Rapid effects of aggressive interactions on aromatase activity and oestradiol in discrete brain regions of wild male white-crowned sparrows

Journal of Neuroendocrinology

Volumn 23, Issue 8, 2011, Pages 742-753

  Charlier, T D ^a,b   Newman, A E M ^b   Heimovics, S A ^b   Po, K W L ^b   Saldanha, C J ^c   Soma, K K ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c LEHIGH UNIVERSITY   (United States)

Author keywords

Aggression; Estradiol; Estrogens; Hippocampus; Songbird

Indexed keywords

AROMATASE; ESTRADIOL;

AGGRESSION; AMYGDALOID NUCLEUS; ARTICLE; BRAIN; BRAIN REGION; BREEDING; CAUDAL MEDIAL NIDOPALLIUM; CENTRAL GRAY MATTER; CEREBELLUM; CHEMICAL INTERACTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; HORMONE BLOOD LEVEL; HYPOTHALAMUS NUCLEUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; MALE; MEDIAL MAGNOCELLULAR NUCLEUS OF THE ANTERIOR NIDOPALLIUM; MEDIAL PREOPTIC AREA; MESENCEPHALIC CENTRAL GREY; NONHUMAN; NUCLEUS TAENIAE OF THE AMYGDALA; OPTIC LOBE; PALKOVIT PUNCH TECHNIQUE; PRIORITY JOURNAL; ROBUST NUCLEUS OF ARCOPALLIUM; SEASON; SIMULATED TERRITORIAL INTRUSION; SIMULATION; SPARROW; STRIA TERMINALIS; TECHNIQUE; VENTROMEDIAL NUCLEUS OF THE HYPOTHALAMUS; WILD ANIMAL; ZONOTRICHIA LEUCOPHRYS PUGETENSIS;

AGGRESSION; ANIMALS; AROMATASE; BRAIN; ESTRADIOL; MALE; SEASONS; SEXUAL BEHAVIOR, ANIMAL; SPARROWS; TERRITORIALITY; TESTOSTERONE; VOCALIZATION, ANIMAL;

EID: 79960252908     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02170.x     Document Type: Article

References (89)

1. Naftolin F, Ryan KJ, Davies IJ, Petro Z, Kuhn M. The formation and metabolism of estrogens in brain tissue. Adv Biosci 1975; 15: 105-121.
2. Roselli CE, Liu M, Hurn PD. Brain aromatization: classic roles and new perspectives. Semin Reprod Med 2009; 27: 207-217.
3. Schlinger BA, Callard GV. Aromatization mediates aggressive behavior in quail. Gen Comp Endocrinol 1990; 79: 39-53.
4. Soma KK, Scotti MA, Newman AE, Charlier TD, Demas GE. Novel mechanisms for neuroendocrine regulation of aggression. Front Neuroendocrinol 2008; 29: 476-489.
5. Roselli CE, Resko JA. Sex differences in androgen-regulated expression of cytochrome P450 aromatase in the rat brain. J Steroid Biochem Mol Biol 1997; 61: 365-374.
6. Foidart A, Reid J, Absil P, Yoshimura N, Harada N, Balthazart J. Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J Chem Neuroanat 1995; 8: 267-282.
7. Wagner CK, Morrell JI. Neuroanatomical distribution of aromatase mRNA in the rat brain: indications of regional regulation. J Steroid Biochem Mol Biol 1997; 61: 307-314.
8. Saldanha CJ, Tuerk MJ, Kim YH, Fernandes AO, Arnold AP, Schlinger BA. Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J Comp Neurol 2000; 423: 619-630.
9. Metzdorf R, Gahr M, Fusani L. Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol 1999; 407: 115-129.
10. Balthazart J, Absil P, Foidart A, Houbart M, Harada N, Ball GF. Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J Neurobiol 1996; 31: 129-148.
11. Roselli CE, Abdelgadir SE, Resko JA. Regulation of aromatase gene expression in the adult rat brain. Brain Res Bull 1997; 44: 351-357.
12. Balthazart J. Steroid control and sexual differentiation of brain aromatase. J Steroid Biochem Mol Biol 1997; 61: 323-339.
13. Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD, Mendelson CR, Bulun SE. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 1994; 15: 342-355.
14. Balthazart J, Baillien M, Ball G. Phosphorylation processes mediate rapid changes of brain aromatase activity. J Steroid Biochem Mol Biol 2001; 79: 261-277.
15. Balthazart J, Baillien M, Charlier TD, Ball G. Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 2003; 17: 1591-1606.
16. Balthazart J, Baillien M, Ball GF. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 2006; 147: 359-366.
17. Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Dejace C, Ball GF, Balthazart J. Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 2005; 146: 3809-3820.
18. Balthazart J, Ball GF. Is brain estradiol a hormone or a neurotransmitter. Trends Neurosci 2006; 29: 241-249.
19. Cornil CA, Ball GF, Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 2006; 1126: 2-26.
20. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM. The nuclear receptor superfamily: the second decade. Cell 1995; 83: 835-839.
21. Kelly MJ, Moss RL, Dudley CA. The effects of microelectrophoretically applied estrogen, cortisol and acetylcholine on medial preoptic-septal unit activity throughout the estrous cycle of female rat. Exp Brain Res 1977; 30: 53-64.
22. Kelly MJ, Ronnekleiv OK. Membrane-initiated estrogen signaling in hypothalamic neurons. Mol Cell Endocrinol 2008; 290: 14-23.
23. Remage-Healey L, Bass AH. Rapid, hierarchical modulation of vocal patterning by steroid hormones. J Neurosci 2004; 24: 5892-5900.
24. Lord LD, Bond J, Thompson RR. Rapid steroid influences on visually guided sexual behavior in male goldfish. Horm Behav 2009; 56: 519-526.
25. Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Balthazart J. Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav Brain Res 2006; 66: 110-123.
26. Trainor BC, Lin S, Finy MS, Rowland MR, Nelson RJ. Photoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways. Proc Natl Acad Sci USA 2007; 104: 9840-9845.
27. Trainor BC, Finy MS, Nelson RJ. Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice. Horm Behav 2008; 53: 192-199.
28. Tremere LA, Jeong JK, Pinaud R. Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 2009; 29: 5949-5963.
29. Tremere LA, Pinaud R. Brain-generated estradiol drives long-term optimization of auditory coding to enhance the discrimination of communication signals. J Neurosci 2011; 31: 3271-3289.
30. Remage-Healey L, Maidment NT, Schlinger BA. Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 2008; 11: 1327-1334.
31. Charlier TD, Po KW, Newman AE, Shah AH, Saldanha CJ, Soma KK. 17beta-Estradiol levels in male zebra finch brain: combining Palkovits punch and an ultrasensitive radioimmunoassay. Gen Comp Endocrinol 2010; 167: 18-26.
32. Charlier TD, Underhill C, Hammond GL, Soma KK. Effects of aggressive encounters on plasma corticosteroid-binding globulin and its ligands in white-crowned sparrows. Horm Behav 2009; 56: 339-347.
33. Lynn SE, Hahn TP, Breuner CW. Free-living male mountain white-crowned sparrows exhibit territorial aggression without modulating total or free plasma testosterone. Condor 2007; 109: 173-180.
34. Wingfield JC, Hahn TP. Testosterone and territorial behavior in sedentary and migratory sparrrows. Anim Behav 1994; 47: 77-89.
35. Petrinovitch L, Patterson TL. The response of white-crowned sparrows to songs of different dialects and subspecies. Z Tierpsychol 1981; 57: 1-14.
36. Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 1973; 59: 449-450.
37. Vockel A, Prove E, Balthazart J. Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Res 1990; 511: 291-302.
38. Nixdorf-bergweiler BE, Bischof H-J. Stereotaxic Atlas of the Brain of the Zebra Finch, Taeniopygia guttata with Special Emphais on Telencephalic Visual and Song System Nuclei in Transverse and Sagital Sections. Bethesda, MD: National Center for Biotechnology Information, 2007.
39. Schumacher M, Contenti E, Balthazart J. Testosterone metabolism in discrete areas of the hypothalamus and adjacent brain regions of male and female Japanese quail. Brain Res 1983; 278: 337-340.
40. Thompson EA Jr, Siiteri PK. Utilization of oxygen and reduced nicotinamide adenine dinucleotide phosphate by human placental microsomes during aromatization of androstenedione. J Biol Chem 1974; 249: 5364-5372.
41. Roselli CE, Resko JA. In vitro assay of aromatase activity in the central nervous system. In: Greenstein B, ed. Neuroendocrine Research Methods. Chur: Harwood Academic Publishers, 1991: 937-951.
42. Silverin B, Baillien M, Balthazart J. Territorial aggression, circulating levels of testosterone, and brain aromatase activity in free-living pied flycatchers. Horm Behav 2004; 45: 225-234.
43. Silverin B, Baillien M, Foidart A, Balthazart J. Distribution of aromatase activity in the brain and peripheral tissues of passerine and nonpasserine avian species. Gen Comp Endocrinol 2000; 117: 34-53.
44. Newman AE, Chin EH, Schmidt KL, Bond L, Wynne-Edwards KE, Soma KK. Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen Comp Endocrinol 2008; 155: 503-510.
45. Schmidt KL, Soma KK. Cortisol and corticosterone in the songbird immune and nervous systems: local vs. systemic levels during development. Am J Physiol Regul Integr Comp Physiol 2008; 295: R103-R110.
46. Taves MD, Schmidt KL, Ruhr IM, Kapusta K, Prior NH, Soma KK. Steroid concentrations in plasma, whole blood and brain: effects of saline perfusion to remove blood contamination from brain. PLoS ONE 2011; 5: e15727.
47. Soma KK, Schlinger BA, Wingfiel JC, Saldanha CJ. Brain aromatase, 5α-reductase and 5β-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J Neurobiol 2003; 56: 209-221.
48. Schlinger BA, Slotow RH, Arnold AP. Plasma estrogens and brain aromatase in winter white-crowned sparrows. Ornis Scand 1992; 23: 292-297.
49. Balthazart J, Schumacher M, Evrard L. Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J Neuroendocrinol 1990; 2: 675-683.
50. Wacker DW, Wingfield JC, Davis JE, Meddle SL. Seasonal changes in aromatase and androgen receptor, but not estrogen receptor mRNA expression in the brain of the free-living male song sparrow, melospiza melodia morphna. J Comp Neurol 2010; 518: 3819-3835.
51. Trainor BC, Kyomen HH, Marler CA. Estrogenic encounters: how interaction between aromatase and the environment modulate agression. Front Neuroendocrinol 2006; 27: 170-179.
52. Soma KK. Testosterone and aggression: Berthold, birds and beyond. J Neuroendocrinol 2006; 18: 543-551.
53. Soma KK, Tramontin AD, Wingfield JC. Oestrogen regulates male aggression in the non-breeding season. Proc R Soc Lond B Biol Sci 2000; 267: 1089-1096.
54. Soma KK, Bindra RK, Gee J, Wingfield JC, Schlinger BA. Androgen-metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild song-bird. J Neurobiol 1999; 41: 176-188.
55. Harding CF, Walters MJ, Collado D, Sheridan K. Hormonal specificity and activation of social behavior in male red-winged blackbirds. Horm Behav 1988; 22: 402-418.
56. Soma KK, Sullivan KA, Tramontin AD, Saldanha CJ, Schlinger BA, Wingfield JC. Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and nonbreeding male song sparrows. J Comp Physiol A 2000; 186: 759-769.
57. Matsumoto T, Honda S, Harada N. Alteration in sex-specific behaviors in male mice lacking the aromatase gene. Neuroendocrinology 2003; 77: 416-424.
58. Toda K, Saibara T, Okada T, Onishi S, Shizuta Y. A loss of aggressive behaviour and its reinstatement by oestrogen in mice lacking the aromatase gene (Cyp19). J Endocrinol 2001; 168: 217-220.
59. Trainor BC, Greiwe KM, Nelson RJ. Individual differences in estrogen receptor alpha in select brain nuclei are associated with individual differences in aggression. Horm Behav 2006; 50: 338-345.
60. Simon NG. 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. New York, NY: Academic Press, 2002: 339-392.
61. Pradhan DS, Newman AE, Wacker DW, Wingfield JC, Schlinger BA, Soma KK. Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm Behav 2010; 57: 381-389.
62. Soma KK, Tramontin AD, Featherstone J, Brenowitz EA. Estrogen contributes to seasonal plasticity of the adult avian song control system. J Neurobiol 2004; 58: 413-422.
63. Tramontin AD, Wingfield JC, Brenowitz EA. Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J Neurobiol 2003; 57: 130-140.
64. Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ. Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 2007; 27: 12045-12057.
65. Remage-Healey L, Coleman MJ, Oyama RK, Schlinger BA. Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc Natl Acad Sci USA 2010; 107: 3852-3857.
66. Marler P, Peters S, Ball GF, Dufty AM, Wingfield JC. The role of sex steroids in the acquisition and production of birdsong. Nature 1988; 336: 770-772.
67. Adkins-Regan E, Abdelnabi M, Mobarak M, Ottinger MA. Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen Comp Endocrinol 1990; 78: 93-109.
68. Schlinger BA, Arnold AP. Circulating estrogens in a male songbird riginate in the brain. Proc Natl Acad Sci USA 1992; 89: 7650-7653.
69. Goodson JL, Evans AK, Lindberg L, Allen CD. Neuro-evolutionary patterning of sociality. Proc R Soc Lond B Biol Sci 2005; 272: 227-235.
70. Delville Y, De Vries GJ, Ferris CF. Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav Evol 2000; 55: 53-76.
71. Kruk MR, Van der Poel AM, Meelis W, Hermans J, Mostert PG, Mos J, Lohman AH. Discriminant analysis of the localization of aggression-inducing electrode placements in the hypothalamus of male rats. Brain Res 1983; 260: 61-79.
72. Kruk MR. Ethology and pharmacology of hypothalamic aggression in the rat. Neurosci Biobehav Rev 1991; 15: 527-538.
73. Siegel A, Roeling TAP, Gregg TR, Kruk MR. Neuropharmacology of brain-stimulation-evoked aggression. Neurosci Biobehav Rev 1999; 23: 359-389.
74. Goodson JL, Bass AH. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Brain Res Rev 2001; 35: 246-265.
75. Simerly RB. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 2002; 25: 507-536.
76. Jeffery KJ. Self-localization and the entorhinal-hippocampal system. Curr Opin Neurobiol 2007; 17: 684-691.
77. Bingman VP, Able KP. Maps in birds: representational mechanisms and neural bases. Curr Opin Neurobiol 2002; 12: 745-750.
78. Moser EI, Moser MB. A metric for space. Hippocampus 2008; 18: 1142-1156.
79. Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM. Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 2005; 29: 83-97.
80. Kogan JH, Frankland PW, Silva AJ. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 2000; 10: 47-56.
81. Shugrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor alpha and beta mRNA in the rat central nervous system. J Comp Neurol 1997; 388: 507-525.
82. Ball GF, Bernard DJ, Foidart A, Lakaye B, Balthazart J. Steroid sensitive sites in the avian brain: does the distribution of the estrogen receptor alpha and beta types provide insight into their function? Brain Behav Evol 1999; 54: 28-40.
83. Hodgson ZG, Meddle SL, Christians JK, Sperry TS, Healy SD. Influence of sex steroid hormones on spatial memory in a songbird. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2008; 194: 963-969.
84. Fuxjager MJ, Mast G, Becker EA, Marler CA. The 'home advantage' is necessary for a full winner effect and changes in post-encounter testosterone. Horm Behav 2009; 56: 214-219.
85. Trainor BC, Bird IM, Marler CA. Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm Behav 2004; 45: 115-121.
86. Dalla C, Antoniou K, Kokras N, Drossopoulou G, Papathanasiou G, Bekris S, Daskas S, Papadopoulou-Daifoti Z. Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol Behav 2008; 93: 595-605.
87. Karstaedt PJ, Kerasidis H, Pincus JH, Meloni R, Graham J, Gale K. Unilateral destruction of dopamine pathways increases ipsilateral striatal serotonin turnover in rats. Exp Neurol 1994; 126: 25-30.
88. Cransac H, Cottet-Emard JM, Pequignot JM, Peyrin L. Monoamines (norepinephrine, dopamine, serotonin) in the rat medial vestibular nucleus: endogenous levels and turnover. J Neural Transm 1996; 103: 391-401.
89. Song WC, Melner MH. Steroid transformation enzymes as critical regulators of steroid action in vivo. Endocrinology 2000; 141: 1587-1589.