Species Differences in the Immunoreactive Expression of Oxytocin, Vasopressin, Tyrosine Hydroxylase and Estrogen Receptor Alpha in the Brain of Mongolian Gerbils (Meriones unguiculatus) and Chinese Striped Hamsters (Cricetulus barabensis)

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Wang, Yu ^a,b   Xu, Linxi ^a,b   Pan, Yongliang ^a   Wang, Zuoxin ^c   Zhang, Zhibin ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; OXYTOCIN; TYROSINE 3 MONOOXYGENASE; VASOPRESSIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CHINESE HAMSTER; CONTROLLED STUDY; CRICETULUS BARABENSIS; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; FEMALE; GERBIL; HYPOTHALAMUS; IMMUNOREACTIVITY; MALE; MEDIAL PREOPTIC AREA; MERIONES UNGUICULATUS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEX DIFFERENCE; SOCIAL BEHAVIOR; SPECIES DIFFERENTIATION;

ANIMALS; ARGININE VASOPRESSIN; BEHAVIOR, ANIMAL; BRAIN; CRICETINAE; CRICETULUS; ESTROGEN RECEPTOR ALPHA; FEMALE; GERBILLINAE; MALE; OXYTOCIN; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; STAINING AND LABELING; TYROSINE 3-MONOOXYGENASE;

CRICETINAE; CRICETULUS BARABENSIS; MERIONES UNGUICULATUS;

EID: 84878779632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065807     Document Type: Article

References (124)

1. Bester-Meredith JK, Young LJ, Marler CA, (1999) Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 36: 25-38.
2. Xu LX, Pan YL, Young KA, Wang ZX, Zhang ZB, (2010) Oxytocin and vasopressin immunoreactive staining in the brains of Brandt's voles (Lasiopodomys brandtii) and greater long-tailed hamsters (Tscherskia triton). Neuroscience 169: 1235-1247.
3. Madison DM, Hill JP, Gleason PE, (1984) Seasonality in the nesting-behavior of Peromyscus leucopus. Am Midl Nat 112: 201-204.
4. Wang ZX, Hulihan TJ, Insel TR, (1997) Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Res 767: 321-332.
5. Insel TR, Shapiro LE, (1992) Oxytocin receptor distribution reflects social-organization in monogamous and polygamous voles. Proc Natl Acad Sci USA 89: 5981-5985.
6. Insel TR, Wang ZX, Ferris CF, (1994) Patterns of brain vasopressin receptor distribution associated with social-organization in microtine rodents. J Neurosci 14: 5381-5392.
7. Young KA, Liu Y, Wang ZX, (2008) The neurobiology of social attachment: A comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comp Biochem Phys C148: 401-410.
8. Aragona BJ, Liu Y, Curtis JT, Stephan FK, Wang ZX, (2002) A critical role for dopamine in pair bonding in male prairie voles. Horm Behav 41: 455-455.
9. Gingrich B, Liu Y, Cascio C, Wang ZX, Insel TR, (2000) Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav Neurosci 114: 173-183.
10. Wang ZX, Yu GZ, Cascio C, Liu Y, Gingrich B, et al. (1999) Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): A mechanism for pair bonding? Behav Neurosci 113: 602-611.
11. Cushing BS, Razzoli M, Murphy AZ, Epperson PM, Le WW, et al. (2004) Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two populations of prairie voles. Brain Res 1016: 247-254.
12. Cushing BS, Wynne-Edwards KE, (2006) Estrogen receptor-alpha distribution in male rodents is associated with social organization. J Comp Neurol 494: 595-605.
13. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, et al. (1998) Roles of estrogen receptor alpha gene expression in reproduction-related behaviors in female mice. Endocrinology 139: 5070-5081.
14. Cushing BS, Perry A, Musatov S, Ogawa S, Papademetriou E, (2008) Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior. J Neurosci 28: 10399-10403.
15. Trainor BC, Greiwe KM, Nelson RJ, (2006) Individual differences in estrogen receptor α in select brain nuclei are associated with individual differences in aggression. Horm Behav 50: 338-345.
16. Lei K, Cushing BS, Musatov S, Ogawa S, Kramer KM, (2010) Estrogen receptor-alpha in the bed nucleus of the stria terminalis regulates social affiliation in male prairie voles (Microtus ochrogaster). Plos One 5(1): e8931.
17. Lonstein JS, Greco B, De Vries G, Stern JM, Blaustein JD, (2000) Maternal behavior stimulates c-fos activity within estrogen receptor alpha-containing neurons in lactating rats. Neuroendocrinology 72: 91-101.
18. Rissman EF, (2008) Roles of oestrogen receptors alpha and beta in behavioural neuroendocrinology: Beyond yin/yang. J Neuroendocrinol 20: 873-879.
19. Bodo C, Kudwa AE, Rissman EF, (2006) Both estrogen receptor-alpha and-beta are required for sexual differentiation of the anteroventral periventricular area in mice. Endocrinology 147: 415-420.
20. Scordalakes EM, Rissman EF, (2004) Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha. Genes Brain Behav 3: 20-26.
21. Tetel MJ, Pfaff DW, (2010) Contributions of estrogen receptor-alpha and estrogen receptor-beta to the regulation of behavior. BBA-Gen Subjects 1800: 1084-1089.
22. Ferris CF, Melloni RH, Koppel G, Perry KW, Fuller RW, et al. (1997) Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J Neurosci 17: 4331-4340.
23. Wang ZX, Young LJ, De Vries GJ, Insel TR, (1998) Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 119: 483-499.
24. Bamshad M, Novak MA, Devries GJ, (1993) Sex and species-differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J Neuroendocrinol 5: 247-255.
25. Beery AK, Lacey EA, Francis DD, (2008) Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J Comp Neurol 507: 1847-1859.
26. Bester-Meredith JK, Marler CA, (2001) Vasopressin and aggression in cross-fostered California mice (Peromyscus californicus) and white-footed mice (Peromyscus leucopus). Horm Behav 40: 51-64.
27. Wang ZX, (1995) Species-differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Behav Neurosci 109: 305-311.
28. Wang ZX, Zhou L, Hulihan TJ, Insel TR, (1996) Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: A quantitative comparative study. J Comp Neurol 366: 726-737.
29. Bester-Meredith JK, Marler CA, (2003) Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered peromyscus mice. Behav Neurosci 117: 455-463.
30. Mallon DP, (1985) The mammals of the Mongolian People's Republic. Mamm Rev 15: 71-102.
31. Gromov IM, Gurejew AA, Nowukov GA, Sokolov II,Strelkov PP, et al. (1963) Fauna of the USSR. Moscow: Nauka Publ House. pp.513-528.
32. Luo ZX, Chen W, Gao W, Wang YX, Li CY, et al.(2000) Fauna sinica: Mammalia, vol. 6, rodentia, part iii, cricetidae. Beijing: Science Press.pp.121-128.[in Chinese].
33. Agren G, Zhou Q, Zhong W, (1989) Ecology and social-behavior of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China. Anim Behav 37: 11-27.
34. Agren G, Zhou Q, Zhong W, (1989) Territoriality, cooperation and resource priority- hoarding in the Mongolian gerbil, Meriones unguiculatus. Anim Behav 37: 28-32.
35. Wang MJ, Zhong WQ, Wan XR (1998) Ecology and management of Mongolian gerbils (Meriones unguiculatus). In: Zhang ZB, Wang ZW,editors. Ecology and management of rodent pests in agriculture.Beijing: Ocean Press. PP.221-236.[in Chinese].
36. Agren G, (1984) Pair formation in the Mongolian gerbil. Anim Behav 32: 528-535.
37. Elwood RW, (1975) Parental and maternal behaviour in the Mongolian gerbil. Anim Behav 23: 766-772.
38. Nyby J, Wallace P, Owen K, Thiessen DD, (1973) Influence of hormones on hoarding behavior in Mongolian gerbil (meriones-unguiculatus). Horm Behav 4: 283-288.
39. Prates EJ, Guerra RF, (2005) Parental care and sexual interactions in Mongolian gerbils (meriones unguiculatus) during the postpartum estrus. Behav Process 70: 104-112.
40. Bridges NJ, Starkey NJ, (2004) Sex differences in Mongolian gerbils in four tests of anxiety. Physiol Behav 83: 119-127.
41. Wang YZ, Lu HQ, Wang YS, Jiang LY (1998) Ecology and management of Chinese stripped hamsters (Cricetulus barabensis). In: Zhang ZB,Wang ZW,editors. Ecology and management of rodent pests in agriculture.Beijing: Ocean Press. PP.20-40.[in Chinese].
42. Skirrow MH, Rysan M, (1976) Observations on social-behavior of Chinese-hamster, Cricetulus griseus. Can J Zool 54: 361-368.
43. Pan YL, Xu LX, Wang ZX, Zhang ZB, (2011) Expression of oestrogen receptor alpha in the brain of Brandt's voles (Lasiopodomys brandtii): Sex differences and variations during ovarian cycles. J Neuroendocrinol 23: 926-932.
44. Fowler CD, Johnson F, Wang ZX, (2005) Estrogen regulation of cell proliferation and distribution of estrogen receptor-alpha in the brains of adult female prairie and meadow voles. J Comp Neurol 489: 166-179.
45. Elwood RW, Broom DM, (1978) Influence of litter size and parental behavior on development of Mongolian gerbil pups. Anim Behav 26: 438-454.
46. Gerling S, Yahr P, (1979) Effect of the male parent on pup survival in Mongolian gerbils (Meriones unguiculatus). Anim Behav 27: 310-311.
47. Liu W, Wang G, Wan XR, Zhong WQ, (2009) Effects of supplemental food on the social organization of Mongolian gerbils during the breeding season. J Zool 278: 249-257.
48. Xia W, Liao C, Zhong W, Sun C, Tian Y, (1982) On the population dynamics and regulation of Meriones unguiculatus in agricultural region north to Yin Mountains, Inner Mongolia. Acta Theriologica Sinica 2: 51-71 [in Chinese].
49. Ostermeyer MC, Elwood RW, (1984) Helpers- at the nest in the Mongolian gerbil, Meriones unguiculatus. Behaviour 91: 61-77.
50. Sorensen DB, Krohn T, Hansen HN, Ottesen JL, Hansen AK, (2005) An ethological approach to housing requirements of golden hamsters, Mongolian gerbils and fat sand rats in the laboratory- a review. Appl Anim Behav Sci 94: 181-195.
51. Ferris CF, Potegal M, (1988) Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol Behav 44: 235-239.
52. Riters LV, Panksepp J (1997) Effects of vasotocin on aggressive behavior in male japanese quail. In: Carter CS, Lederhendler II, Kirkpatrick B, editors. Integrative neurobiology of affiliation. pp. 478-480.
53. Gobrogge KL, Liu Y, Young LJ, Wang ZX, (2009) Anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent. P Natl Acad Sci USA 106: 19144-19149.
54. Weitzman RE, Kleeman CR, (1979) Clinical physiology of water metabolism. 1. Physiologic regulation of arginine vasopressin secretion and thirst. West J Med 131: 373-400.
55. Dasilva RKP, Saad WA, Renzi A, Menani JV, Camargo LAD, (1995) Effect of lateral hypothalamus lesions on the water and salt intake, and sodium and urine excretion induced by activation of the median preoptic nucleus in conscious rats. J Auton Nerv Syst 53: 195-204.
56. Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, et al. (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. P Natl Acad Sci USA 92: 1013-1017.
57. Delgado JMR, Anand BK, (1953) Increase of food intake induced by electrical stimulation of the lateral hypothalamus. Am J Physiol 172: 162-168.
58. Caldwell JD, Jirikowski GF, Greer ER, Pedersen CA, (1989) Medial preoptic area oxytocin and female sexual receptivity. Behav Neurosci 103: 655
59. Caldwell JD, Moe BD, (1999) Conjugated estradiol increases female sexual receptivity in response to oxytocin infused into the medial preoptic area and medial basal hypothalamus. Horm Behav 35: 38-46.
60. Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA, (1994) Oxytocin activates the postpartum onset of rat maternal-behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108: 1163-1171.
61. Rosen GJ, De Vries GJ, Goldman SL, Goldman BD, Forger NG, (2008) Distribution of oxytocin in the brain of a eusocial rodent. Neuroscience 155: 809-817.
62. Popik P, van Ree JM, (1991) Oxytocin but not vasopressin facilitates social recognition following injection into the medial preoptic area of the rat brain. Eur Neuropsychopharm 1: 555-560.
63. Popik P, Vos PE, Vanree JM, (1992) Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat. Behav Pharmacol 3: 351-358.
64. Hennessey AC, Huhman KL, Albers HE, (1994) Vasopressin and sex-differences in hamster flank marking. Physiol Behav 55: 905-911.
65. Rosenblatt JS, Hazelwood S, Poole J, (1996) Maternal behavior in male rats: Effects of medial preoptic area lesions and presence of maternal aggression. Horm Behav 30 (3): 201-215.
66. Gammie SC, Nelson RJ, (1999) Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J Neurosci 19 (18): 8027-8035.
67. Harmon AC, Huhman KL, Moore TO, Albers HE, (2002) Oxytocin inhibits aggression in female Syrian hamsters. J Neuroendocrinol 14 (12): 963-969.
68. Gray P, Brooks PJ, (1984) Effect of lesion location within the medial preoptic-anterior hypothalamic continuum on maternal and male sexual behaviors in female rats. Behav Neurosci 98: 703-711.
69. Giuliano F, Rampin O, Brown K, Courtois F, Benoit G, et al. (1996) Stimulation of the medial preoptic area of the hypothalamus in the rat elicits increases in intracavernous pressure. Neurosci Lett 209: 1-4.
70. Reuss S, Hermes B, Fuchs E, Hiemke C, (1999) Day- and night-time contents of monoamines and their metabolites in the medial preoptic area of the rat hypothalamus. Neurosci Lett 266: 29-32.
71. McGinnis MY, Montana RC, Lumia AR, (2002) Effects of hydroxyflutamide in the medial preoptic area or lateral septum on reproductive behaviors in male rats. Brain Res Bull 59: 227-234.
72. Simerly RB, Swanson LW, Gorski RA, (1985) The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin-release- immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res 330: 55-64.
73. Schradin C, Anzenberger G, (1999) Prolactin, the hormone of paternity. News Physiol Sci 14: 223-231.
74. Simerly RB, Swanson LW, Handa RJ, Gorski RA, (1985) Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology 40: 501-510.
75. Simerly RB, (1989) Hormonal-control of the development and regulation of tyrosine-hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Mol Brain Res 6: 297-310.
76. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS, (1997) Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. P Natl Acad Sci USA 94: 14077-14082.
77. Zup SL, Carrier H, Waters EM, Tabor A, Bengston L, et al. (2003) Overexpression of Bcl-2 reduces sex differences in neuron number in the brain and spinal cord. J Neurosci 23: 2357-2362.
78. Wu RY, Yuan AF, Yuan QW, Guo R, Tai FD, et al. (2011) Comparison of sociability, parental care and central estrogen receptor alpha expression between two populations of mandarin voles (Microtus mandarinus). J Comp Physiol A 197: 267-277.
79. Plumari L, Viglietti-Panzica C, Allieri F, Honda S, Harada N, et al. (2002) Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J Neuroendocrinol 14: 971-978.
80. Dellovade TL, Zhu YS, Pfaff DW, (1999) Thyroid hormones and estrogen affect oxytocin gene expression in hypothalamic neurons. J Neuroendocrinol 11: 1-10.
81. Akaishi T, Sakuma Y, (1985) Estrogen excites oxytocinergic, but not vasopressinergic cells in the paraventricular nucleus of female rat hypothalamus. Brain Res 335: 302-305.
82. Young LJ, Wang ZX, Donaldson R, Rissman EF, (1998) Estrogen receptor alpha is essential for induction of oxytocin receptor by estrogen. Neuroreport 9: 933-936.
83. Panayotacopoulou MT, Raadsheer FC, Swaab DF, (1994) Colocalization of tyrosine-hydroxylase with oxytocin or vasopressin in neurons of the human paraventricular and supraoptic nucleus. Dev Brain Res 83: 59-66.
84. Dudas B, Semeniken KR, Merchenthaler I, (2006) Morphological substrate of the catecholaminergic input of the vasopressin neuronal system in humans. J Neuroendocrinol 18: 895-901.
85. Buccafusco JJ, Terry AV, (2000) Multiple central nervous system targets for eliciting beneficial effects on memory and cognition. J Pharmacol Exp Ther 295: 438-446.
86. Bartfai T, Iverfeldt K, Fisone G, Serfozo P, (1988) Regulation of the release of coexisting neurotransmitters. Annu Rev Pharmacol 28: 285-310.
87. Mohankumar PS, Thyagarajan S, Quadri SK, (1997) Tyrosine hydroxylase and DOPA decarboxylase activities in the medial preoptic area and arcuate nucleus during the estrous cycle: Effects of aging. Brain Res Bull 42: 265-271.
88. McDermott JL, Fischer J, Carter CS, (1980) Long-term estrogen and progesterone and mating stimuli as regulators of female sexual receptivity in the Mongolian gerbil. Behav Neural Biol 29: 63-72.
89. Yang YP, Li Y, Zhou YL, Li QH, (2002) Study on characteristics of artificial feeding and breeding habits of striped hamster. Journal of Inner Mongolia University (Natural Science Edition) Vol. 33: 201-204 [in Chinese].
90. Tabak J, Gonzalez-Iglesias AE, Toporikova N, Bertram R, Freeman ME, (2010) Variations in the response of pituitary lactotrophs to oxytocin during the rat estrous cycle. Endocrinology 151: 1806-1813.
91. Kawamata M, Tonomura Y, Kimura T, Yanagisawa T, Nishimori K, (2004) The differential coupling of oxytocin receptors to uterine contractions in murine estrous cycle. Biochem Biophys Res Commun 321: 695-699.
92. Shughrue PJ, Bushnell CD, Dorsa DM, (1992) Estrogen-receptor messenger-ribonucleic-acid in female rat-brain during the estrous-cycle- a comparison with ovariectomized females and intact males. Endocrinology 131: 381-388.
93. Simerly RB, Carr AM, Zee MC, Lorang D, (1996) Ovarian steroid regulation of estrogen and progesterone receptor messenger ribonucleic acid in the anteroventral periventricular nucleus of the rat. J Neuroendocrinol 8: 45-56.
94. Greco B, Allegretto EA, Tetel MJ, Blaustein JD, (2001) Coexpression of ER beta with ER alpha and progestin receptor proteins in the female rat forebrain: Effects of estradiol treatment. Endocrinology 142: 5172-5181.
95. Francis DD, Young LJ, Meaney MJ, Insel TR, (2002) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (v1a) receptors: Gender differences. J Neuroendocrinol 14: 349-353.
96. Olazabal DE, Young LJ, (2006) Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 141: 559-568.
97. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB, (1998) Hypothalamic paraventricular nucleus modulates maternal aggression in rats: Effects of ibotenic acid lesion and oxytocin antisense. Physiol Behav 63: 351-359.
98. Consiglio AR, Borsoi A, Pereira GAM, Lucion AB, (2005) Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol Behav 85: 354-362.
99. Ferris CF, Foote KB, Meltser HM, Plenby MG, Smith KL, et al. (1992) Oxytocin in the amygdala facilitates maternal aggression. Ann Ny Acad Sci 652: 456-457.
100. Ferguson JN, Aldag JM, Insel TR, Young LJ, (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21: 8278-8285.
101. Young LJ, Lim MM, Gingrich B, Insel TR, (2001) Cellular mechanisms of social attachment. Horm Behav 40: 133-138.
102. Liu Y, Wang ZX, (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121: 537-544.
103. Caldwell JD, Greer ER, Johnson MF, Prange AJ, Pedersen CA, (1987) Oxytocin and vasopressin immunoreactivity in hypothalamic and extrahypothalamic sites in late pregnant and postpartum rats. Neuroendocrinology 46: 39-47.
104. Gobrogge KL, Liu Y, Jia X, Wang Z, (2007) Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles. J Comp Neurol 502: 1109-1122.
105. Delville W, Mansour KM, Ferris CF, (1996) Testosterone facilitates aggression by modulating vasopressin receptors in the hypothalamus. Physiol Behav 60: 25-29.
106. Delville Y, De Vries GJ, Ferris CF, (2000) Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav Evolut 55: 53-76.
107. Caldwell HK, Albers HE, (2004) Effect of photoperiod on vasopressin-induced aggression in Syrian hamsters. Horm Behav 46: 444-449.
108. Engelmann M, Landgraf R, (1994) Microdialysis administration of vasopressin into the septum improves social recognition in brattleboro rats. Physiol Behav 55: 145-149.
109. Landgraf R, Frank E, Aldag JM, Neumann ID, Sharer CA, et al. (2003) Viral vector-mediated gene transfer of the vole v1a vasopressin receptor in the rat septum: Improved social discrimination and active social behaviour. Eur J Neurosci 18: 403-411.
110. Liu Y, Curtis JT, Wang ZX, (2001) Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (microtus ochrogaster). Behav Neurosci 115: 910-919.
111. Keer SE, Stern JM, (1999) Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 67: 659-669.
112. Numan M, Numan MJ, Pliakou N, Stolzenberg DS, Mullins OJ, et al. (2005) The effects of d1 or d2 dopamine receptor antagonism in the medial preoptic area, ventral pallidum, or nucleus accumbens on the maternal retrieval response and other aspects of maternal behavior in rats. Behav Neurosci 119: 1588-1604.
113. Silva MRP, Bernardi MM, Cruz-Casallas PE, Felicio LF, (2003) Pimozide injections into the nucleus accumbens disrupt maternal behaviour in lactating rats. Pharmacology & Toxicology 93: 42-47.
114. Hansen S, (1994) Maternal-behavior of female rats with 6-ohda lesions in the ventral striatum- characterization of the pup retrieval deficit. Physiol Behav 55: 615-620.
115. Lubin DA, Cannon JB, Black MC, Brown LE, Johns JM, (2003) Effects of chronic cocaine on monoamine levels in discrete brain structures of lactating rat dams. Pharmacol Biochem Be 74: 449-454.
116. Aragona BJ, Liu Y, Yu YJ, Curtis JT, Detwiler JM, et al. (2006) Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 9: 133-139.
117. Northcutt KV, Wang Z, Lonstein JS, (2007) Sex and species differences in tyrosine hydroxylase-synthesizing cells of the rodent olfactory extended amygdala. J Comp Neurol 500: 103-115.
118. Aragona BJ, Liu Y, Curtis T, Stephan FK, Wang ZX, (2003) A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. J Neurosci 23: 3483-3490.
119. Pfaus JG, Phillips AG, (1991) Role of dopamine in anticipatory and consummatory aspects of sexual-behavior in the male-rat. Behav Neurosci 105: 727-743.
120. Everitt BJ, (1990) Sexual motivation- a neural and behavioral-analysis of the mechanisms underlying appetitive and copulatory responses of male-rats. Neurosci Biobehav Rev 14: 217-232.
121. Warner RK, Thompson JT, Markowski VP, Loucks JA, Bazzett TJ, et al. (1991) Microinjection of the dopamine antagonist cis-flupentixol into the mpoa impairs copulation, penile reflexes and sexual motivation in male-rats. Brain Res 540: 177-182.
122. Pellis SM, Castaneda E, McKenna MM, Trannguyen LTL, Whishaw IQ, (1993) The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats. Neurosci Lett 158: 13-15.
123. Champagne FA, Weaver ICG, Diorio J, Dymov S, Szyf M, et al. (2006) Maternal care associated with methylation of the estrogen receptor-alpha 1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147: 2909-2915.
124. Spiteri T, Musatov S, Ogawa S, Ribeiro A, Pfaff DW, et al. (2010) Estrogen-induced sexual incentive motivation, proceptivity and receptivity depend on a functional estrogen receptor alpha in the ventromedial nucleus of the hypothalamus but not in the amygdala. Neuroendocrinology 91: 142-154.