Regulation of the mesocorticolimbic and mesostriatal dopamine systems by α-melanocyte stimulating hormone and agouti-related protein

Neuroscience and Biobehavioral Reviews

Volumn 56, Issue , 2015, Pages 15-25

  Roseberry, Aaron G ^a   Stuhrman, Katherine ^a   Dunigan, Anna I ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

AgRP; Dopamine; Drug abuse; Feeding; MC3R; MC4R; Melanocortin; VTA; MSH

Indexed keywords

4 AMINOBUTYRIC ACID; AGOUTI RELATED PROTEIN; ALPHA INTERMEDIN; AMPHETAMINE; BETA ENDORPHIN; COCAINE; GLUTAMIC ACID; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; MU OPIATE RECEPTOR; PROOPIOMELANOCORTIN; DOPAMINE; MELANOCORTIN RECEPTOR;

ALCOHOL CONSUMPTION; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DOPAMINERGIC TRANSMISSION; DRUG ABUSE; FOOD INTAKE; GROOMING; LOCOMOTION; MESOCORTICOLIMBIC DOPAMINE SYSTEM; MESOSTRIATAL DOPAMINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; REARING; REINFORCEMENT; REVIEW; REWARD; SELF ADMINISTRATION TEST; SUCROSE PREFERENCE TEST; VENTRAL TEGMENTUM; ANIMAL; BRAIN; DRUG EFFECTS; EATING; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

AGOUTI-RELATED PROTEIN; ALPHA-MSH; ANIMALS; BRAIN; DOPAMINE; EATING; HUMANS; RECEPTORS, MELANOCORTIN; REWARD; SIGNAL TRANSDUCTION;

EID: 84947280588     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2015.06.020     Document Type: Review

References (97)

1. Adan R.A., Szklarczyk A.W., Oosterom J., Brakkee J.H., Nijenhuis W.A., Schaaper W.M., Meloen R.H., Gispen W.H. Characterization of melanocortin receptor ligands on cloned brain melanocortin receptors and on grooming behavior in the rat. Eur. J. Pharmacol. 1999, 378:249-258.
2. Agosti F., Lopez Soto E.J., Cabral A., Castrogiovanni D., Schioth H.B., Perello M., Raingo J. Melanocortin 4 receptor activation inhibits presynaptic N-type calcium channels in amygdaloid complex neurons. Eur. J. Neurosci. 2014, 40:2755-2765.
3. Alserda E., Adan R.A., Ramakers G.M. Repeated agouti related peptide (83-132) injections inhibit cocaine-induced locomotor sensitisation, but not via the nucleus accumbens. Eur. J. Pharmacol. 2013, 719:187-191.
4. Alvaro J.D., Taylor J.R., Duman R.S. Molecular and behavioral interactions between central melanocortins and cocaine. J. Pharmacol. Exp. Ther. 2003, 304:391-399.
5. Aponte Y., Atasoy D., Sternson S.M. AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat. Neurosci. 2011, 14:351-355.
6. Atalayer D., Robertson K.L., Haskell-Luevano C., Andreasen A., Rowland N.E. Food demand and meal size in mice with single or combined disruption of melanocortin type 3 and 4 receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1667-R1674.
7. Bagnol D., Lu X.Y., Kaelin C.B., Day H.E., Ollmann M., Gantz I., Akil H., Barsh G.S., Watson S.J. Anatomy of an endogenous antagonist: relationship between Agouti-related protein and proopiomelanocortin in brain. J. Neurosci. 1999, 19:RC26.
8. Bell S.M., Stewart R.B., Thompson S.C., Meisch R.A. Food-deprivation increases cocaine-induced conditioned place preference and locomotor activity in rats. Psychopharmacology (Berl) 1997, 131:1-8.
9. Betley J.N., Cao Z.F., Ritola K.D., Sternson S.M. Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell 2013, 155:1337-1350.
10. Boghossian S., Park M., York D.A. Melanocortin activity in the amygdala controls appetite for dietary fat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R385-R393.
11. 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. U. S. A. 1998, 95:15043-15048.
12. Butler A.A. The melanocortin system and energy balance. Peptides 2006, 27:281-290.
13. Butler A.A., Kesterson R.A., Khong K., Cullen M.J., Pelleymounter M.A., Dekoning J., Baetscher M., Cone R.D. A unique metabolic syndrome causes obesity in the melanocortin-3 receptor-deficient mouse. Endocrinology 2000, 141:3518-3521.
14. Butler A.A., Marks D.L., Fan W., Kuhn C.M., Bartolome M., Cone R.D. Melanocortin-4 receptor is required for acute homeostatic responses to increased dietary fat. Nat. Neurosci. 2001, 4:605-611.
15. Cabeza de Vaca S., Hao J., Afroz T., Krahne L.L., Carr K.D. Feeding, body weight, and sensitivity to non-ingestive reward stimuli during and after 12-day continuous central infusions of melanocortin receptor ligands. Peptides 2005, 26:2314-2321.
16. Cabeza de Vaca S., Kim G.Y., Carr K.D. The melanocortin receptor agonist MTII augments the rewarding effect of amphetamine in ad-libitum-fed and food-restricted rats. Psychopharmacology (Berl) 2002, 161:77-85.
17. Carr K.D. Chronic food restriction: enhancing effects on drug reward and striatal cell signaling. Physiol. Behav. 2007, 91:459-472.
18. Carroll M.E. The role of food deprivation in the maintenance and reinstatement of cocaine-seeking behavior in rats. Drug Alcohol Depend. 1985, 16:95-109.
19. Carroll M.E., France C.P., Meisch R.A. Food deprivation increases oral and intravenous drug intake in rats. Science 1979, 205:319-321.
20. Chen A.S., Marsh D.J., Trumbauer M.E., Frazier E.G., Guan X.M., Yu H., Rosenblum C.I., Vongs A., Feng Y., Cao L., Metzger J.M., Strack A.M., Camacho R.E., Mellin T.N., Nunes C.N., Min W., Fisher J., Gopal-Truter S., MacIntyre D.E., Chen H.Y., Van der Ploeg L.H. Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat. Genet. 2000, 26:97-102.
21. Cone R.D. Anatomy and regulation of the central melanocortin system. Nat. Neurosci. 2005, 8:571-578.
22. Cone R.D. Studies on the physiological functions of the melanocortin system. Endocr. Rev. 2006, 27:736-749.
23. Cowley M.A., Pronchuk N., Fan W., Dinulescu D.M., Colmers W.F., Cone R.D. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 1999, 24:155-163.
24. Cremer M.C., De Barioglio S.R., Celis M.E. Interaction between alpha-MSH and gabaergic agents upon striatal cAMP levels: an in vitro model. Peptides 1998, 19:383-388.
25. Cui H., Lutter M. The expression of MC4Rs in D1R neurons regulates food intake and locomotor sensitization to cocaine. Genes Brain Behav. 2013, 12:658-665.
26. Cui H., Mason B.L., Lee C., Nishi A., Elmquist J.K., Lutter M. Melanocortin 4 receptor signaling in dopamine 1 receptor neurons is required for procedural memory learning. Physiol. Behav. 2012, 106:201-210.
27. Davis J.F., Choi D.L., Shurdak J.D., Krause E.G., Fitzgerald M.F., Lipton J.W., Sakai R.R., Benoit S.C. Central melanocortins modulate mesocorticolimbic activity and food seeking behavior in the rat. Physiol. Behav. 2011, 102:491-495.
28. Dietrich M.O., Bober J., Ferreira J.G., Tellez L.A., Mineur Y.S., Souza D.O., Gao X.B., Picciotto M.R., Araujo I., Liu Z.W., Horvath T.L. AgRP neurons regulate development of dopamine neuronal plasticity and nonfood-associated behaviors. Nat. Neurosci. 2012, 15:1108-1110.
29. DiLeone R.J., Taylor J.R., Picciotto M.R. The drive to eat: comparisons and distinctions between mechanisms of food reward and drug addiction. Nat. Neurosci. 2012, 15:1330-1335.
30. Fan W., Boston B.A., Kesterson R.A., Hruby V.J., Cone R.D. Role of melanocortinergic neurons in feeding and the agouti obesity syndrome. Nature 1997, 385:165-168.
31. Farooqi I.S., Keogh J.M., Yeo G.S., Lank E.J., Cheetham T., O'Rahilly S. Clinical spectrum of obesity and mutations in the melanocortin 4 receptor gene. N. Engl. J. Med. 2003, 348:1085-1095.
32. Fulton S., Woodside B., Shizgal P. Modulation of brain reward circuitry by leptin. Science 2000, 287:125-128.
33. Gantz I., Konda Y., Tashiro T., Shimoto Y., Miwa H., Munzert G., Watson S.J., DelValle J., Yamada T. Molecular cloning of a novel melanocortin receptor. J. Biol. Chem. 1993, 268:8246-8250.
34. Gantz I., Miwa H., Konda Y., Shimoto Y., Tashiro T., Watson S.J., DelValle J., Yamada T. Molecular cloning, expression, and gene localization of a fourth melanocortin receptor. J. Biol. Chem. 1993, 268:15174-15179.
35. Grace A.A., Floresco S.B., Goto Y., Lodge D.J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 2007, 30:220-227.
36. Hsu R., Taylor J.R., Newton S.S., Alvaro J.D., Haile C., Han G., Hruby V.J., Nestler E.J., Duman R.S. Blockade of melanocortin transmission inhibits cocaine reward. Eur. J. Neurosci. 2005, 21:2233-2242.
37. Huszar D., Lynch C.A., Fairchild-Huntress V., Dunmore J.H., Fang Q., Berkemeier L.R., Gu W., Kesterson R.A., Boston B.A., Cone R.D., Smith F.J., Campfield L.A., Burn P., Lee F. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 1997, 88:131-141.
38. Jansone B., Bergstrom L., Svirskis S., Lindblom J., Klusa V., Wikberg J.E. Opposite effects of gamma(1)- and gamma(2)-melanocyte stimulating hormone on regulation of the dopaminergic mesolimbic system in rats. Neurosci. Lett. 2004, 361:68-71.
39. Jewett D.C., Cleary J., Levine A.S., Schaal D.W., Thompson T. Effects of neuropeptide Y, insulin, 2-deoxyglucose, and food deprivation on food-motivated behavior. Psychopharmacology (Berl) 1995, 120:267-271.
40. Kenny P.J. Common cellular and molecular mechanisms in obesity and drug addiction. Nat. Rev. Neurosci. 2011, 12:638-651.
41. Kenny P.J. Reward mechanisms in obesity: new insights and future directions. Neuron 2011, 69:664-679.
42. King C.M., Hentges S.T. Relative number and distribution of murine hypothalamic proopiomelanocortin neurons innervating distinct target sites. PLoS ONE 2011, 6:e25864.
43. Kishi T., Aschkenasi C.J., Lee C.E., Mountjoy K.G., Saper C.B., Elmquist J.K. Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J. Comp. Neurol. 2003, 457:213-235.
44. Klusa V., Svirskis S., Opmane B., Muceniece R., Wikberg J.E. Behavioural responses of gamma-MSH peptides administered into the rat ventral tegmental area. Acta Physiol. Scand. 1999, 167:99-104.
45. Korotkova T.M., Brown R.E., Sergeeva O.A., Ponomarenko A.A., Haas H.L. Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur. J. Neurosci. 2006, 23:2677-2685.
46. Krashes M.J., Koda S., Ye C., Rogan S.C., Adams A.C., Cusher D.S., Maratos-Flier E., Roth B.L., Lowell B.B. Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J. Clin. Invest. 2011, 121:1424-1428.
47. Lee Y.S., Poh L.K., Loke K.Y. A novel melanocortin 3 receptor gene (MC3R) mutation associated with severe obesity. J. Clin. Endocrinol. Metab. 2002, 87:1423-1426.
48. Lerma-Cabrera J.M., Carvajal F., de la Torre L., de la Fuente L., Navarro M., Thiele T.E., Cubero I. Control of food intake by MC4-R signaling in the lateral hypothalamus, nucleus accumbens shell and ventral tegmental area: interactions with ethanol. Behav. Brain Res. 2012, 234:51-60.
49. Lezcano N.E., De Barioglio S.R., Celis M.E. alpha-MSH changes cyclic AMP levels in rat brain slices by an interaction with the D1 dopamine receptor. Peptides 1995, 16:133-137.
50. Lezcano N.E., de Barioglio S.R., de Velez B.M., Celis M.E. Independent and simultaneous effects of alpha-MSH and dopamine on cyclic AMP levels in rat brain slices. Peptides 1993, 14:53-57.
51. 2+-exchanger, NCKX4, in melanocortin-4-receptor-dependent satiety. J. Biol. Chem. 2014, 289:25445-25459.
52. Lim B.K., Huang K.W., Grueter B.A., Rothwell P.E., Malenka R.C. Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens. Nature 2012, 487:183-189.
53. Lindblom J., Opmane B., Mutulis F., Mutule I., Petrovska R., Klusa V., Bergstrom L., Wikberg J.E. The MC4 receptor mediates alpha-MSH induced release of nucleus accumbens dopamine. Neuroreport 2001, 12:2155-2158.
54. Lindblom J., Wikberg J.E., Bergstrom L. Alcohol-preferring AA rats show a derangement in their central melanocortin signalling system. Pharmacol. Biochem. Behav. 2002, 72:491-496.
55. Lippert R.N., Ellacott K.L., Cone R.D. Gender-specific roles for the melanocortin-3 receptor in the regulation of the mesolimbic dopamine system in mice. Endocrinology 2014, 155:1718-1727.
56. Liu H., Kishi T., Roseberry A.G., Cai X., Lee C.E., Montez J.M., Friedman J.M., Elmquist J.K. Transgenic mice expressing green fluorescent protein under the control of the melanocortin-4 receptor promoter. J. Neurosci. 2003, 23:7143-7154.
57. Liu J., Garza J.C., Li W., Lu X.Y. Melanocortin-4 receptor in the medial amygdala regulates emotional stress-induced anxiety-like behaviour, anorexia and corticosterone secretion. Int. J. Neuropsychopharmacol. 2013, 16:105-120.
58. Luscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
59. Mizuno T.M., Kleopoulos S.P., Bergen H.T., Roberts J.L., Priest C.A., Mobbs C.V. Hypothalamic pro-opiomelanocortin mRNA is reduced by fasting and [corrected] in ob/ob and db/db mice, but is stimulated by leptin. Diabetes 1998, 47:294-297.
60. Mizuno T.M., Mobbs C.V. Hypothalamic agouti-related protein messenger ribonucleic acid is inhibited by leptin and stimulated by fasting. Endocrinology 1999, 140:814-817.
61. Morikawa H., Paladini C.A. Dynamic regulation of midbrain dopamine neuron activity: intrinsic, synaptic, and plasticity mechanisms. Neuroscience 2011, 198:95-111.
62. Mul J.D., van Boxtel R., Bergen D.J., Brans M.A., Brakkee J.H., Toonen P.W., Garner K.M., Adan R.A., Cuppen E. Melanocortin receptor 4 deficiency affects body weight regulation, grooming behavior, and substrate preference in the rat. Obesity (Silver Spring) 2012, 20:612-621.
63. Navarro M., Cubero I., Chen A.S., Chen H.Y., Knapp D.J., Breese G.R., Marsh D.J., Thiele T.E. Effects of melanocortin receptor activation and blockade on ethanol intake: a possible role for the melanocortin-4 receptor. Alcohol Clin. Exp. Res. 2005, 29:949-957.
64. Navarro M., Cubero I., Knapp D.J., Thiele T.E. MTII-induced reduction of voluntary ethanol drinking is blocked by pretreatment with AgRP-(83-132). Neuropeptides 2003, 37:338-344.
65. Navarro M., Cubero I., Ko L., Thiele T.E. Deletion of agouti-related protein blunts ethanol self-administration and binge-like drinking in mice. Genes Brain Behav. 2009, 8:450-458.
66. Navarro M., Lerma-Cabrera J.M., Carvajal F., Lowery E.G., Cubero I., Thiele T.E. Assessment of voluntary ethanol consumption and the effects of a melanocortin (MC) receptor agonist on ethanol intake in mutant C57BL/6J mice lacking the MC-4 receptor. Alcohol Clin. Exp. Res. 2011, 35:1058-1066.
67. Obregon A.M., Amador P., Valladares M., Weisstaub G., Burrows R., Santos J.L. Melanocortin-3 receptor gene variants: association with childhood obesity and eating behavior in Chilean families. Nutrition 2010, 26:760-765.
68. Ollmann M.M., Wilson B.D., Yang Y.K., Kerns J.A., Chen Y., Gantz I., Barsh G.S. Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 1997, 278:135-138.
69. Oude Ophuis R.J., Boender A.J., van Rozen A.J., Adan R.A. Cannabinoid, melanocortin and opioid receptor expression on DRD1 and DRD2 subpopulations in rat striatum. Front. Neuroanat. 2014, 8:14.
70. Paladini C.A., Roeper J. Generating bursts (and pauses) in the dopamine midbrain neurons. Neuroscience 2014, 282C:109-121.
71. Panaro B.L., Cone R.D. Melanocortin-4 receptor mutations paradoxically reduce preference for palatable foods. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7050-7055.
72. Ploj K., Roman E., Kask A., Hyytia P., Schioth H.B., Wikberg J.E., Nylander I. Effects of melanocortin receptor ligands on ethanol intake and opioid peptide levels in alcohol-preferring AA rats. Brain Res. Bull. 2002, 59:97-104.
73. Roseberry A.G. Altered feeding and body weight following melanocortin administration to the ventral tegmental area in adult rats. Psychopharmacology (Berl) 2013, 226:25-34.
74. Roselli-Rehfuss L., Mountjoy K.G., Robbins L.S., Mortrud M.T., Low M.J., Tatro J.B., Entwistle M.L., Simerly R.B., Cone R.D. Identification of a receptor for gamma melanotropin and other proopiomelanocortin peptides in the hypothalamus and limbic system. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:8856-8860.
75. Samama P., Rumennik L., Grippo J.F. The melanocortin receptor MCR4 controls fat consumption. Regul. Pept. 2003, 113:85-88.
76. Sanchez M.S., Barontini M., Armando I., Celis M.E. Correlation of increased grooming behavior and motor activity with alterations in nigrostriatal and mesolimbic catecholamines after alpha-melanotropin and neuropeptide glutamine-isoleucine injection in the rat ventral tegmental area. Cell Mol. Neurobiol. 2001, 21:523-533.
77. Savastano D.M., Tanofsky-Kraff M., Han J.C., Ning C., Sorg R.A., Roza C.A., Wolkoff L.E., Anandalingam K., Jefferson-George K.S., Figueroa R.E., Sanford E.L., Brady S., Kozlosky M., Schoeller D.A., Yanovski J.A. Energy intake and energy expenditure among children with polymorphisms of the melanocortin-3 receptor. Am. J. Clin. Nutr. 2009, 90:912-920.
78. Schultz W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 1998, 80:1-27.
79. Shelkar G.P., Kale A.D., Singh U., Singru P.S., Subhedar N.K., Kokare D.M. Alpha-melanocyte stimulating hormone modulates ethanol self-administration in posterior ventral tegmental area through melanocortin-4 receptors. Addict. Biol. 2015, 20:302-315.
80. Shen Y., Fu W.Y., Cheng E.Y., Fu A.K., Ip N.Y. Melanocortin-4 receptor regulates hippocampal synaptic plasticity through a protein kinase A-dependent mechanism. J. Neurosci. 2013, 33:464-472.
81. Srisai D., Gillum M.P., Panaro B.L., Zhang X.M., Kotchabhakdi N., Shulman G.I., Ellacott K.L., Cone R.D. Characterization of the hyperphagic response to dietary fat in the MC4R knockout mouse. Endocrinology 2011, 152:890-902.
82. Sulzer D. How addictive drugs disrupt presynaptic dopamine neurotransmission. Neuron 2011, 69:628-649.
83. Takahashi K.A., Cone R.D. Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons. Endocrinology 2005, 146:1043-1047.
84. Tatro J.B. Melanotropin receptors in the brain are differentially distributed and recognize both corticotropin and alpha-melanocyte stimulating hormone. Brain Res. 1990, 536:124-132.
85. Torre E., Celis M.E. Alpha-MSH injected into the substantia nigra or intraventricularly alters behavior and the striatal dopaminergic activity. Neurochem. Int. 1986, 9:85-89.
86. Torre E., Celis M.E. Cholinergic mediation in the ventral tegmental area of alpha-melanotropin induced excessive grooming: changes of the dopamine activity in the nucleus accumbens and caudate putamen. Life Sci. 1988, 42:1651-1657.
87. Tracy A.L., Clegg D.J., Johnson J.D., Davidson T.L., Benoit S.C. The melanocortin antagonist AgRP (83-132) increases appetitive responding for a fat, but not a carbohydrate, reinforcer. Pharmacol. Biochem. Behav. 2008, 89:263-271.
88. Vaisse C., Clement K., Durand E., Hercberg S., Guy-Grand B., Froguel P. Melanocortin-4 receptor mutations are a frequent and heterogeneous cause of morbid obesity. J. Clin. Invest. 2000, 106:253-262.
89. van der Klaauw A.A., von dem Hagen E.A., Keogh J.M., Henning E., O'Rahilly S., Lawrence A.D., Calder A.J., Farooqi I.S. Obesity-associated melanocortin-4 receptor mutations are associated with changes in the brain response to food cues. J. Clin. Endocrinol. Metab. 2014, 99:E2101-E2106.
90. Van Wimersma Greidanus T.B., Maigret C., Torn M., Ronner E., Van der Kracht S., Van der Wee N.J., Versteeg D.H. Dopamine D-1 and D-2 receptor agonists and antagonists and neuropeptide-induced excessive grooming. Eur. J. Pharmacol. 1989, 173:227-231.
91. Vaughan C., Moore M., Haskell-Luevano C., Rowland N.E. Food motivated behavior of melanocortin-4 receptor knockout mice under a progressive ratio schedule. Peptides 2006, 27:2829-2835.
92. Volkow N.D., Wang G.J., Baler R.D. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn. Sci. 2011, 15:37-46.
93. Watabe-Uchida M., Zhu L., Ogawa S.K., Vamanrao A., Uchida N. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 2012, 74:858-873.
94. Wise R.A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 2004, 5:483-494.
95. Yang S.C., Shieh K.R. Differential effects of melanin concentrating hormone on the central dopaminergic neurons induced by the cocaine- and amphetamine-regulated transcript peptide. J. Neurochem. 2005, 92:637-646.
96. Yen H.H., Roseberry A.G. Decreased consumption of rewarding sucrose solutions after injection of melanocortins into the ventral tegmental area of rats. Psychopharmacology (Berl) 2015, 232:285-294.
97. Yetnikoff L., Lavezzi H.N., Reichard R.A., Zahm D.S. An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience 2014, 282C:23-48.