Neonatal melanocortin receptor agonist treatment reduces play fighting and promotes adult attachment in prairie voles in a sex-dependent manner

Neuropharmacology

Volumn 85, Issue , 2014, Pages 357-366

  Barrett, Catherine E ^a   Modi, Meera E ^a   Zhang, Billy C ^a   Walum, Hasse ^a   Inoue, Kiyoshi ^a   Young, Larry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Early experience; Melanocortin receptor; Melanotan II; Oxytocin; Prairie voles; Social behavior

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; EARLY GROWTH RESPONSE FACTOR 1; MELANOCORTIN RECEPTOR; MELANOCORTIN RECEPTOR AGONIST; MELANOTAN II; MESSENGER RNA; OXYTOCIN; OXYTOCIN RECEPTOR; PF 44687; UNCLASSIFIED DRUG; VASOPRESSIN V1A RECEPTOR; ALPHA INTERMEDIN; CYCLOPEPTIDE; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; MELANOTAN-II; PSYCHOTROPIC AGENT;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COHABITATION; CONTROLLED STUDY; CORTICOSTERONE RELEASE; EGR 1 GENE; EMOTIONAL ATTACHMENT; EXPLORATORY BEHAVIOR; FEMALE; FIGHTING; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; MALE; MICROTUS OCHROGASTER; NEWBORN; NONHUMAN; OT GENE; OTR GENE; PERINATAL PERIOD; PRIORITY JOURNAL; SEX DIFFERENCE; SOCIAL BONDING; SOCIAL EVOLUTION; VASOPRESSIN V1A RECEPTOR GENE; AGGRESSION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ARVICOLINAE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HYPOTHALAMUS; METABOLISM; NERVE CELL; PAIR BONDING; PHYSIOLOGY; RANDOMIZATION; RECREATION; SEXUAL DEVELOPMENT;

AGGRESSION; ALPHA-MSH; ANIMALS; ANIMALS, NEWBORN; ARVICOLINAE; BEHAVIOR, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; FEMALE; HYPOTHALAMUS; MALE; NEURONS; PAIR BOND; PEPTIDES, CYCLIC; PLAY AND PLAYTHINGS; PSYCHOTROPIC DRUGS; RANDOM ALLOCATION; RECEPTOR, MELANOCORTIN, TYPE 3; RECEPTOR, MELANOCORTIN, TYPE 4; SEX CHARACTERISTICS;

EID: 84903180693     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.05.041     Document Type: Article

References (85)

1. G.R. Acker, J. Berran, and F.L. Strand ACTH neuromodulation of the developing motor system and neonatal learning in the rat Peptides 6 Suppl. 2 1985 41 49 (Pubitemid 16211106)
2. T.H. Ahern, M.E. Modi, J.P. Burkett, and L.J. Young Evaluation of two automated metrics for analyzing partner preference tests J. Neurosci. Methods 182 2009 180 188
3. T.H. Ahern, and L.J. Young The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster) Front. Behav. Neurosci. 3 2009 17
4. J.D. Alvaro, J.B. Tatro, and R.S. Duman Melanocortins and opiate addiction Life Sci. 61 1997 1 9 (Pubitemid 27288314)
5. J.D. Alvaro, J.B. Tatro, J.M. Quillan, M. Fogliano, M. Eisenhard, M.R. Lerner, E.J. Nestler, and R.S. Duman Morphine down-regulates melanocortin-4 receptor expression in brain regions that mediate opiate addiction Mol. Pharmacol. 50 1996 583 591 (Pubitemid 26303589)
6. B.J. Aragona, Y. Liu, Y.J. Yu, J.T. Curtis, J.M. Detwiler, T.R. Insel, and Z. Wang Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds Nat. Neurosci. 9 2006 133 139 (Pubitemid 43011919)
7. A. Argiolas, M.R. Melis, S. Murgia, and H.B. Schioth ACTH- and alpha-MSH-induced grooming, stretching, yawning and penile erection in male rats: site of action in the brain and role of melanocortin receptors Brain Res. Bull. 51 2000 425 431 (Pubitemid 30133216)
8. R. Arletti, A. Benelli, and A. Bertolini Influence of oxytocin on feeding behavior in the rat Peptides 10 1989 89 93 (Pubitemid 19108042)
9. K.L. Bales, and C.S. Carter Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster) Behav. Neurosci. 117 2003 854 859 (Pubitemid 36935395)
10. K.L. Bales, and C.S. Carter Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster) Horm. Behav. 44 2003 178 184 (Pubitemid 37371973)
11. K.L. Bales, J.A. van Westerhuyzen, A.D. Lewis-Reese, N.D. Grotte, J.A. Lanter, and C.S. Carter Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles Horm. Behav. 52 2007 274 279 (Pubitemid 47088456)
12. B.E. Beckwith, R.K. O'Quin, M.S. Petro, A.J. Kastin, and C.A. Sandman The effects of neonatal injections of alpha-MSH on the open-field behavior of juvenile and adult rats Physiol. Psych. 5 1977 295 299 (Pubitemid 8214799)
13. B.E. Beckwith, C.A. Sandman, D. Hothersall, and A.J. Kastin Influence of neonatal injections of alpha-MSH on learning, memory and attention in rats Physiol. Behav. 18 1977 63 71 (Pubitemid 8068312)
14. Y. Ben-Barak, J.T. Russell, M.H. Whitnall, K. Ozato, and H. Gainer Neurophysin in the hypothalamo-neurohypophysial system. I. Production and characterization of monoclonal antibodies J. Neurosci. 5 1985 81 97 (Pubitemid 15155673)
15. O.J. Bosch, H.P. Nair, T.H. Ahern, I.D. Neumann, and L.J. Young The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent Neuropsychopharmacology 34 2009 1406 1415
16. I. Branchi, J.P. Curley, I. D'Andrea, F. Cirulli, F.A. Champagne, and E. Alleva Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels Psychoneuroendocrinology 38 2013 522 532
17. K.L. Brunson, N. Khan, M. Eghbal-Ahmadi, and T.Z. Baram Corticotropin (ACTH) acts directly on amygdala neurons to down-regulate corticotropin- releasing hormone gene expression Ann. Neurol. 49 2001 304 312 (Pubitemid 32202783)
18. J.P. Burkett, L.L. Spiegel, K. Inoue, A.Z. Murphy, and L.J. Young Activation of mu-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles Neuropsychopharmacology 36 2011 2200 2210
19. J.P. Burkett, and L.J. Young The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction Psychopharmacol. Berl. 224 2012 1 26
20. M. Caba, M.J. Rovirosa, and R. Silver Suckling and genital stroking induces Fos expression in hypothalamic oxytocinergic neurons of rabbit pups Brain Res. Dev. Brain Res. 143 2003 119 128 (Pubitemid 36835856)
21. C.S. Carter, E.M. Boone, H. Pournajafi-Nazarloo, and K.L. Bales Consequences of early experiences and exposure to oxytocin and vasopressin are sexually dimorphic Dev. Neurosci. 31 2009 332 341
22. C.S. Carter, D.M. Witt, E.G. Thompson, and K. Carlstead Effects of hormonal, sexual, and social history on mating and pair bonding in prairie voles Physiol. Behav. 44 1988 691 697 (Pubitemid 19037731)
23. S. Chaki, and S. Okuyama Involvement of melanocortin-4 receptor in anxiety and depression Peptides 26 2005 1952 1964 (Pubitemid 41354554)
24. T.F. Champney, T.L. Sahley, and C.A. Sandman Effects of neonatal cerebral ventricular injection of ACTH 4-9 and subsequent adult injections on learning in male and female albino rats Pharmacol. Biochem Behav. 5 1976 3 9
25. M.J. Chau, A.I. Stone, S.P. Mendoza, and K.L. Bales Is play behavior sexually dimorphic in monogamous species? Ethology 114 2008 989 998
26. A.S. Chen, D.J. Marsh, M.E. Trumbauer, E.G. Frazier, X.M. Guan, H. Yu, C.I. Rosenblum, A. Vongs, Y. Feng, L. Cao, J.M. Metzger, A.M. Strack, R.E. Camacho, T.N. Mellin, C.N. Nunes, W. Min, J. Fisher, S. Gopal-Truter, D.E. MacIntyre, H.Y. Chen, and L.H. Van der Ploeg Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass Nat. Genet. 26 2000 97 102
27. B.S. Cushing, K. Levine, and N.L. Cushing Neonatal manipulation of oxytocin influences female reproductive behavior and success Horm. Behav. 47 2005 22 28 (Pubitemid 39592616)
28. S.R. De Barioglio, N. Lezcano, and M.E. Celis Alpha MSH-induced excessive grooming behavior involves a GABAergic mechanism Peptides 12 1991 203 205
29. W.S. Dhillo, C.J. Small, L.J. Seal, M.S. Kim, S.A. Stanley, K.G. Murphy, M.A. Ghatei, and S.R. Bloom The hypothalamic melanocortin system stimulates the hypothalamo-pituitary-adrenal axis in vitro and in vivo in male rats Neuroendocrinology 75 2002 209 216 (Pubitemid 34455094)
30. M.N. Edelmann, C.H. Demers, and A.P. Auger Maternal touch moderates sex differences in juvenile social play behavior PLoS One 8 2013 e57396
31. C. Egles, F. Rene, S. Varon, J.C. Louis, J.M. Felix, and S. Schimchowitsch Differentiation of rat hypothalamic dopaminergic neurons is stimulated in vitro by target cells: the melanotrophs Eur. J. Neurosci. 10 1998 1270 1281 (Pubitemid 28330569)
32. K. Felszeghy, M. Sasvari, and C. Nyakas Behavioral depression: opposite effects of neonatal dexamethasone and ACTH-(4-9) analogue (ORG 2766) treatments in the rat Horm. Behav. 27 1993 380 396 (Pubitemid 23281958)
33. L. Gavish, C.S. Carter, and L.L. Getz Male-female interactions in prairie voles Anim. Behav. 31 1983 511 517
34. M.M. Glavas, S.E. Joachim, S.J. Draper, M.S. Smith, and K.L. Grove Melanocortinergic activation by melanotan II inhibits feeding and increases uncoupling protein 1 messenger ribonucleic acid in the developing rat Endocrinology 148 2007 3279 3287 (Pubitemid 46996975)
35. F. Gomez-Pinilla, S. Vaynman, and Z. Ying Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition Eur. J. Neurosci. 28 2008 2278 2287
36. B.B. Gorzalka, and G.L. Lester Oxytocin-induced facilitation of lordosis behaviour in rats is progesterone-dependent Neuropeptides 10 1987 55 65 (Pubitemid 17130245)
37. Y. Greenman, Y. Kuperman, Y. Drori, S.L. Asa, I. Navon, O. Forkosh, S. Gil, N. Stern, and A. Chen Postnatal ablation of POMC neurons induces an obese phenotype characterized by decreased food intake and enhanced anxiety-like behavior Mol. Endocrinol. 27 2013 1091 1102
38. R. Hsu, J.R. Taylor, S.S. Newton, J.D. Alvaro, C. Haile, G. Han, V.J. Hruby, E.J. Nestler, and R.S. Duman Blockade of melanocortin transmission inhibits cocaine reward Eur. J. Neurosci. 21 2005 2233 2242 (Pubitemid 40695248)
39. D. Huszar, C.A. Lynch, V. Fairchild-Huntress, J.H. Dunmore, Q. Fang, L.R. Berkemeier, W. Gu, R.A. Kesterson, B.A. Boston, R.D. Cone, F.J. Smith, L.A. Campfield, P. Burn, and F. Lee Targeted disruption of the melanocortin-4 receptor results in obesity in mice Cell 88 1997 131 141 (Pubitemid 27180337)
40. E.A. Joosten, S. Verhaagh, D. Martin, P. Robe, R. Franzen, M. Hooiveld, R. Doornbos, P.R. Bar, and G. Moonen Alpha-MSH stimulates neurite outgrowth of neonatal rat corticospinal neurons in vitro Brain Res. 736 1996 91 98 (Pubitemid 26356465)
41. A.C. Keebaugh, and L.J. Young Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults Horm. Behav. 60 2011 498 504
42. Y. Konda, I. Gantz, J. DelValle, Y. Shimoto, H. Miwa, and T. Yamada Interaction of dual intracellular signaling pathways activated by the melanocortin-3 receptor J. Biol. Chem. 269 1994 13162 13166 (Pubitemid 24206079)
43. K.M. Kramer, B.S. Cushing, and C.S. Carter Developmental effects of oxytocin on stress response: single versus repeated exposure Physiol. Behav. 79 2003 775 782 (Pubitemid 37087974)
44. M.I. Lansdell, D. Hepworth, A. Calabrese, A.D. Brown, J. Blagg, D.J. Burring, P. Wilson, D. Fradet, T.B. Brown, F. Quinton, N. Mistry, K. Tang, N. Mount, P. Stacey, N. Edmunds, C. Adams, S. Gaboardi, S. Neal-Morgan, C. Wayman, S. Cole, J. Phipps, M. Lewis, H. Verrier, V. Gillon, N. Feeder, A. Heatherington, S. Sultana, S. Haughie, S.W. Martin, M. Sudworth, and S. Tweedy Discovery of a selective small-molecule melanocortin-4 receptor agonist with efficacy in a pilot study of sexual dysfunction in humans J. Med. Chem. 53 2010 3183 3197
45. B.K. Lim, K.W. Huang, B.A. Grueter, P.E. Rothwell, and R.C. Malenka Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens Nature 487 2012 183 189
46. M.M. Lim, Y. Liu, A.E. Ryabinin, Y. Bai, Z. Wang, and L.J. Young CRF receptors in the nucleus accumbens modulate partner preference in prairie voles Horm. Behav. 51 2007 508 515 (Pubitemid 46550427)
47. J. Lindblom, A. Kask, E. Hagg, L. Harmark, L. Bergstrom, and J. Wikberg Chronic infusion of a melanocortin receptor agonist modulates dopamine receptor binding in the rat brain Pharmacol. Res. 45 2002 119 124 (Pubitemid 35428846)
48. J. Lindblom, B. Opmane, F. Mutulis, I. Mutule, R. Petrovska, V. Klusa, L. Bergstrom, and J.E. Wikberg The MC4 receptor mediates alpha-MSH induced release of nucleus accumbens dopamine Neuroreport 12 2001 2155 2158 (Pubitemid 32646263)
49. H. Liu, T. Kishi, A.G. Roseberry, X. Cai, C.E. Lee, J.M. Montez, J.M. Friedman, and J.K. Elmquist Transgenic mice expressing green fluorescent protein under the control of the melanocortin-4 receptor promoter J. Neurosci. 23 2003 7143 7154 (Pubitemid 36975878)
50. J. Liu, J.C. Garza, W. Li, and X.Y. Lu Melanocortin-4 receptor in the medial amygdala regulates emotional stress-induced anxiety-like behaviour, anorexia and corticosterone secretion Int. J. Neuropsychopharmacol. 16 2013 105 120
51. X.Y. Lu, G.S. Barsh, H. Akil, and S.J. Watson Interaction between alpha-melanocyte-stimulating hormone and corticotropin-releasing hormone in the regulation of feeding and hypothalamo-pituitary-adrenal responses J. Neurosci. 23 2003 7863 7872 (Pubitemid 37052354)
52. L.A. McGraw, and L.J. Young The prairie vole: an emerging model organism for understanding the social brain Trends Neurosci. 33 2010 103 109
53. M.R. Melis, A. Argiolas, and G.L. Gessa Oxytocin-induced penile erection and yawning: site of action in the brain Brain Res. 398 1986 259 265 (Pubitemid 17210169)
54. Modi, M. E., K. Inoue, C. E. Barrett, K. A. Kittelberger, D. G. Smith, R. Landgraf and L. J. Young, Unpublished results. Melanocortin Receptor Agonists Enhance Oxytocin-dependent Partner Preference Formation in the Prairie Vole.
55. C.L. Moore, and K.L. Power Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring Dev. Psychobiol. 25 1992 165 182
56. K.G. Mountjoy Distribution and function of melanocortin receptors within the brain Adv. Exp. Med. Biol. 681 2010 29 48
57. R. Muceniece, L. Zvejniece, R. Vilskersts, E. Liepinsh, L. Baumane, I. Kalvinsh, J.E. Wikberg, and M. Dambrova Functional evaluation of THIQ, a melanocortin 4 receptor agonist, in models of food intake and inflammation Basic Clin. Pharmacol. Toxicol. 101 2007 416 420 (Pubitemid 350135344)
58. J.R. Nicholson, J.C. Peter, A.C. Lecourt, Y.A. Barde, and K.G. Hofbauer Melanocortin-4 receptor activation stimulates hypothalamic brain-derived neurotrophic factor release to regulate food intake, body temperature and cardiovascular function J. Neuroendocrinol. 19 2007 974 982 (Pubitemid 350131084)
59. S.A. Nickolls, B. Fleck, S.R. Hoare, and R.A. Maki Functional selectivity of melanocortin 4 receptor peptide and nonpeptide agonists: evidence for ligand-specific conformational states J. Pharmacol. Exp. Ther. 313 2005 1281 1288 (Pubitemid 40727033)
60. J. Oosterom, W.A. Nijenhuis, W.M. Schaaper, J. Slootstra, R.H. Meloen, W.H. Gispen, J.P. Burbach, and R.A. Adan Conformation of the core sequence in melanocortin peptides directs selectivity for the melanocortin MC3 and MC4 receptors J. Biol. Chem. 274 1999 16853 16860
61. J. Panksepp, and W.W. Beatty Social deprivation and play in rats Behav. Neural Biol. 30 1980 197 206
62. C.I. Parent, and M.J. Meaney The influence of natural variations in maternal care on play fighting in the rat Dev. Psychobiol. 50 2008 767 776
63. K.J. Parker, and D. Maestripieri Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates Neurosci. Biobehav Rev. 35 2011 1466 1483
64. R. Poggioli, A.V. Vergoni, and A. Bertolini ACTH-(1-24) and alpha-MSH antagonize feeding behavior stimulated by kappa opiate agonists Peptides 7 1986 843 848 (Pubitemid 17182352)
65. E.K. Polston, and M.S. Erskine Patterns of induction of the immediate-early genes c-fos and egr-1 in the female rat brain following differential amounts of mating stimulation Neuroendocrinology 62 1995 370 384
66. T.B. Poole, and J. Fish An investigation of individual, age and sexual differences in the play of Rattus norvegicus (Mammalia: Rodentia) J. Zool. 179 1976 249 259
67. A.S. Rossler, J.G. Pfaus, H.K. Kia, J. Bernabe, L. Alexandre, and F. Giuliano The melanocortin agonist, melanotan II, enhances proceptive sexual behaviors in the female rat Pharmacol. Biochem Behav. 85 2006 514 521 (Pubitemid 46097062)
68. M.G. Ruscio, T. Sweeny, J. Hazelton, P. Suppatkul, and C. Sue Carter Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles Horm. Behav. 51 2007 54 61 (Pubitemid 44838631)
69. N. Sabatier alpha-Melanocyte-stimulating hormone and oxytocin: a peptide signalling cascade in the hypothalamus J. Neuroendocrinol. 18 2006 703 710 (Pubitemid 44132618)
70. N. Sabatier, C. Caquineau, G. Dayanithi, P. Bull, A.J. Douglas, X.M. Guan, M. Jiang, L. Van der Ploeg, and G. Leng Alpha-melanocyte-stimulating hormone stimulates oxytocin release from the dendrites of hypothalamic neurons while inhibiting oxytocin release from their terminals in the neurohypophysis J. Neurosci. 23 2003 10351 10358 (Pubitemid 37444612)
71. Y. Shen, W.Y. Fu, E.Y. Cheng, A.K. Fu, and N.Y. Ip Melanocortin-4 receptor regulates hippocampal synaptic plasticity through a protein kinase A-dependent mechanism J. Neurosci. 33 2013 464 472
72. M.A. Smith, S.Y. Kim, H.J. van Oers, and S. Levine Maternal deprivation and stress induce immediate early genes in the infant rat brain Endocrinology 138 1997 4622 4628 (Pubitemid 27460896)
73. L.P. Spear, and S.C. Brake Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats Dev. Psychobiol. 16 1983 83 109 (Pubitemid 13144147)
74. J.M. Stribley, and C.S. Carter Developmental exposure to vasopressin increases aggression in adult prairie voles Proc. Natl. Acad. Sci. U. S. A. 96 1999 12601 12604 (Pubitemid 29513548)
75. Y.X. Tao The melanocortin-4 receptor: physiology, pharmacology, and pathophysiology Endocr. Rev. 31 2010 506 543
76. G.T. Taylor Fighting in juvenile rats and the ontogeny of agonistic behavior J. Comp. Physiol. Psychol. 94 1980 953 961 (Pubitemid 11248519)
77. A.J. Thody alpha-MSH and the regulation of melanocyte function Ann. N. Y. Acad. Sci. 885 1999 217 229
78. D.H. Thor, and W.R. Holloway Jr. Play-solicitation behavior in juvenile male and female rats Animal Leaning Behav. 11 1983 173 178
79. A.H. Veenema, and I.D. Neumann Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats Psychoneuroendocrinology 34 2009 463 467
80. J. Wang, F. Tai, X. Yan, and P. Yu Paternal deprivation alters play-fighting, serum corticosterone and the expression of hypothalamic vasopressin and oxytocin in juvenile male mandarin voles J. Comp. Physiol. a Neuroethol. Sens. Neural Behav. Physiol. 198 2012 787 796
81. J.E. Wikberg, R. Muceniece, I. Mandrika, P. Prusis, J. Lindblom, C. Post, and A. Skottner New aspects on the melanocortins and their receptors Pharmacol. Res. 42 2000 393 420
82. J.R. Williams, K.C. Catania, and C.S. Carter Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience Horm. Behav. 26 1992 339 349
83. C.S. Wu, D.R. Greenwood, J.M. Cooney, D.J. Jensen, M.A. Tatnell, G.J. Cooper, and K.G. Mountjoy Peripherally administered desacetyl alpha-MSH and alpha-MSH both influence postnatal rat growth and associated rat hypothalamic protein expression Am. J. Physiol. Endocrinol. Metab. 291 2006 E1372 E1380
84. B. Xu, E.H. Goulding, K. Zang, D. Cepoi, R.D. Cone, K.R. Jones, L.H. Tecott, and L.F. Reichardt Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor Nat. Neurosci. 6 2003 736 742 (Pubitemid 36792889)
85. L.J. Young, and Z. Wang The neurobiology of pair bonding Nat. Neurosci. 7 2004 1048 1054 (Pubitemid 41184443)