011) Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab 14, 313-323.
71. Thompson RH, Canteras NS, Swanson LW (1996) Organization of projections from the dorsomedial nucleus of the hypothalamus: A PHA-L study in the rat. J Comp Neurol 376, 143-173.
72. Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12, 483-488.
73. Korotkova TM, Sergeeva OA, Eriksson KS et al. (2003) Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J Neurosci 23, 7-11.
74. Cheung CC, Clifton DK, Steiner RA (1997) Proopiomelanocortin neurons are direct targets for leptin in the hypothalamus. Endocrinology 138, 4489-4492.
75. Schwartz MW, Woods SC, Porte D, Jr et al. (2000) Central nervous system control of food intake. Nature 404, 661-671.
76. Schwartz MW, Seeley RJ, Campfield LA et al. (1996) Identification of targets of leptin action in rat hypothalamus. J Clin Invest 98, 1101-1106.
77. van den Top M, Lee K, Whyment AD et al. (2004) Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7, 493-494.
78. Nakazato M, Murakami N, Date Y et al. (2001) A role for ghrelin in the central regulation of feeding. Nature 409, 194-198.
79. Campfield LA, Smith FJ, Guisez Y et al. (1995) Recombinant mouse OB protein: Evidence for a peripheral signal linking adiposity and central neural networks. Science 269, 546-549.
80. Grill HJ, Schwartz MW, Kaplan JM et al. (2002) Evidence that the caudal brainstem is a target for the inhi-bitory effect of leptin on food intake. Endocrinology 143, 239-246.
81. Pelleymounter MA, Cullen MJ, Baker MB et al. (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269, 540-543.
82. Zhang Y, Proenca R, Maffei M et al. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432.
83. Speakman J, Hambly C, Mitchell S et al. (2007) Animal models of obesity. Obes Rev 8, Suppl. 1, 55-61.
84. Morton GJ, Blevins JE, Kim F et al. (2009) The action of leptin in the ventral tegmental area to decrease food intake is dependent on Jak-2 signaling. Am J Physiol Endocrinol Metab 297, E202-E210.
85. Fulton S, Pissios P, Manchon RP et al. (2006) Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51, 811-822.
86. Figlewicz DP, Evans SB, Murphy J et al. (2003) Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat. Brain Res 964, 107-115.
87. Leshan RL, Opland DM, Louis GW et al. (2010) Ventral tegmental area leptin receptor neurons specifically project to and regulate cocaine- and amphetamine-regulated transcript neurons of the extended central amygdala. J Neurosci 30, 5713-5723.
88. Krugel U, Schraft T, Kittner H et al. (2003) Basal and feeding-evoked dopamine release in the rat nucleus accumbens is depressed by leptin. Eur J Pharmacol 482, 185-187.
89. Liu J, Perez SM, Zhang W et al. (2011) Selective deletion of the leptin receptor in dopamine neurons produces anxiogenic-like behavior and increases dopaminergic activity in amygdala. Mol Psychiatry 16, 1024-1038.
90. Roseberry AG, Painter T, Mark GP et al. (2007) Decreased vesicular somatodendritic dopamine stores in leptindeficient mice. J Neurosci 27, 7021-7027.
91. Pfaffly J, Michaelides M, Wang GJ et al. (2010) Leptin increases striatal dopamine D2 receptor binding in leptindeficient obese (ob/ob) mice. Synapse 64, 503-510.
92. Thanos PK, Michaelides M, Piyis YK et al. (2008) Food restriction markedly increases dopamine D2 receptor (D2R) in a rat model of obesity as assessed with in-vivo muPET imaging ([11C] raclopride) and in-vitro ([3H] spiperone) autoradiography. Synapse 62, 50-61.
93. Matheny M, Shapiro A, Tumer N et al. (2011) Regionspecific diet-induced and leptin-induced cellular leptin resistance includes the ventral tegmental area in rats. Neuropharmacology 60, 480-487.
94. Wettschureck N, Moers A, Wallenwein B et al. (2005) Loss of Gq/11 family G proteins in the nervous system causes pituitary somatotroph hypoplasia and dwarfism in mice. Mol Cell Biol 25, 1942-1948.
95. Zigman JM, Jones JE, Lee CE et al. (2006) Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 494, 528-548.
96. Mondal MS, Date Y, Yamaguchi H et al. (2005) Identification of ghrelin and its receptor in neurons of the rat arcuate nucleus. Regul Pept 126, 55-59.
97. Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407, 908-913.
98. Horvath TL, Diano ST, Schop M (2003) Ghrelin in hypothalamic regulation of energy balance. Curr Top Med Chem 3, 921-927.
99. Verhagen LA, Egecioglu E, Luijendijk MC et al. (2011) Acute and chronic suppression of the central ghrelin signaling system reveals a role in food anticipatory activity. Eur Neuropsychopharmacol 21, 384-392.
100. LeSauter J, Hoque N, Weintraub M et al. (2009) Stomach ghrelin-secreting cells as food-entrainable circadian clocks. Proc Natl Acad Sci USA 106, 13582-13587.
101. Blum ID, Patterson Z, Khazall R et al. (2009) Reduced anticipatory locomotor responses to scheduled meals in ghrelin receptor deficient mice. Neuroscience 164, 351-359.
102. Guan XM, Yu H, Palyha OC et al. (1997) Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res Mol Brain Res 48, 23-29.
103. Quarta D, Di Francesco C, Melotto S et al. (2009) Systemic administration of ghrelin increases extracellular dopamine in the shell but not the core subdivision of the nucleus accumbens. Neurochem Int 54, 89-94.
104. Skibicka KP, Hansson C, Alvarez-Crespo M et al. (2011) Ghrelin directly targets the ventral tegmental area to increase food motivation. Neuroscience 180, 129-137.
105. King SJ, Isaacs AM, O'Farrell E et al. (2011) Motivation to obtain preferred foods is enhanced by ghrelin in the ventral tegmental area. Horm Behav 60, 572-580.
106. Naleid AM, Grace MK, Cummings DE et al. (2005) Ghrelin induces feeding in the mesolimbic reward pathway between the ventral tegmental area and the nucleus accumbens. Peptides 26, 2274-2279.
107. Jerlhag E, Egecioglu E, Dickson SL et al. (2007) Ghrelin administration into tegmental areas stimulates locomotor activity and increases extracellular concentration of dopamine in the nucleus accumbens. Addict Biol 12, 6-16.
108. Egecioglu E, Jerlhag E, Salome N et al. (2010) Ghrelin increases intake of rewarding food in rodents. Addict Biol 15, 304-311.
109. Berthoud HR, Munzberg H (2011) The lateral hypothalamus as integrator of metabolic and environmental needs: From electrical self-stimulation to opto-genetics. Physiol Behav 104, 29-39.
110. Fadel J, Deutch AY (2002) Anatomical substrates of orexindopamine interactions: Lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111, 379-387.
111. Cason AM, Smith RJ, Tahsili-Fahadan P et al. (2010) Role of orexin/hypocretin in reward-seeking and addiction: Implications for obesity. Physiol Behav 100, 419-428.
112. Leinninger GM, Jo YH, Leshan RL et al. (2009) Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab 10, 89-98.
113. Kelley AE, Cador M, Stinus L et al. (1989) Neurotensin, substance P, neurokinin-alpha, and enkephalin: Injection into ventral tegmental area in the rat produces differential effects on operant responding. Psychopharmacology (Berlin) 97, 243-252.
114. Toshinai K, Date Y, Murakami N et al. (2003) Ghrelininduced food intake is mediated via the orexin pathway. Endocrinology 144, 1506-1512.
115. Verhagen LA, Luijendijk MC, de Groot JW et al. (2011) Anticipation of meals during restricted feeding increases activity in the hypothalamus in rats. Eur J Neurosci 34, 1485-1491.
116. Merkestein M, Brans MA, Luijendijk MC et al. (2012) Ghrelin mediates anticipation to a palatable meal in rats. Obesity (Silver Spring) 20, 963-971.
117. Ribeiro AC, Ceccarini G, Dupre C et al. (2011) Contrasting effects of leptin on food anticipatory and total locomotor activity. PLoS One 6, e23364.
118. Mistlberger RE, Marchant EG (1999) Enhanced foodanticipatory circadian rhythms in the genetically obese Zucker rat. Physiol Behav 66, 329-335.
119. Persons JE, Stephan FK, Bays ME (1993) Diet-induced obesity attenuates anticipation of food access in rats. Physiol Behav 54, 55-64.
120. Davis JF, Choi DL, Clegg DJ et al. (2011) Signaling through the ghrelin receptor modulates hippocampal function and meal anticipation in mice. Physiol Behav 103, 39-43.
121. Garzon M, Pickel VM (2001) Plasmalemmal mu-opioid receptor distribution mainly in nondopaminergic neurons in the rat ventral tegmental area. Synapse 41, 311-328.
122. Korotkova TM, Brown RE, Sergeeva OA et al. (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.
123. Lindblom J, Opmane B, Mutulis F et al. (2001) The MC4 receptor mediates alpha-MSH induced release of nucleus accumbens dopamine. Neuroreport 12, 2155-2158.