Estrogen receptor-α distribution in male rodents is associated with social organization

Journal of Comparative Neurology

Volumn 494, Issue 4, 2006, Pages 595-605

  Cushing, Bruce S ^a   Wynne Edwards, Katherine E ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

Bed nucleus of the stria terminalis; ER ; Medial amygdala; Microtus; Phodopus; Social monogamy

Indexed keywords

ESTROGEN RECEPTOR ALPHA;

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; IMMUNOREACTIVITY; MALE; MONOGAMY; NONHUMAN; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SOCIAL STRUCTURE; SPECIES DIFFERENCE; STRIA TERMINALIS; VIRILIZATION; VOLE;

AMYGDALA; ANIMALS; ARVICOLINAE; CRICETINAE; ESTROGEN RECEPTOR ALPHA; FEMALE; HIERARCHY, SOCIAL; MALE; PHODOPUS; SEPTAL NUCLEI; SEX CHARACTERISTICS; SOCIAL BEHAVIOR; SPECIES SPECIFICITY;

EID: 30144435643     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20826     Document Type: Article

References (79)

1. Arletti R, Bertolini A. 1985. Oxytocin stimulates lordosis behavior in female rats. Neuropeptides 6:247-253.
2. Bakker J, Honda SI, Harada N, Balthazart J. 2002. Sexual partner preference requires aromatase (Cyp19) gene in male mice. Horm Behav 42:158-171.
3. Bale TL, Dorsa DM. 1997. Cloning, novel promoter sequence, and estrogen regulation of a rat oxytocin receptor gene. Endocrinology 138:1151-1158.
4. Bamshad M, Novak MA, DeVries GJ. 1994. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiol Behav 56:751-758,
5. Caldwell JD, Prange AJ Jr, Pedersen CA. 1986. Oxytocin facilitates the sexual receptivity of estrogen-treated female rats. Neuropeptides 7:175-189.
6. Choleris E, Gustafsson J, Korach KS, Muglia LJ, Pfaff DW, Ogawa S. 2003. An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-α and -β knockout mice. Proc Natl Acad Sci U S A 100:6192-6197.
7. Coirini H, Johnson AE, McEwen BS. 1989. Estradiol modulation of oxytocin binding in the ventromedial hypothalamic nucleus of male and female rats. Neuroendocrinology 50:193-198.
8. Cushing BS, Carter CS. 2000. Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles. Horm Behav 37:49-56.
9. Cushing BS, Kramer KM. 2005. Microtines: a model system for studying the evolution and regulation of social monogamy. Acta Theriol Sin 25:182-199.
10. Cushing BS, Martin JO, Young LJ, Carter CS. 2001. The effects of peptides on partner preference formation are predicted by habitat in prairie voles. Horm Behav 39:48-58.
11. 1a receptors. J Neuroendocrinol 15:1021-1026.
12. Cushing BS, Razzoli M, Murphy AZ, Epperson PD, Le WW, Hoffman GE. 2004. Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two population of prairie voles. Brain Res 1016:247-254.
13. De Vries GJ, Villalba C. 1997. Brain sexual dimorphism and sex differences in parental and other social behaviors. Ann N Y Acad Sci 807:273-286.
14. De Vries GJ, Buijs RM, Sluitter AA. 1984. Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Res 298:141-145.
15. De Vries GJ, Buijs RM, Van Leeuwen FW, Caffe AR, Swaab DF. 1985. The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 233:236-254.
16. Dewsbury DA. 1981. An exercise in the prediction of monogamy in the field from laboratory data on 42 species of muriod rodents. Biologist 63:138-162.
17. 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.
18. Fowler CD, Johnson F, Wang Z. 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.
19. Funabashi T, Shinohara K, Mitsushima D, Kimura F. 2000. Estrogen increases arginine-vasopressin Via receptor mRNA in the preoptic area of young but not of middle-aged female rats. Neurosci Lett 285:205-208.
20. Getz LL, Carter CS, Gavish L. 1981. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding. Behav Ecol Sociobiol 8:189-194.
21. Han TM, De Vries GJ. 2003. Organizational effects of testosterone, estradiol, and dihydrotestostereone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J Neurobiol 54:502-510.
22. Hnatczuk OC, Lisciotto CA, DonCarlos LL, Carter CS, Morrell JI. 1994. Estrogen receptor immunoreactivity in specific brain areas of the prairie vole (Microtus ochrogaster) is altered by sexual receptivity and genetic sex. J Neuroendocrinol 6:81-100.
23. Hutchison JB. 1997. Gender-specific steroid metabolism in neural differentiation. Cell Mol Neurobiol 17:603-626.
24. Insel TR, Hulihan TJ. 1995. A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109:782-789.
25. Insel TR, Shapiro LE. 1992. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci U S A. 89:5981-5985.
26. Insel TR, Gelhard R, Shapiro LE. 1991. The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience 43:623-630.
27. Insel TR, Wang Z, Ferris CF. 1994. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14:5381-5392.
28. Insel TR, Winslow JT, Wang ZX, Young LJ. 1998. Oxytocin, vasopressin, and the neuroendocrine basis of pair bond formation. Adv Exp Med Biol 449:215-224.
29. Jannett FJ. 1980. Social dynamics of the montane vole, Microtus montanus, as a paradigm. Biologist 62:3-19.
30. Johnson AE. 1992. The regulation of oxytocin receptor binding in the ventromedial hypothalamic nucleus by gonadal steroids. Ann N Y Acad Sci 652:357-373.
31. Jones JS, Wynne-Edwards KE. 2000. Paternal hamsters mechanically assist the delivery, consume amniotic fluid and placenta, remove fetal membranes, and provide parental care during the birth process. Horm Behav 37:116-125.
32. Kawata M, Yuri K, Ozawa H, Nishi M, Ito T, Hu ZT, Lu HP, Yoshida M. 1998. Steroid hormones and their receptors in the brain. J Steroid Biochem Mol Biol 65:273-280.
33. Kendrick KM, Drewett RF. 1980. Testosterone-sensitive neurons respond to estradiol but not to dihydrotestosterone. Nature 286:67-68.
34. Kleiman D. 1977. Monogamy in mammals. Q Rev Biol 52:39-69.
35. Kudwa AE, Bodo C, Gustafsson JA, Rissman EF. 2005. A previously uncharacterized role for estrogen receptor β: defeminization of male brain and behavior. Proc Natl Acad Sci U S A 102:4608-4612.
36. Kuhnemann S, Brown TJ, Hochberg RB, MacLusky NJ. 1995. Sexual differentiation of estrogen receptor concentrations in the rat brain: effects of neonatal testosterone exposure. Brain Res 691:229-234.
37. Laflamme N, Nappi RE, Drolet G, Labrie C, Rivest S. 1998. Expression and neuropetidergic characterization of estrogen receptors (ERα and ERβ) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J Neurobiol 36:357-378.
38. Lauber AH, Mobbs CV, Muramatsu M, Pfaff DW. 1991. Estrogen-receptor messenger-RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 1293:180-186.
39. Lim MM, Wang ZX, Olazabal DE, Ren XH, Terwilliger EF, Young LJ. 2004. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429:754-757.
40. Lonstein JS, Rood BD, De Vries GJ. 2002. Parental responsiveness is feminized after neonatal castration in virgin male prairie voles, but not masculinized by perinatal testosterone in virgin females. Horm Behav 41:80-87.
41. Madison DM. 1980. Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav Ecol Sociobiol 7:65-71.
42. McGuire B. 1988. Effects of cross-fostering on parental behavior of meadow voles (Microtus pennsylvanicus). J Mammal 69:332-341.
43. McInroy JKE, Brousmiche DG, Wynne-Edwards KE. 2000. Fathers, fat and maternal energetics in a biparental hamster: paternal presence determines the outcome of a current reproductive effort and adipose tissue limits subsequent reproductive effort. Horm Behav 37:399-409.
44. Moffatt CA, Rissman EF, Shupnik MA, Blaustein JD. 1998. Induction of progestin receptors by estradiol in the forebrain of estrogen receptor-α gene-disrupted mice. J Neurosci 18:9556-9563.
45. Murphy AZ, Shupnik MA, Hoffman GE. 1995. Androgen and estrogen (a) receptor distribution in the periaqueductal gray of the male rat. Horm Behav 36:98-108.
46. Newman SW. 1999. The medial extended amygdala in male reproductive behavior-a node in the mammalian social behavior network. Ann N Y Acad Sci 877:242-257.
47. Ogawa S, Lubahn DB, Korach KS, Pfaff DW. 1997. Behavioral effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci U S A 94:1476-1481.
48. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW. 1998. Roles of estrogen receptor alpha gene expression in reproduction-related behaviors in female mice. Endocrinology 139:5070-5081.
49. Parker KJ, Lee TM. 2001. Social and environmental factors influence the suppression of pup-directed aggression and development of paternal behavior in captive meadow voles (Microtus pennsylvanicus). J Comp Psychol 115:331-336.
50. Plumari L, Viglietti-Panzica C, Allieri F, Honda S, Harada N, Absil P, Balthazart J, Panzica GC. 2002. Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J Neuroendocrinol 14:971-978.
51. Rasia-Filho AA, Londero RG, Achaval M. 2000. Functional activities of the amygdala: an overview. J Psych Neurosci 25:14-23.
52. Reburn CJ, Wynne-Edwards KE. 1999 Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav 35:163-176.
53. Rissman EF, Wersinger SR, Fugger HN, Foster TC. 1999. Sex with knock-out models: behavioral studies of estrogen receptor alpha. Brain Res 835:80-90.
54. Roselli CE, Chambers K. 1999. Sex differences in male-typical behaviors in response to androgen and estrogen treatments in rats. Neuroendocrinology 69:290-298.
55. Schreihofer DA, Resnick EM, Soh AY, Shupnik MA. 1999. Transcriptional regulation by a naturally occurring truncated rat estrogen receptor (ER), truncated ER product-1 (TERP-1). Mol Endocrinol 13:320-329.
56. Schum JE, Wynne-Edwards KE. 2005. Estradiol and progesterone in paternal and on-paternal hamsters (Phodopus) becoming fathers: conflict with hypothesized roles. Horm Behav 47:410-418.
57. Scordalakes EM, Rissmand EF. 2004. Aggression and arginine vasopressin immunoreactivity regulation by androgens receptor and estrogen receptor alpha. Genes Brain Behav 3:20-26.
58. Scordalakes EM, Imwalle DB, Rissman EF. 2002. Estrogen's masculine side: mediation of mating in male mice. Reproduction 124:331-338.
59. Shapiro RA, Xu C, Dorsa DM. 2000. Differential transcriptional regulation of rat vasopressin gene expression by estrogen receptor alpha and beta. Endocrinology 141:4056-4064.
60. Simerly RB, Chang C, Muramatsu M, Swanson LW. 1990. Distribution of androgen and estrogen receptors mRNA-containing cells in the rat brain: An in situ hybridization study. J Comp Neurol 294:76-95.
61. Storey AE, Bradbury CG, Joyce TL. 1994. Nest attendance in male meadow voles: The role of the female in regulating male interactions with pups. Anim Behav 49:1-10.
62. Trainor BC, Marier CA. 2002. Testosterone promotes parental behavior in a monogamous mammal via conversion to estrogen. Proc R Soc Lond B Biol Sci 269:823-829.
63. Vagell ME, McGinnis MY. 1998. The role of gonadal steroid receptors activation in the restoration of sociosexual behavior in adult male rats. Horm Behav 33:163-179.
64. Walton JM, Wynne-Edwards KE. 1998. Paternal care reduces maternal hyperthermia in Djungarian hamsters (Phodopus campbelli). Physiol Behav 63:41-47.
65. Wang ZX, De Vries GJ. 1993. Testosterone effects paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res 631:156-160.
66. Wang Z, 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.
67. Watson RE, Wiegand SJ, Clough RW, Hoffman GE. 1986. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155-159.
68. Wersinger SR, Rissman EF. 2000. Estrogen receptor alpha is essential for female-directed chemo-investigatory behavior but not required for the pheromone-induced luteinizing hormone surge in male mice. J Neuroendocrinol 12:103-110.
69. Wersinger SR, Sannen K, Villalba C, Lubahn DB, Rissman EF, De Vries GJ. 1997. Masculine sexual behavior is disrupted in ale and female mice lacking a functional estrogen receptor alpha gene. Horm Behav 32:176-183.
70. Williams JR, Insel TR, Harbaugh CR, Carter CS. 1994. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles. J Neuroendocrinol 6:247-250.
71. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR. 1993. A role for central vasopressin in pair bonding monogamous prairie voles. Nature 365:545-548.
72. Wynne-Edwards KE. 1995. Biparental care in Djungarian but not Siberian dwarf hamsters (Phodopus). Anim Behav 50:1571-1585.
73. Wynne-Edwards KE. 1998. Evolution of parental care in Phodopus: conflict between adaptations for survival and adaptations for rapid reproduction. Am Zool 38:238-250.
74. Wynne-Edwards KE. 2003. From dwarf hamster to daddy: the intersection of ecology, evolution and physiology that produces paternal behavior. Adv Study Behav 32:207-261.
75. Yamamoto Y, Carter CS, Cushing BS. 2005. Neonatal manipulation of oxytocin effects expression of estrogen receptor alpha. Neuroscience (in press).
76. Yokosuka, M, Okamura H, Hayashi S. 1997. Postnatal development and sex differences in neurons containing estrogen receptro-alpha immunoreactivity in the preoptic brain, the diencephalon, and the amygdala in the rat. J Comp Neurol 389:81-93.
77. Young LJ, Wang Z. 2004. The neurobiology of pair bonding. Nat Neurosci 10:1048-1054.
78. Young LJ, Winslow JT, Nilsen R, Insel TR. 1997. Species differences in Via receptor gene expression in monogmaous and non-monogamous voles: behavioral consequences. Behav Neurosci 111:599-605.
79. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR. 1999. Increased affiliative response to vasopressin in mice expressing the vasopressin receptor from a monogamous vole. Nature 400:766-768.