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. 2006 Feb 17;27(4):287–296. doi: 10.1007/s11357-005-4555-9

Songbirds: A novel perspective on estrogens and the aging brain

Barney A Schlinger 1,3,✉, Colin J Saldanha 2
PMCID: PMC3455882  PMID: 23598662

Abstract

Songbirds perform some remarkable feats of memory, including forming memories for songs and for complex spatial features of their environments. Research into the neural and hormonal control of these behaviors reveals discrete circuits that can retain considerable plasticity in adulthood. The songbird brain is also a prominent site of estrogen synthesis and a target of estrogen action. Estrogens contribute to the plasticity of the adult songbird brain and contribute to the bird's capacity to form and retrieve some memories. We describe the brain, behavior and endocrinology of songbirds and discuss these findings within the context of the neurology of the aging brain.

Key words: aromatase, estradiol, hippocampus, learning and memory, neurosteroids, plasticity, song system, steroidogenesis, testosterone, 3β-HSD

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References

  1. Allolio B, Arlt W. DHEA treatment: myth or reality? Trends Endocrinol Metab. 2002;13:288–294. doi: 10.1016/s1043-2760(02)00617-3. [DOI] [PubMed] [Google Scholar]
  2. Altman J. Are new neurons formed in the brains of adult mammals? Science. 1962;135:1127–1128. doi: 10.1126/science.135.3509.1127. [DOI] [PubMed] [Google Scholar]
  3. Alvarez-Buylla A, Nottebohm F. Migration of young neurons in adult avian brain. Nature. 1988;335:353–354. doi: 10.1038/335353a0. [DOI] [PubMed] [Google Scholar]
  4. Alvarez-Buylla A, Theelen M, Nottebohm F. Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron. 1990;5:101–109. doi: 10.1016/0896-6273(90)90038-h. [DOI] [PubMed] [Google Scholar]
  5. Alvarez-Buylla A, Kirn JR, Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning [published erratum appears in Science 1990 Oct 19; 250(4979):360] Science. 1990;249:1444–1446. doi: 10.1126/science.1698312. [DOI] [PubMed] [Google Scholar]
  6. Balthazart J, Ball GF. New insights into the regulation and function of brain estrogen synthase (aromatase) Trends Neurosci. 1998;21:243–249. doi: 10.1016/S0166-2236(97)01221-6. [DOI] [PubMed] [Google Scholar]
  7. Balthazart J, Tlemcani O, Ball GF. Do sex differences in the brain explain sex differences in the hormonal induction of reproductive behavior? What 25 years of research on the Japanese Quail tells us. Horm Behav. 1996;30:627–661. doi: 10.1006/hbeh.1996.0066. [DOI] [PubMed] [Google Scholar]
  8. Barnea A, Nottebohm F. Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc Nat Acad Sci USA. 1996;93:714–718. doi: 10.1073/pnas.93.2.714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bednekoff PA, Balda RP, Kamil AC, Hile AG. Long-term spatial memory in four seed-caching corvid species. Anim Behav. 1997;53:335–341. doi: 10.1006/anbe.1996.0395. [DOI] [Google Scholar]
  10. Berthold P, Gwinner E, Sonnenschein E, editors. Avian Migration. Berlin, Heidelberg, New York: Springer; 2003. [Google Scholar]
  11. Bingman VP, Able KP. Maps in birds: representational mechanisms and neural bases. Curr Opin Neurobio. 2002;12:745–750. doi: 10.1016/s0959-4388(02)00375-6. [DOI] [PubMed] [Google Scholar]
  12. Bottjer SW, Johnson F. Circuits, hormones, and learning: vocal behavior in songbirds. J Neurobiol. 1997;33:602–618. doi: 10.1002/(SICI)1097-4695(19971105)33:5<602::AID-NEU8>3.0.CO;2-8. [DOI] [PubMed] [Google Scholar]
  13. Brainard MS, Doupe AJ. What songbirds teach us about learning. Nature. 2002;417:351–358. doi: 10.1038/417351a. [DOI] [PubMed] [Google Scholar]
  14. Brown SD, Johnson F, Bottjer SW. Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels. J. Neuroscience. 1993;13:2024–2032. doi: 10.1523/JNEUROSCI.13-05-02024.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Callard GV. Aromatization in brain and pituitary: an evolutionary prespective. In: Celotti F, Naftolin F, Martini L, editors. Metabolism of Hormonal Steroids in the Neuroendocrine Structures. NY: Raven; 1984. pp. 79–102. [Google Scholar]
  16. Callard GV, Drygas M, Gelinas D. Molecular and cellular physiology of aromatase in the brain and retina. J Steroid Biochem Mol Biol. 1993;44:541–547. doi: 10.1016/0960-0760(93)90257-W. [DOI] [PubMed] [Google Scholar]
  17. Canick JA, Vaccaro DE, Livingston EM, Leeman SE, Ryan KJ, Fox TO. Localization of aromatase and 5 alpha-reductase to neuronal and non-neuronal cells in the fetal rat hypothalamus. Brain Res. 1986;372:277–282. doi: 10.1016/0006-8993(86)91135-2. [DOI] [PubMed] [Google Scholar]
  18. Clayton N. Brain, perception, memory: Advances in cognitive neuroscience. Q J Exp Psychol B-Comp Physiol Psychol. 2002;55:191–192. [Google Scholar]
  19. Dittrich F, Feng Y, Metzdorf R, Gahr M. Estrogen-inducible, sex-specific expression of brain-derived neurotrophic factor mRNA in a forebrain song control nucleus of the juvenile zebra finch. Proc Natl Acad Sci USA. 1999;96:8241–8246. doi: 10.1073/pnas.96.14.8241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Erickson KI, Colcombe SJ, Raz N, Korol DL, Scalf P, Webb A, et al. Selective sparing of brain tissue in postmenopausal women receiving hormone replacement therapy. Neurobiol Aging. 2005;26:1205–1213. doi: 10.1016/j.neurobiolaging.2004.11.009. [DOI] [PubMed] [Google Scholar]
  21. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A, Norborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4:1313–1317. doi: 10.1038/3305. [DOI] [PubMed] [Google Scholar]
  22. Forlano PM, Deitcher DL, Myers DA, Bass AH. Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: Aromatase enzyme and mRNA expression identify glia as source. J Neurosci. 2001;21:8943–8955. doi: 10.1523/JNEUROSCI.21-22-08943.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gahr M (2004) Hormone-dependent neural plasticity in the juvenile and adult song system – What makes a successful male? In: Behavioral Neurobiology of Birdsong, pp 684–703 [DOI] [PubMed]
  24. Garcia-Segura LM, Wozniak A, Azcoitia I, Rodriguez JR, Hutchison RE, Hutchison JB. Aromatase expression by astrocytes after brain injury: Implications for local estrogen formation in brain repair. Neurosci. 1999;89:567–578. doi: 10.1016/S0306-4522(98)00340-6. [DOI] [PubMed] [Google Scholar]
  25. Garcia-Segura LM, Veiga S, Sierra A, Melcangi RC, Azcoitia I. Aromatase: A neuroprotective enzyme. Prog Neurobiol. 2003;71:31–41. doi: 10.1016/j.pneurobio.2003.09.005. [DOI] [PubMed] [Google Scholar]
  26. Gibson BM, Kamil AC. The fine-grained spatial abilities of three seed-caching corvids. Learn Behav. 2005;33:59–66. doi: 10.3758/bf03196050. [DOI] [PubMed] [Google Scholar]
  27. Goldman SA. Neuronal development and migration in explant cultures of the adult canary forebrain. J Neurosci. 1990;10:2931–2939. doi: 10.1523/JNEUROSCI.10-09-02931.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Goldman SA, Nottebohm F. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA. 1983;80:2390–2394. doi: 10.1073/pnas.80.8.2390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Goldman SA, Nedergaard M. Newly generated neurons of the adult songbird brain become functionally active in long-term culture. Dev Brain Res. 1992;68:217–223. doi: 10.1016/0165-3806(92)90063-3. [DOI] [PubMed] [Google Scholar]
  30. Goldman SA, Zaremba A, Niedzwiecki D. In vitro neurogenesis by neuronal precursor cells derived from the adult songbird brain. J Neurosci. 1992;12:2532–2541. doi: 10.1523/JNEUROSCI.12-07-02532.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Goodson J, Saldanha C, Hahn T and Soma K (2005) Recent advances in behavioral neuroendocrinology: Insights from studies on birds. Horm. Behav. 48: 461–473 [DOI] [PMC free article] [PubMed]
  32. Gould E, Gross CG. Neurogenesis in adult mammals: Some progress and problems. J Neurosci. 2002;22:619–623. doi: 10.1523/JNEUROSCI.22-03-00619.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Gould E, Woolley CS, Frankfurt M, McEwen BS. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci. 1990;10:1286–1291. doi: 10.1523/JNEUROSCI.10-04-01286.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hajszan T, Maclusky NJ, Leranth C. Dehydroepiandrosterone increases hippocampal spine synapse density in ovariectomized female rats. Endocrinol. 2004;145:1042–1045. doi: 10.1210/en.2003-1252. [DOI] [PubMed] [Google Scholar]
  35. Hampton RR, Shettleworth SJ. Hippocampal lesions impair memory for location but not color in passerine birds. Behav Neurosci. 1996;110:831–835. doi: 10.1037//0735-7044.110.4.831. [DOI] [PubMed] [Google Scholar]
  36. Healy SD, Suhonen J. Memory for locations of stored food in willow tits and marsh tits. Behav. 1996;133:71–80. [Google Scholar]
  37. Hidalgo A, Barami K, Iversen K, Goldman SA. Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol. 1995;27:470–487. doi: 10.1002/neu.480270404. [DOI] [PubMed] [Google Scholar]
  38. Hidalgo A, Barami K, Iversen K, Goldman SA. Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol. 1995;27:470–487. doi: 10.1002/neu.480270404. [DOI] [PubMed] [Google Scholar]
  39. Holloway CC, Clayton DE. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci. 2001;V4:170–175. doi: 10.1038/84001. [DOI] [PubMed] [Google Scholar]
  40. Hoshooley JS, Sherry DF. Neuron production, neuron number, and structure size are seasonally stable in the hippocampus of the food-storing black-capped chickadee (Poecile atricapillus) Behav Neurosci. 2004;118:345–355. doi: 10.1037/0735-7044.118.2.345. [DOI] [PubMed] [Google Scholar]
  41. Hung AJ, Stanbury MG, Shanabrough M, Horvath TL, Garcia-Segura LM, Naftolin F. Estrogen, synaptic plasticity and hypothalamic reproductive aging. Exp Gerontol. 2003;38:53–59. doi: 10.1016/S0531-5565(02)00183-3. [DOI] [PubMed] [Google Scholar]
  42. Iivonen S, Corder E, Lehtovirta M, Helisalmi S, Mannermaa A, Vepsalainen S, et al. Polymorphisms in the CYP19 gene confer increased risk for Alzheimer disease. Neurol. 2004;62:1170–1176. doi: 10.1212/01.wnl.0000118208.16939.60. [DOI] [PubMed] [Google Scholar]
  43. Kirn JR, Nottebohm F. Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci. 1993;13:1654–1663. doi: 10.1523/JNEUROSCI.13-04-01654.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kirn J, O'Loughlin B, Kasparian S, Nottebohm F. Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song [see comments] Proc Natl Acad Sci USA. 1994;91:7844–7848. doi: 10.1073/pnas.91.17.7844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kretz O, Fester L, Wehrenberg U, Zhou LP, Brauckmann S, Zhao ST, et al. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci. 2004;24:5913–5921. doi: 10.1523/JNEUROSCI.5186-03.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Lephart ED. A review of brain aromatase cytochrome P450. Brain Res Revs. 1996;22:1–26. [PubMed] [Google Scholar]
  47. London SE, Boulter J, Schlinger BA. Cloning of the zebra finch androgen synthetic enzyme CYP17: A study of its neural expression throughout posthatch development. J Comp Neurol. 2003;467(4):496–508. doi: 10.1002/cne.10936. [DOI] [PubMed] [Google Scholar]
  48. Lu SF, Mo QX, Hu S, Garippa C, Simon NG. Dehydroepiandrosterone upregulates neural androgen receptor level and transcriptional activity. J Neurobiol. 2003;57:163–171. doi: 10.1002/neu.10260. [DOI] [PubMed] [Google Scholar]
  49. Marler P. Three models of song learning: Evidence from behavior. J Neurobiol. 1997;33:501–516. doi: 10.1002/(SICI)1097-4695(19971105)33:5<501::AID-NEU2>3.0.CO;2-8. [DOI] [PubMed] [Google Scholar]
  50. Moller AQ, Pavlick B, Hile AG, Balda RP. Clark's nutcrackers Nucifraga columbiana remember the size of their cached seeds. Ethol. 2001;107:451–461. [Google Scholar]
  51. Naftolin F, Ryan KJ, Petro Z. Aromatization of androstenedione by limbic system tissue from human foetuses. J Endocrinol. 1971;51:795–796. doi: 10.1677/joe.0.0510795. [DOI] [PubMed] [Google Scholar]
  52. Nottebohm F. A brain for all seasons: Cyclical anatomical changes in song control nuclei of the canary brain. Science. 1981;214:1368–1370. doi: 10.1126/science.7313697. [DOI] [PubMed] [Google Scholar]
  53. Nottebohm F. The King Solomon Lectures in Neuroethology. A white canary on Mount Acropolis. J Comp Physiol A. 1996;179:149–156. doi: 10.1007/BF00222782. [DOI] [PubMed] [Google Scholar]
  54. Nottebohm F. Neuronal replacement in adult brain. Brain Res Bull. 2002;57:737–749. doi: 10.1016/S0361-9230(02)00750-5. [DOI] [PubMed] [Google Scholar]
  55. Nottebohm F (2004) The road we travelled – Discovery, choreography, and significance of brain replaceable neurons. In: Behavioral Neurobiology of Birdsong, pp 628–658 [DOI] [PubMed]
  56. Oberlander JG, Schlinger BA, Clayton NS, Saldanha CJ. Neural aromatization accelerates the acquisition of spatial memory via an influence on the songbird hippocampus. Horm Behav. 2004;45:250–258. doi: 10.1016/j.yhbeh.2003.12.003. [DOI] [PubMed] [Google Scholar]
  57. Pasmanik M, Callard GV. Aromatase and 5-Alpha-Reductase in the Teleost Brain, Spinal Cord, and Pituitary Gland. Gen Comp Endocrinol. 1985;60:244–251. doi: 10.1016/0016-6480(85)90320-X. [DOI] [PubMed] [Google Scholar]
  58. Paton JA, Nottebohm FN. Neurons generated in the adult brain are recruited into functional circuits. Science. 1984;225:1046–1048. doi: 10.1126/science.6474166. [DOI] [PubMed] [Google Scholar]
  59. Perrini S, Laviola L, Nataliccio A, Giorgino F. Associated hormonal declines in aging: DHEAS. J Endocrinol Invest. 2005;28:2885–2893. [PubMed] [Google Scholar]
  60. Peterson RS, Saldanha CJ, Schlinger BA. Rapid upregulation of aromatase mRNA and protein following neural injury in the zebra finch (Taeniopygia guttata) J Neuroendocrinol. 2001;13:317–323. doi: 10.1046/j.1365-2826.2001.00647.x. [DOI] [PubMed] [Google Scholar]
  61. Peterson RS, Lee DW, Fernando G, Schlinger BA. Radial glia express aromatase in the injured zebra finch brain. J Comp Neurol. 2004;480:261–269. doi: 10.1002/cne.20157. [DOI] [PubMed] [Google Scholar]
  62. Peterson RS, Yarram L, Schlinger BA and Saldanha CJ (2005) Aromatase is Presynaptic and Sexually Dimorphic in the Adult Zebra Finch Brain. Proc Roy Soc Lond B 272: 2089–2096 [DOI] [PMC free article] [PubMed]
  63. Prather J, Mooney R. Neural correlates of learned song in the avaian forebrain: Simultaneous representation of self and others. Curr Opin Neurobiol. 2004;14:496–502. doi: 10.1016/j.conb.2004.06.004. [DOI] [PubMed] [Google Scholar]
  64. Roselli CE, Resko JA. Cytochrome P450 aromatase (CYP19) in the non-human primate brain: distribution, regulation, and functional significance. J Steroid Biochem Mol Biol. 2001;79:247–253. doi: 10.1016/S0960-0760(01)00141-8. [DOI] [PubMed] [Google Scholar]
  65. Saldanha CJ, Popper P, Micevych PE, Schlinger BA. The passerine hippocampus is a site of high aromatase: Inter- and intraspecies comparisons. Horm Behav. 1998;34:85–97. doi: 10.1006/hbeh.1998.1447. [DOI] [PubMed] [Google Scholar]
  66. Saldanha CJ, Clayton NS, Schlinger BA. Androgen metabolism in the juvenile oscine forebrain: A cross-species analysis at neural sites implicated in memory function. J Neurobiol. 1999;40:397–406. doi: 10.1002/(SICI)1097-4695(19990905)40:3<397::AID-NEU11>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  67. Saldanha CJ, Tuerek MJ, Kim Y-H, 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. doi: 10.1002/1096-9861(20000807)423:4<619::AID-CNE7>3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  68. Saldanha C, Patel N, Randall J, Kullar R. Orthogonal patterns of neuroplasticity in the hippocampus and song circuit of a food storing songbird. Soc Neurosci Abstracts. 2004;554:18. [Google Scholar]
  69. Saldanha CJ, Schlinger BA, Micevych PE, Horvath TL. Presynaptic N-methyl-D-aspartate receptor expression is increased by estrogen in an aromatase-rich area of the songbird hippocampus. J Comp Neurol. 2004;469:522–534. doi: 10.1002/cne.11035. [DOI] [PubMed] [Google Scholar]
  70. Saldanha CJ, Rohmann KN, Coomaralingam L, Wynne RD. Estrogen provision by reactive glia decreases apoptosis in the zebra finch (Taeniopygia guttata) J Neurobiol. 2005;64:192–201. doi: 10.1002/neu.20147. [DOI] [PubMed] [Google Scholar]
  71. Schlinger BA. Estrogen synthesis and secretion by the songbird brain. In: Micevych PE, Hammer RP Jr, editors. Neurobiological Effects of Sex Steroid Hormones. Cambridge: Cambridge University Press; 1995. [Google Scholar]
  72. Schlinger BA. Sex steroids and their actions on the birdsong system. J Neurobiol. 1997;33:619–631. doi: 10.1002/(SICI)1097-4695(19971105)33:5<619::AID-NEU9>3.0.CO;2-7. [DOI] [PubMed] [Google Scholar]
  73. Schlinger BA, Brenowitz EA. Neural and hormonal control of birdsong. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, Brain and Behavior. Amsterdam: Academic; 2002. pp. 799–839. [Google Scholar]
  74. Schlinger BA, Amur-Umarjee S, Shen P, Campagnoni AT, Arnold AP. Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J Neurosci. 1994;14:7541–7552. doi: 10.1523/JNEUROSCI.14-12-07541.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Shen P, Schlinger BA, Campagnoni AT, Arnold AP. An atlas of aromatase mRNA expression in the zebra finch brain. J Comp Neurol. 1995;360:172–184. doi: 10.1002/cne.903600113. [DOI] [PubMed] [Google Scholar]
  76. Sherry DF, Duff SJ. Behavioural and neural bases of orientation in food-storing birds. J Exp Biol. 1996;199:165–171. doi: 10.1242/jeb.199.1.165. [DOI] [PubMed] [Google Scholar]
  77. Shettleworth SJ, Hampton RR, Westwood RP. Effects of season and photoperiod on food storing by black-capped chickadees, Parus atricapillus. Anim Behav. 1995;49:989–998. doi: 10.1006/anbe.1995.0128. [DOI] [Google Scholar]
  78. Smulders TV, Sasson AD, DeVoogd TJ. Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol. 1995;27:15–25. doi: 10.1002/neu.480270103. [DOI] [PubMed] [Google Scholar]
  79. Smulders TV, Shiflett MW, Sperling AJ, DeVoogd TJ. Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: The black-capped chickadee. J Neurobiol. 2000;44:414–422. doi: 10.1002/1097-4695(20000915)44:4<414::AID-NEU4>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar]
  80. Sohrabji F, Miranda RC, Toran-Allerand CD. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci. 1994;14:459–471. doi: 10.1523/JNEUROSCI.14-02-00459.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Soma KK, Wingfield JC. Dehydroepiandrosterone in songbird plasma: Seasonal regulation and relationship to territorial aggression. Gen Comp Endocrinol. 2001;123:144–155. doi: 10.1006/gcen.2001.7657. [DOI] [PubMed] [Google Scholar]
  82. 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 songbird. J Neurobiol. 1999;41:176–188. doi: 10.1002/(SICI)1097-4695(19991105)41:2<176::AID-NEU2>3.0.CO;2-2. [DOI] [PubMed] [Google Scholar]
  83. Soma KK, Wissman AM, Brenowitz EA, Wingfield JC. Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm Behav. 2002;41:203–212. doi: 10.1006/hbeh.2001.1750. [DOI] [PubMed] [Google Scholar]
  84. Soma KK, Schlinger BA, Wingfield JC, Saldanha CJ. Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: Relationship to aggressive and sexual behavior. J Neurobiol. 2003;56:209–221. doi: 10.1002/neu.10225. [DOI] [PubMed] [Google Scholar]
  85. Soma KK, Alday NA, Schlinger BA. DHEA metabolism by 3b-HSD in Adult Zebra Finch Brain: Sex Difference and Rapid Effect of Stress. Endocrinol. 2004;145:1668–1677. doi: 10.1210/en.2003-0883. [DOI] [PubMed] [Google Scholar]
  86. Tramontin AD, Brenowitz EA. Seasonal plasticity in the adult brain. Trends Neurosci. 2000;23:251–258. doi: 10.1016/S0166-2236(00)01558-7. [DOI] [PubMed] [Google Scholar]
  87. 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. doi: 10.1002/neu.10263. [DOI] [PubMed] [Google Scholar]
  88. Vanson A, Arnold AP, Schlinger BA. 3 beta-hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch telencephalon: Dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen Comp Endocrinol. 1996;102:342–350. doi: 10.1006/gcen.1996.0077. [DOI] [PubMed] [Google Scholar]
  89. Vockel A, Pröve 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. doi: 10.1016/0006-8993(90)90174-A. [DOI] [PubMed] [Google Scholar]
  90. Wang N, Aviram R, Kirn JR. Deafening alters neuron turnover within the telencephalic motor pathway for song control in adult zebra finches. J Neurosci. 1999;19:10554–10561. doi: 10.1523/JNEUROSCI.19-23-10554.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Wang NG, Hurley P, Pytte C, Kirn JR. Vocal control neuron incorporation decreases with age in the adult zebra finch. J Neurosci. 2002;22:10864–10870. doi: 10.1523/JNEUROSCI.22-24-10864.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. White SA, Livingston FS, Mooney R. Androgens modulate NMDA receptor-mediated EPSCs in the zebra finch song system. J Neurophysiol. 1999;82:2221–2234. doi: 10.1152/jn.1999.82.5.2221. [DOI] [PubMed] [Google Scholar]
  93. Wise PM. Estrogens and neuroprotection. Trends Endocrinol Metabol. 2002;13:229–230. doi: 10.1016/s1043-2760(02)00611-2. [DOI] [PubMed] [Google Scholar]
  94. Wise PM, Dubal DB. Estradiol protects against ischemic brain injury in middle-aged rats. Biol Reprod. 2000;63:982–985. doi: 10.1095/biolreprod63.4.982. [DOI] [PubMed] [Google Scholar]
  95. Wynne RD, Saldanha CJ. Glial aromatization decreases neural injury in the zebra finch (Taeniopygia guttata): Influence on apoptosis. J Neuroendocrinol. 2004;16:676–683. doi: 10.1111/j.1365-2826.2004.01217.x. [DOI] [PubMed] [Google Scholar]
  96. Wynne RD, Coomaralingam L, Rohmann KN, Saldanha CJ. Locally synthesized estradiol via glial aromatization decreases neural injury in the zebra finch. Horm Behav. 2004;46:124. [Google Scholar]
  97. Zwain IH, Yen SSC, Cheng CY. Astrocytes cultured in vitro produce estradiol-17 beta and express aromatase cytochrome P-450 (P-450 AROM) mRNA. Biochimica Et Biophysica Acta – General Subjects. 1997;1334:338–348. doi: 10.1016/s0304-4165(96)00115-8. [DOI] [PubMed] [Google Scholar]

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