Effects of castration on aggression and levels of serum sex hormones and their central receptors in mandarin voles (Microtus mandarinus)

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 198, Issue 5, 2012, Pages 347-362

  He, Fengqin ^a,b   Tai, Fadao ^a   Zhang, Yuhui ^a   Zhang, Xia ^a,c  

^a SHAANXI NORMAL UNIVERSITY   (China)

^b XI'AN UNIVERSITY OF ARTS AND SCIENCE   (China)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Androgen receptor; Estrogen receptor ; Estrogen receptor ; Mandarin vole Microtus mandarinus; Testosterone

Indexed keywords

SEX HORMONE; STEROID RECEPTOR;

AGGRESSION; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; ARVICOLINAE; BLOOD; BRAIN; CASTRATION; MALE; METABOLISM; PHYSIOLOGY; TISSUE DISTRIBUTION;

AGGRESSION; ANIMALS; ARVICOLINAE; BEHAVIOR, ANIMAL; BRAIN; CASTRATION; GONADAL STEROID HORMONES; MALE; RECEPTORS, STEROID; TISSUE DISTRIBUTION;

EID: 84862830369     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-012-0713-6     Document Type: Article

References (106)

1. Arteaga-Silva M, Rodríguez Dorantes M, Baig S, Morales Montor J (2007) Effects of castration and hormone replacement on male sexual behavior and pattern of expression in the brain of sex-steroid receptors in BALB/c AnN mice. Comp Biochem Physiol A Mol Integr Physiol 147: 607-615.
2. Bramley PS, Neaves WB (1972) The relationship between social status and reproductive activity in male impala, Aepyceros melampus. J Reprod Fertil 31: 77-81.
3. Bronson FH, Desjardins C (1968) Aggression in adult mice: modification by neonatal injections of gonadal hormones. Science 161: 705-706.
4. Buhl AE, Hasler JF, Tyler MC, Goldberg N, Banks EM (1978) The effects of social rank on reproductive indices in groups of male collared lemmings (Dicrostonyx groenlandicus). Biol Reprod 18: 317-324.
5. Caldwell GS, Glickman SE, Smith ER (1984) Seasonal aggression independent of seasonal testosterone in wood rats. Proc Natl Acad Sci USA 81: 5255-5257.
6. Choleris E, Gustafsson JA, 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-alpha and-beta knockout mice. Proc Natl Acad Sci USA 100: 6192-6197.
7. Clark AS, Barber DM (1994) Anabolic-androgenic steroids and aggression in castrated male rats. Physiol Behav 56: 1107-1113.
8. Clipperton Allen AE, Cragg CL, Wood AJ, Pfaff DW, Choleris E (2010) Agonistic behavior in males and females: Effects of an estrogen receptor beta agonist in gonadectomized and gonadally intact mice. Psychoneuroendocrinology 35: 1008-1022.
9. Cushing BS, Wynne-Edwards KE (2006) Estrogen receptor-distribution in male rodents is associated with social organization. J Comp Neurol 494: 595-605.
10. Cushing BS, Razzoli IM, Murphy AZ, Epperson PD, Hoffman GE (2004) Intraspecific variation in estrogen receptor alpha and the expression of male behavior in two population of prairie voles. Brain Res 1016: 247-254.
11. Davis DE (1959) Territorial rank in starlings. Anim Behav 7: 214-221.
12. de Wied D, Diamant M, Fodor M (1993) Central nervous system effects of the neurohypophyseal hormones and related peptides. Front Neuroendocrinol 14: 251-302.
13. Delville Y, De Vries GJ, Ferris CF (2000) Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav Evol 55: 53-76.
14. Demas GE, Moffatt CA, Drazen DL, Nelson RJ (1999) Castration does not inhibit aggressive behavior in adult male prairie voles (Microtus ochrogaster). Physiol Behav 66: 59-62.
15. Desjardins D, Persinger MA (1995) Association between intermale social aggression and cellular density within the central amygdaloid nucleus in rats with lithium/pilocarpine-induced seizures. Percept Mot Skills 81: 635-641.
16. Farkas G (2011) Surgical treatment of chronic pancreatitis, 2010. Magy Seb 64: 63-68.
17. Ferris CF, Melloni RH, Koppel G, Perry KW, Fuller RW, Delville Y (1997) Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J Neurosci 17: 4331-4340.
18. Grahm JM, Desjardins C (1980) Classical conditioning: induction of luteinizing hormone and testosterone secretion in anticipation of sexual activity. Science 210: 1039-1041.
19. Greco B, Edwards DA, Micheal RP, Clancy AN (1996) Androgen receptor immunoreactivity and mating-induced Fos expression in forebrain and midbrain structures in the male rat. Neuroscience 75: 161-171.
20. Greco B, Allegretto EA, Tetel MJ, Blaustein JD (2001) Co-expression of ER [beta] with ER [alpha] and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinol 142: 5172-5181.
21. Gubernick DJ, Nordby JC (1992) Parental influences on female puberty in the monogamous California mouse, Peromyscus californicus. Anim Behav 44: 259-267.
22. Hall JM, McDonnell DP (1999) The estrogen receptor beta-isoform (ER beta) of the human estrogen receptor modulates ER alpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140: 5566-5578.
23. Halpern CT, Udry JR, Suchindran C (1998) Monthly measures of salivary testosterone predict sexual activity in adolescent males. Arch Sex Behav 27: 445-465.
24. Hau M, Wikelski M, Soma KK, Wingfield JC (2000) Testosterone and year-round territorial aggression in a tropical bird. Gen Comp Endocrinol 117: 20-33.
25. Hau M, Stoddard ST, Soma KK (2004) Territorial aggression and hormones during the non-breeding season in a tropical bird. Horm Behav 45: 40-49.
26. He F, Tai F (2009) Mating behavior induces changes of expression of Fos protein, plasma testosterone and androgen receptors in the accessory olfactory bulb (AOB) of the male mandarin vole Microtus mandarinus. Current Zool 55: 288-295.
27. He F, Tai F, Zhang Y, An S (2004) The relationship between social behavior and the expression of estrogen receptor β and androgen receptor in olfactory-related brain regions of the male mandarin vole Microtus mandarinus and reed vole M. fostis. Acta Zool Sin 50: 165-175.
28. He F, Zhang J, Shi J, Wang B (2008) Changes of estrogen in serum and estrogen receptor β in the relevant brain regions following mating behavior of the male mandarin vole Microtus mandarinus. Zool Res 29: 529-536.
29. Hnatczuk OC, Lisciotto CA, DonCarlos LL, Carter CS, Morrell JI (1994) Estrogen and progesterone receptor immunoreactivity (ER-IR and PR-IR) in specific brain areas of the prairie vole (Microtus ochrogaster) is altered by sexual receptivity and genetic sex. J Neuroendocrinol 6: 89-100.
30. Hume JM, Wynne-Edwards KE (2005) Castration reduces male testosterone, estradiol, and territorial aggression, but not paternal behavior in biparental dwarf hamsters (Phodopus campbelli). Horm Behav 48: 303-310.
31. Imwalle DB, GustaVson JA, Rissman EF (2005) Lack of functional estrogen receptor beta influences anxiety behavior and serotonin content in female mice. Physiol Behav 84: 157-163.
32. Iqbal J, Swanson JJ, Prins GS, Jacobson CD (1995) Androgen receptor-like immunoreactivity in the Brazilian opossum brain and pituitary: distribution and effects of castration and testosterone replacement in the adult male. Brain Res 703: 1-18.
33. Jia R, Tai F, An S, Broders H, Sun R (2008) Neonatal manipulation of oxytocin influences the partner preference in mandarin voles (Microtus mandarinus). Neuropeptides 42: 525-533.
34. Kashon ML, Arbogast JA, Sisk CL (1996) Distribution and hormonal regulation of androgen receptor immunoreactivity in the forebrain of the male European ferret. J Comp Neurol 376: 567-586.
35. Kessel B (1957) A study of the breeding biology of the European starling (Sturnus vulgaris L.) in north America. Am Midland Nat 58: 257-331.
36. Klein SL, Hairston JE, DeVries AC, Nelson RJ (1997) Social environment and steroid hormones affect species and sex differences in immune function among voles. Horm Behav 32: 30-39.
37. Kollack-Walker S, Newman SW (1995) Mating and agonistic behavior produce different patters of Fos immunolabeling in the male Syrian hamster brain. Neuroscience 66: 721-736.
38. Kudryavtseva NN, Bondar NP, Avgustinovich DF (2002) Association between experience of aggression and anxiety in male mice. Behav Brain Res 133: 83-93.
39. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustaffson JA (1996) Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93: 5925-5930.
40. Lincoln GA, Guinness F, Short RV (1972) The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus eiaphus). Horm Behav 3: 375-396.
41. Liu MM, Albanese C, Anderson CM, Hilty K, Webb P, Uht RM, Price RH Jr, Pestell RG, Kushner PJ (2002) Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J Biol Chem 277: 24353-24360.
42. Lund TD, Rovis T, Chung WC, Handa RJ (2005) Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146: 797-807.
43. McEachern MB, McElreath RL, VanVuren DH, Eadie JM (2009) Another genetically promiscuous 'polygynous' mammal: mating system variation in Neotoma fuscipes. Anim Behav 77: 449-455.
44. Meek LR, Romeo RD, Novak CM, Sisk CL (1997) Actions of testosterone in prepubertal and postpubertal male hamsters: dissociation of effects on reproductive behavior and brain androgen receptor immunoreactivity. Horm Behav 31: 75-88.
45. Merchenthaler I, Lane M, Numan S, Dellovade T (2004) Distribution of estrogen receptor alpha and beta in the mouse central nervous system: in vivo autoradiographic and immunocytochemical analyses. J Comp Neurol 473: 270-291.
46. Mosselman S, Polman J, Dijkema R (1996) ERβ: identification and characterization of a novel human estrogen receptor. FEBS Lett 392: 49-53.
47. Nieminen P, Mustonen AM, Lindström-Seppä P, Kärkkäinen V, Mussalo-Rauhamaa H, Kukkonen JVK (2003) Phytosterols affect endocrinology and metabolism of the field vole (Microtus agrestis). Exp Biol Med 228: 188-193.
48. Nomura M, Durbak I, Chan J, Gustafsson JA, Smithies O, Korach KS, Pfaff DW, Ogawa S (2002) Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor beta knockout (ERKO) male mice. Horm Behav 41: 288-296.
49. Ogawa S, Lubahn DB, Korach KS, Pfaff DW (1998) Behavioral effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci USA 94: 1476-1481.
50. Ogawa S, Chan J, Chester AE, Gustafsson J, Korach KS, Pfaff DW (1999) Survival of reproductive behaviors in estrogen receptor beta gene-deficient (βERKO) male and female mice. Proc Natl Acad Sci USA 96: 12887-12892.
51. Ogawa S, Nomura M, Choleris E, Pfaff D (2005) The role of estrogen receptors in the regulation of aggressive behaviors. In: Nelson RJ (ed) Biology of Aggression. Oxford Univ Press, New York, pp 231-249.
52. Ohno S, Geller LN, Lai EV (1974) Tfm mutation and masculinization versus feminization of the mouse central nervous system. Cell 3: 235-242.
53. Payne AP, Swanson HH (1971) The effect of castration and ovarian implantation on aggressive behaviour of male hamsters. J Endocrinol 51: 217-218.
54. Pedraza-Alva G, Zingg JM, Donda A, Pérez-Martínez L (2009) Estrogen receptor regulates MyoD gene expression by preventing AP-1-mediated repression. Biochem Biophys Res Commun 389: 360-365.
55. Pinxten R, Ridder ED, Cock MD, Eens M (2003) Castration does not decrease nonreproductive aggression in yearling male European starlings (Sturnus vulgaris). Horm Behav 43: 394-401.
56. Prins GS, Birch L (1993) Immunocytochemical analysis of androgen receptors along the ducts of the separate rat prostate lobes after androgen withdraw and replacement. Endocrinology 132: 169-178.
57. Romeo RD, Schulz KM, Nelson AL, Menard TA, Sisk CL (2003) Testosterone, puberty, and the pattern of male aggression in Syrian hamsters. Dev Psychobiol 43: 102-108.
58. Rose RM, Holaday JW, Bernstein IS (1971) Plasma testosterone, dominance rank and aggressive behavior in male rhesus monkeys. Nature 231: 366-368.
59. Rose RM, Gordon TP, Bernstein IS (1972) Plasma testosterone levels in the male rhesus: influences of sexual and social stimuli. Science 178: 643-645.
60. Rzhevsky DI, Zhokhov SS, Babichenko II, Goleva AV, Goncharenko EN, Baizhumanov AA, Murashev AN, Lipkin VM, Kostanyan IA (2005) HLDF-6 peptide affects behavioral reactions and organism functions dependent on androgen hormones in normal and castrated male mice. Regul Pept 127: 111-121.
61. Santen RJ, Samojlik E, Demers L, Badder E (1980) Adrenal of male dog secretes androgens and estrogens. Am J Physiol 239: 109-112.
62. Sato T, Matsumoto T, Kawano H, Watanabe T, Uematsu Y, Sekine K, Fukuda T, Aihara K, Krust A, Yamada T, Nakamichi Y, Yamamoto Y, Nakamura T, Yoshimura K, Yoshizawa T, Metzger D, Chambon P, Kato S (2004) Brain masculinization requires androgen receptor function. Proc Natl Acad Sci USA 101: 1673-1678.
63. Schlinger BA, Arnold AP (1991) Brain is the major site of estrogen synthesis in a male songbird. Neurobiology 88: 4191-4194.
64. Schlinger BA, Callard GV (1990) Aromatization mediates aggressive behavior in quail. Gen Comp Endocrinol 79: 39-53.
65. Scordalakes EM, Rissman EF (2003) Aggression in male mice lacking functional estrogen receptor α. Behav Neurosci 117: 38-45.
66. Scordalakes EM, Rissman EF (2004) Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha. Genes Brain Behav 3: 20-26.
67. Scotti MAL, Belen J, Jackson JE, Demas GE (2008) The role of androgens in the mediation of seasonal territorial aggression in male Siberian hamsters (Phodopus sungorus). Physiol Behav 95: 633-640.
68. Sharma PK, Thakur MK (2006) Expression of estrogen receptor (ER) alpha and beta in mouse cerebral cortex: effect of age, sex and gonadal steroids. Neurobiol Aging 27: 880-887.
69. Siegel A, Roeling TAP, Gregg TR, Kruk MR (1999) Neuropharmacology of brain-stimulation-evoked aggression. Neurosci Biobehav Rev 23: 359-389.
70. Simon NG (2002) Hormonal processes in the development and expression of aggressive behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain, and behavior. Academic Press, New York, pp 339-392.
71. Simon N, Lu S, McKenna S, Chen X, Clifford A (1993) Sexual dimorphisms in regulatory systems for aggression. In: Haug M, Whalen R, Aron C, Olsen K (eds) The development of sex differences and similarities in behavior. Kluwer Academic Press, Boston, pp 389-408.
72. Simon N, McKenna S, Lu S, Cologer-Clifford A (1996) Development and expression of hormonal systems regulating aggression. Ann N Y Acad Sci 794: 8-17.
73. Simon NG, Cologer-Clifford A, Lu SF, McKenna SE, Hu S (1998) Testosterone and its metabolites modulate 5HT1A and 5HT1B agonist effects on intermale aggression. Neurosci Biobehav Rev 23: 325-336.
74. Simon NG, Mo Q, Hu S, Garippa C, Lu SF (2006) Hormonal pathways regulating intermale and inter-female aggression. Int Rev Neurobiol 73: 99-123.
75. Solomon NG, Keane B, Knoch LR, Hogan PJ (2004) Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster). Can J Zool 82: 1667-1671.
76. Solomon MB, Karom MC, Norvelle A, Markham CA, Erwin WD, Huhman KL (2009) Gonadal hormones modulate the display of conditioned defeat in male Syrian hamsters. Horm Behav 56: 423-428.
77. Soma KK, Tramontin AD, Wingfield JC (2000) Oestrogen regulates male aggression in the non-breeding season. Proc Biol Sci 267: 1089-1096.
78. Soma KK, Wissman AM, Brenowitz EA, Wingfield JC (2002) Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm Behav 41: 203-212.
79. Soma KK, Scotti MA, Newman AE, Charlier TD, Demas GE (2008) Novel mechanisms for neuroendocrine regulation of aggression. Front Neuroendocrinol 29: 476-489.
80. Song Z, Tai F, Yu C, Wu R, Zhang X, Broders H, He F, Guo R (2010) Sexual or paternal experiences alter alloparental behavior and the central expression of ERα and OT in male mandarin voles (Microtus mandarinus). Behav Brain Res 214: 290-300.
81. Soto AM, Lee H, Siiteri PK, Murai JT, Sonnenschein C (1984) Estrogen induction of progestophilins in rat estrogen-sensitive cells grown in media supplemented with sera from castrated rats and from rats bearing an α-fetoprotein-secreting hepatoma. Exp Cell Res 150: 390-399.
82. Sperry TS, Wacker DW, Wingfield JC (2010) The role of androgen receptors in regulating territorial aggression in male song sparrows. Horm Behav 57: 86-95.
83. Tai F, Wng T, Zhou Y (2001) Mate choice and related characteristics of mandarin voles Microtus mandarinus. Acta Zool Sin 47: 260-267.
84. Thieulant ML, Pelletier J (1979) Evidence for androgen and estrogen receptors in castrated ram pituitary cytosol: Influence of time after castration. J Steroid Biochem 10: 677-687.
85. Thomas CR, Bruce P, Bruce SM (1982) Sex differences in rat brain oestrogen and progestin receptors. Nature 300: 648-649.
86. Topping MG, Millar JS (1999) Mating success of male bushy-tailed woodrats when bigger is not always better. Behav Ecol 10: 161-168.
87. Trainor BC, Marler CA (2001) Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Horm Behav 40: 32-42.
88. Trainor BC, Bird IM, Marler CA (2004) Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm Behav 45: 115-121.
89. Trainor BC, Greiwe KM, Nelson RJ (2006a) Individual differences in estrogen receptor α in select brain nuclei are associated with individual differences in aggression. Horm Behav 50: 338-345.
90. Trainor BC, Kyomen HH, Marler CA (2006b) Estrogenic encounters: How interactions between aromatase and the environment modulate aggression. Front Neuroendocrinol 27: 170-179.
91. Trainor BC, Lin S, Finy MS, Rowland MR, Nelson RJ (2007) Photoperiod reverses the effects of estrogens on male aggression via genomic and non-genomic pathways. Proc Natl Acad Sci USA 104: 9840-9845.
92. Trainor BC, Finy MS, Nelson RJ (2008) Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice. Horm Behav 53: 192-199.
93. Veenema AH, Beiderbeck DI, Lukas M, Neumann ID (2010) Distinct correlations of vasopressin release within the lateral septum and the bed nucleus of the stria terminalis with the display of intermale aggression. Horm Behav 58: 273-281.
94. Vinke CM, Deijk RV, Houx BB, Schoemaker NJ (2008) The effects of surgical and chemical castration on intermale aggression, sexual behaviour and play behaviour in the male ferret (Mustela putorius furo). Appl Anim Behav Sci 115: 104-121.
95. Weihua Z, Saji S, Makinen S, Cheng G, Jensen EV, Warner M, Gustafsson JA (2000) Estrogen receptor (ER) beta, a modulator of ER alpha in the uterus. Proc Natl Acad Sci USA 97: 5936-5941.
96. Weiland NG, Orikasa C, Hayashi S, McEwen BS (1997) Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 388: 603-612.
97. Wersinger SR, Rissman EF (2000) Oestrogen receptor alpha is essential for female-directed chemo-investigatory behavior but is not required for the pheromone-induced luteinizing hormone surge in male mice. J Neuroendocrinol 12: 103-110.
98. White R, Lees JA, Needham M, Ham J, Parker M (1987) Structural organization of the mouse estrogen receptor. Mol Endocrinol 1: 735-744.
99. Wingfield JC, Hegner RE, Lewis D (1992) Hormonal responses to removal of a breeding male in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. Horm Behav 26: 145-155.
100. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365: 545-548.
101. Wood RI, Newman SW (1993) Intracellular partitioning of androgen receptor immunoreactivity in the brain of the male Syrian hamster: effects of castration and steroid replacement. J Neurobiol 24: 925-938.
102. Wood RI, Newman SW (1999) Androgen receptor immunoreactivity in the male and female Syrian hamster brain. J Neurobiol 39: 359-370.
103. Wu R, Yuan A, Yuan Q, Guo R, Tai F, Song Z, Yu C (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.
104. Zhai P, Xue H, Tai F, Jia R (2008) Inter-sexual variation in social interactions and distribution of estrogen receptor alpha in the brain of mandarin voles Microtus mandarinus. Acta Zool Sin 54: 1020-1028.
105. Zhou L, Blaustein JD, De Vries GJ (1994) Distribution of androgen receptor immunoreactivity in vasopressin and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134: 2622-2627.
106. Zielinski WJ, Vandenbergh JG (1993) Testosterone and competitive ability in male house mice, Mus musculus: laboratory and field studies. Anim Behav 45: 873-891.