Synaptocrine signaling: Steroid synthesis and action at the synapse

Endocrine Reviews

Volumn 32, Issue 4, 2011, Pages 532-549

  Saldanha, Colin J ^a,d   Remage Healey, Luke ^b   Schlinger, Barney A ^c  

^a LEHIGH UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d AMERICAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; AROMATASE; CHOLESTEROL; CYTOCHROME P450; CYTOCHROME P450 17; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; SEX HORMONE;

AUTOCRINE EFFECT; ENZYME ACTIVITY; HORMONE ACTION; HORMONE RELEASE; HORMONE SENSITIVITY; HORMONE SYNTHESIS; HUMAN; IMMUNOCYTOCHEMISTRY; NEUROENDOCRINE SYSTEM; NEUROMODULATION; NEUROSECRETORY CELL; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEX DIFFERENCE; STEROID RELEASE; STEROIDOGENESIS; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOCRINE SIGNALING;

ANIMALS; AROMATASE; BIRDS; BRAIN; ESTROGENS; HUMANS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 80052377098     PISSN: 0163769X     EISSN: None     Source Type: Journal    
DOI: 10.1210/er.2011-0004     Document Type: Review

References (153)

1. Schlinger BA, Arnold AP 1992 Plasma sex steroids and tissue aromatization in hatchling zebra finches: implications for the sexual differentiation of singing behavior. Endocrinology 130:289-299.
2. Schlinger BA, Callard GV 1989 Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49:434-441.
3. Schlinger BA, Slotow RH, Arnold AP 1992 Plasma estrogens and brain aromatase in winter white-crowned sparrows. Ornis Scandinavica 23:292-297.
4. Arnold AP, Schlinger BA 1993 Sexual-differentiation of brain and behavior-the zebra finch is not just a flying rat. Brain Behav Evol 42:231-241.
5. Naftolin F, Horvath TL, Jakab RL, Leranth C, Harada N, Balthazart J 1996 Aromatase immunoreactivity in axon terminals of the vertebrate brain. An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology 63:149-155.
6. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S, Harada N, Kimoto T, Kawato S 2004 Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017α and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 101:865-870.
7. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ 2005 Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc Biol Sci 272:2089-2096.
8. Rohmann KN, Schlinger BA, Saldanha CJ 2007 The subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. Dev Neurobiol 67: 1-9.
9. Balthazart J, Ball GF 2006 Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29:241-249.
10. Saldanha CJ, Peterson RS, Yarram L, Schlinger BA The synaptocrine hypothesis: a novel form of estrogen delivery. The Seventh Annual Meeting of the Society for Behavioral Neuroendocrinology, Cincinnati, OH, 2003, Abstract 95.
11. Saldanha CJ, Peterson RS, Yarram L, Schlinger BA The synaptocrine hypothesis: a novel form of estrogen delivery. Neuroscience Annual Meeting, New Orleans, LA, 2003, Abstract 610.14.
12. Mukai H, Takata N, Ishii HT, Tanabe N, Hojo Y, FurukawaA, Kimoto T, Kawato S 2006 Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neuroscience 138:757-764.
13. Murakami G, Tanabe N, Ishii HT, Ogiue-Ikeda M, Tsurugizawa T, Mukai H, Hojo Y, Takata N, Furukawa A, Kimoto T, Kawato S 2006 Role of cytochrome P450 in synaptocrinology: endogenous estrogen synthesis in the brain hippocampus. Drug Metab Rev 38:353-369.
14. Blaustein JD 1992 Cytoplasmic estrogen receptors in rat brain: immunocytochemical evidence using three antibodies with distinct epitopes. Endocrinology 131:1336-1342.
15. Blaustein JD, Lehman MN, Turcotte JC, Greene G 1992 Estrogen-receptors in dendrites and axon terminals in the guinea-pig hypothalamus. Endocrinology 131:281-290.
16. McEwen BS, Alves SE 1999 Estrogen actions in the central nervous system. Endocr Rev 20:279-307.
17. McEwen B, Akama K, Alves S, Brake WG, Bulloch K, Lee S, Li C, Yuen G, Milner TA 2001 Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA 98:7093-7100.
18. Beyer C, Pawlak J, Karolczak M 2003 Membrane receptors for oestrogen in the brain. J Neurochem 87:545-550.
19. Mitterling KL, Spencer JL, Dziedzic N, Shenoy S, McCarthy K, Waters EM, McEwen BS, Milner TA 2010 Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol 518:2729-2743.
20. Waters EM, Yildirim M, Janssen WG, Lou WY, McEwen BS, Morrison JH, Milner TA 2011 Estrogen and aging affect the synaptic distribution of estrogen receptor β-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res 1379:86-97.
21. Toran-Allerand CD 2004 Minireview: a plethora of estrogen receptors in the brain: where will it end?. Endocrinology 145:1069-1074.
22. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER 2005Atransmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307:1625-1630.
23. Funakoshi T, Yanai A, Shinoda K, Kawano MM, Mizukami Y 2006 G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 346:904-910.
24. McCarthy MM 2008 Estradiol and the developing brain. Physiol Rev 88:91-124.
25. Kelly MJ, Ronnekleiv OK 2002 Rapid membrane effects of estrogen in the central nervous system. In: Pfaff D, ed. Hormones, brain and behavior. Amsterdam: Academic Press; 361-380.
26. Woolley CS 2007 Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657-680.
27. Micevych PE, Mermelstein PG 2008 Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol 38:66-77.
28. Scharrer E 1954 Neurosecretion and anterior pituitary in the dog. Experientia 10:264-266.
29. MacLusky NJ, Naftolin F 1981 Sexual differentiation of the central nervous system. Science 211:1294-1302.
30. McEwen BS 1981 Neural gonadal steroid actions. Science 211:1303-1311.
31. SkinnerMK, Norton JN, Mullaney BP, RosselliM, Whaley PD, Anthony CT 1991 Cell-cell interactions and the regulation of testis function. Ann NY Acad Sci 637:354-363.
32. Bornstein SR, Vaudry H 1998 Paracrine and neuroendocrine regulation of the adrenal gland-basic and clinical aspects. Horm Metab Res 30:292-306.
33. Ballian N, Brunicardi FC, Wang XP 2006 Somatostatin and its receptors in the development of the endocrine pancreas. Pancreas 33:1-12.
34. Naftolin F, Ryan KJ, Petro Z 1971 Aromatization of androstenedione by limbic system tissue from human foetuses. J Endocrinol 51:795-796.
35. Naftolin F, Ryan KJ, Davies IJ, Reddy VV, Flores F, Petro Z, Kuhn M, White RJ, Takaoka Y, Wolin L 1975 The formation of estrogens by central neuroendocrine tissues. Rec Prog Horm Res 31:295-319.
36. Callard GV, Petro Z, Ryan KJ 1978 Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103: 2283-2290.
37. Canick JA, Vaccaro DE, Livingston EM, Leeman SE, Ryan KJ, Fox TO 1986 Localization of aromatase and 5α-reductase to neuronal and non-neuronal cells in the fetal rat hypothalamus. Brain Res 372:277-282.
38. Martini L 1982 The 5 α-reduction of testosterone in the neuroendocrine structures. Biochemical and biophysical implications. Endocr Rev 3:1-25.
39. Hutchison JB, Steimer T 1981 Brain 5-β-reductase-a correlate of behavioral sensitivity to androgen. Science 213: 244-246.
40. Baulieu EE, Robel P 1990 Neurosteroids: anewbrain function. J Steroid Biochem Mol Biol 37:395-403.
41. Compagnone NA, Bulfone A, Rubenstein JL, Mellon SH 1995 Steroidogenic enzyme P450c17 is expressed in the embryonic central nervous system. Endocrinology 136: 5212-5223.
42. Compagnone NA, Bulfone A, Rubenstein JL, Mellon SH 1995 Expression of the steroidogenic enzyme P450scc in the central and peripheral nervous systems during rodent embryogenesis. Endocrinology 136:2689-2696.
43. King SR, Manna PR, Ishii T, Syapin PJ, Ginsberg SD, Wilson K, Walsh LP, Parker KL, Stocco DM, Smith RG, Lamb DJ 2002 An essential component in steroid synthesis, the steroidogenic acute regulatory protein, is expressed in discrete regions of the brain. J Neurosci 22:10613-10620.
44. Callard GV 1984 Aromatization in brain and pituitary: an evolutionary perspective. In: Celotti F, Naftolin F, Martini L, ed. Metabolism of hormonal steroids in the neuroendocrine structures. New York: Raven Press; 79-102.
45. Santen RJ, Brodie H, Simpson ER, Siiteri PK, Brodie A 2009History of aromatase: saga of an important biological mediator and therapeutic target. Endocr Rev 30:343-375.
46. Balthazart J 1990 Brain aromatization of testosterone regulates male reproductive behavior in birds. Prog Clin Biol Res 342:92-98.
47. London SE, Remage-Healey L, Schlinger BA 2009 Neurosteroid production in the songbird brain: a re-evaluation of core principles. Front Neuroendocrinol 30:302-314.
48. Lephart ED 1996Areview of brain aromatase cytochrome P450. Brain Res Rev 22:1-26.
49. Simpson ER, Clyne C, Rubin G, Boon WC, Robertson K, Britt K, Speed C, Jones M 2002 Aromatase-a brief overview. Annu Rev Physiol 64:93-127.
50. Roselli CE, Resko JA 2001 Cytochrome P450 aromatase (CYP19) in the non-human primate brain: distribution, regulation, and functional significance. J Steroid Biochem Mol Biol 79:247-253.
51. Saldanha CJ, Tuerk MJ, Kim YH, Fernandes AO, Arnold AP, Schlinger BA 2000 Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J Comp Neurol 423:619-630.
52. Horvath TL, Roa-Pena L, Jakab RL, Simpson ER, Naftolin F 1997 Aromatase in axonal processes of early postnatal hypothalamic and limbic areas including the cingulate cortex. J Steroid Biochem Mol Biol 61:349-357.
53. Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, HondaS, Harada N, Shah NM 2009 Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139: 61-72.
54. Miller WL 1988 Molecular biology of steroid hormone synthesis. Endocr Rev 9:295-318.
55. Payne AH, Hales DB 2004 Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25:947-970.
56. Foidart A, Harada N, Balthazart J 1994 Effects of steroidal and nonsteroidal aromatase inhibitors on sexual behavior and aromatase-immunoreactive cells and fibers in the quail brain. Brain Res 657:105-123.
57. Mak P, Zenn R, Callard GV, Subcellular distribution and reaction kinetics of aromatase in goldfish brain. Program of the 67th Annual Meeting of The Endocrine Society, Baltimore, MD, 1985, p 265.
58. Forlano PM, Deitcher DL, Myers DA, Bass AH 2001 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 Neuroscience 21:8943-8955.
59. Diotel N, Le Page Y, Mouriec K, Tong SK, Pellegrini E, Vaillant C, Anglade I, Brion F, Pakdel F, Chung BC, Kah O 2010 Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front Neuroendocrinol 31:172-192.
60. Carlisle HJ, Hales TG, Schlinger BA 1998 Characterization of neuronal zebra finch GABA(A) receptors: steroid effects. J Comp Physiol A 182:531-538.
61. Saldanha CJ, Schlinger BA 2008 Steroidogenesis and neuroplasticity in the songbird brain. In: RitsnerMS, Weizman A, eds. Neuroactive steroids in brain function, behavioral and neuropsychiatric disorders: novel strategies for research and treatment. Pondicherry: Springer; 201-216.
62. Bolhuis JJ, Gahr M 2006 Neural mechanisms of birdsong memory. Nat Rev Neurosci 7:347-357.
63. Mooney R 2009 Neural mechanisms for learned birdsong. Learn Mem 16:655-669.
64. Simerly RB 1993 Distribution and regulation of steroid hormone receptor gene expression in the central nervous system. In: Seil FJ, ed. Advances in neurology. New York: Raven Press; 207-226.
65. Schlinger BA, Arnold AP 1991 Brain is the major site of estrogen synthesis in a male songbird. Proc Natl Acad Sci USA 88:4191-4194.
66. Vockel A, Pröve E, Balthazart J 1990 Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Res 511:291-302.
67. Vockel A, Pröve E, Balthazart J 1990 Effects of castration and testosterone treatment on the activity of testosteronemetabolizing enzymes in the brain of male and female zebra finches. J Neurobiol 21:808-825.
68. Shen P, Campagnoni CW, Kampf K, Schlinger BA, Arnold AP, Campagnoni AT 1994 Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain. Mol Brain Res 24:227-237.
69. Shen P, Schlinger BA, Campagnoni AT, Arnold AP 1995 An atlas of aromatasemRNAexpression in the zebra finch brain. J Comp Neurol 360:172-184.
70. Soma KK, Bindra RK, Gee J, Wingfield JC, Schlinger BA 1999 Androgen metabolizing enzymes show region-specific changes across the breeding season in the brain of a wild breeding song bird. J Neurobiol 41:176-188.
71. Soma KK, Schlinger BA, Wingfield JC, Saldanha CJ 2003 Brain aromatase, 5α-reductase, and 5β-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J Neurobiol 56:209-221.
72. Silverin B, Baillien M, Foidart A, Balthazart J 2000 Distribution of aromatase activity in the brain and peripheral tissues of passerine and nonpasserine avian species. Gen Comp Endocrinol 117:34-53.
73. Riters LV, Baillien M, Eens M, Pinxten R, Foidart A, Ball GF, Balthazart J 2001 Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J Neuroendocrinol 13:985-997.
74. Schlinger BA 1997 Sex steroids and their actions on the birdsong system. J Neurobio 33:619-631.
75. Saldanha CJ, Coomaralingam L 2005 Overlap and co-expression of estrogen synthetic and responsive neurons in the songbird brain-a double-label immunocytochemical study. Gen Comp Endocrinol 141:66-75.
76. Saldanha CJ, Schlinger BA 1997 Estrogen synthesis and secretion in the brown-headed cowbird (Molothrus ater). Gen Comp Endocrinol 105:390-401.
77. Schlinger BA, Arnold AP 1992 Circulating estrogens in a male songbird originate in the brain. Proc Nat Acad Sci USA 89:7650-7653.
78. Fusani L, Hutchison JB, Gahr M 2001 Testosterone regulates the activity and expression of aromatase in the canary neostriatum. J Neurobiol 49:1-8.
79. Balthazart J, Absil P, Foidart A, Houbart M, Harada N, Ball GF 1996 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 31:129-148.
80. Saldanha CJ, Popper P, Micevych PE, Schlinger BA 1998 The passerine hippocampus is a site of high aromatase: inter- and intraspecies comparisons. Horm Behav 34: 85-97.
81. Saldanha CJ, Schlinger BA, Micevych PE, Horvath TL 2004 Presynaptic N-methyl-D-aspartate receptor expression is increased by estrogen in an aromatase-rich area of the songbird hippocampus. J Comp Neurol 469:522-534.
82. Székely AD, Krebs JR 1996 Efferent connectivity of the hippocampal formation of the zebra finch (Taenopygia guttata): an anterograde pathway tracing study using Phaseolus vulgaris leucoagglutinin. J Comp Neurol 368: 198-214.
83. Roselli CE 1991 Synergistic induction of aromatase-activity in the rat-brain by estradiol and 5-α-dihydrotestosterone. Neuroendocrinology 53:79-84.
84. Pasmanik M, Schlinger BA, Callard GV 1988 In vivo steroid regulation of aromatase and 5-reductase in goldfish brain and pituitary. Gen Comp Endocrinol 71:175-182.
85. Fusani L, Van't Hof T, Hutchison JB 2003 Season-related changes in circulating androgen, brain aromatase, and perch-calling in male ring doves. Gen Comp Endocrinol 130:142-147.
86. Balthazart J, Baillien M, Cornil CA, Ball GF 2004 Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav 83:247-270.
87. Portillo W, Castillo CG, Retana-Márquez S, Roselli CE, Paredes RG 2007 Neuronal activity of aromatase enzyme in non-copulating male rats. J Neuroendocrinol 19:139-141.
88. Schlinger BA, Callard GV 1989 Estrogen receptors in quail brain: a functional relationship to aromatase and aggressiveness. Biol Reprod 40:268-275.
89. Roselli CE, Cross E, Poonyagariyagorn HK, Stadelman HL 2003 Role of aromatization in anticipatory and consummatory aspects of sexual behavior in male rats. Horm Behav 44:146-151.
90. Ball GF, Balthazart J 2002 Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. In: Pfaff DW, ed. Hormones, brain and behavior. Amsterdam: Academic Press; 649-798.
91. Immelman K 1969 Song development in the zebra finch and other estrildid finches. In: Hinde R, ed. Bird vocalizations. Cambridge, UK: Cambridge University Press; 61-74.
92. Nottebohm F, Arnold AP 1976 Sexual dimorphism in vocal control areas of the songbird brain. Science 194:211-213.
93. Gurney ME, Konishi M 1980 Hormone-induced sexual differentiation of brain and behavior in zebra finches. Science 208:1380-1383.
94. Simpson HB, Vicario DS 1991 Early estrogen treatment of female zebra finches masculinizes the brain pathway for learned vocalizations. J Neurobiol 22:777-793.
95. Grisham W, Lee J, Park SH, Mankowski JL, Arnold AP 2008 A dose-response study of estradiol's effects on the developing zebra finch song system. Neurosci Lett 445: 158-161.
96. BottjerSW, Johnson F 1997 Circuits, hormones, and learning: vocal behavior in songbirds. J Neurobiol 33:602-618.
97. Tramontin AD, Wingfield JC, Brenowitz EA 2003 Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J Neurobiol 57:130-140.
98. Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ 2007 Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27:12045-12057.
99. Adkins-Regan E, Abdelnabi M, Mobarak M, OttingerMA 1990 Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen Comp Endocrinol 78:93-109.
100. Hutchison JB, Wingfield JC, Hutchison RE 1984 Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. J Endocrinol 103:363-369.
101. Wade J, Schlinger BA, Arnold AP 1995 Aromatase and 5-reductase activity in cultures of developing zebra finch brain: an investigation of sex and regional differences. J Neurobiol 27:240-251.
102. Schlinger BA 2005 Behavioral neuroendocrinology evolving: contributions of comparative and field studies. Horm Behav 48:349-351.
103. Hart SA, Snyder MA, Smejkalova T, Woolley CS 2007 Estrogen mobilizes a subset of estrogen receptor-α-immunoreactive vesicles in inhibitory presynaptic boutons in hippocampal CA1. J Neurosci 27:2102-2111.
104. Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Dejace C, Ball GF, Balthazart J 2005 Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 146:3809-3820.
105. Cornil CA, Charlier TD 2010 Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase. J Neuroendocrinol 22:664-673.
106. Black MP, Balthazart J, Baillien M, Grober MS 2005 Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli. Proc Biol Sci 272:2435-2440.
107. Remage-Healey L, Oyama RK, Schlinger BA 2009 Elevated aromatase activity in forebrain synaptic terminals during song. J Neuroendocrinol 21:191-199.
108. Mermelstein PG, Becker JB, Surmeier DJ 1996 Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J Neurosci 16:595-604.
109. Balthazart J, Baillien M, Ball GF 2001 Rapid and reversible inhibition of brain aromatase activity. J Neuroendocrinol 13:63-73.
110. Balthazart J, Baillien M, Charlier TD, Ball GF 2003 Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 17:1591-1606.
111. Balthazart J, BaillienM, Charlier TD, Ball GF 2005 Effects of calmodulin on aromatase activity in the preoptic area. J Neuroendocrinol 17:664-671.
112. Remage-Healey L, Maidment NT, Schlinger BA 2008 Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327-1334.
113. Hull EM, Du J, Lorrain DS, Matuszewich L 1995 Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci 15:7465-7471.
114. Curtis JT, Stowe JR, Wang Z 2003 Differential effects of intraspecific interactions on the striatal dopamine system in social and non-social voles. Neuroscience 118:1165-1173.
115. Saleh TM, Connell BJ, Legge C, Cribb AE 2005 Estrogen synthesis in the central nucleus of the amygdala following middle cerebral artery occlusion: role in modulating neurotransmission. Neuroscience 135:1141-1153.
116. Balthazart J, Baillien M, Ball GF 2006 Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147:359-366.
117. Hojo Y, Murakami G, Mukai H, Higo S, Hatanaka Y, Ogiue-Ikeda M, Ishii H, Kimoto T, Kawato S 2008 Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol Cell Endocrinol 290:31-43.
118. London SE, Monks DA, Wade J, Schlinger BA 2006 Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147:5975-5987.
119. London SE, Boulter J, Schlinger BA 2003 Cloning of the zebra finch androgen synthetic enzyme CYP17: a study of its neural expression throughout posthatch development. J Comp Neurol 467:496-508.
120. London SE, Clayton DF 2010 Genomic and neural analysis of the estradiol-synthetic pathway in the zebra finch. BMC Neurosci 11:46.
121. Vanson A, Arnold AP, Schlinger BA 1996 3β-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 102: 342-350.
122. Tam H, Schlinger BA 2007 Activities of 3B-HSD and aromatase in slices of the adult and developing zebra finch brain. Gen Comp Endocrinol 150:26-33.
123. London SE, Itoh Y, Lance VA, Wise PM, Ekanayake PS, Oyama RK, Arnold AP, Schlinger BA 2010 Neural expression and post-transcriptional dosage compensation of the steroid metabolic enzyme 17β-HSD type 4.BMCNeurosci 11:47.
124. Soma KK, Wingfield JC 2001 Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen Comp Endocrinol 123:144-155.
125. 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.
126. Pradhan DS, Newman AE, Wacker DW, Wingfield JC, Schlinger BA, Soma KK 2010 Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm Behav 57:381-389.
127. Soma KK, Alday NA, Hau M, Schlinger BA 2004 Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145:1668-1677.
128. Evanson NK, Herman JP, Sakai RR, Krause EG 2010 Nongenomic actions of adrenal steroids in the central nervous system. J Neuroendocrinol 22:846-861.
129. Herbison AE 2009 Rapid actions of oestrogen on gonadotropin-releasing hormone neurons; from fantasy to physiology? J Physiol 587:5025-5030.
130. Remage-Healey L, Bass AH 2007 Plasticity in brain sexuality is revealed by the rapid actions of steroid hormones. J Neurosci 27:1114-1122.
131. Remage-Healey L, Bass AH 2006 A rapid neuromodulatory role for steroid hormones in the control of reproductive behavior. Brain Res 1126:27-35.
132. Grassi S, Frondaroli A, Dieni C, Scarduzio M, Pettorossi VE 2009 Long-term potentiation in the rat medial vestibular nuclei depends on locally synthesized 17β-estradiol. J Neurosci 29:10779-10783.
133. Sisneros JA, Forlano PM, Deitcher DL, Bass AH 2004 Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305:404-407.
134. Noirot IC, Adler HJ, Cornil CA, Harada N, Dooling RJ, Balthazart J, Ball GF 2009 Presence of aromatase and estrogen receptor α in the inner ear of zebra finches. Hear Res 252:49-55.
135. Sanford SE, Lange HS, Maney DL 2010 Topography of estradiol-modulated genomic responses in the songbird auditory forebrain. Dev Neurobiol 70:73-86.
136. Remage-Healey L, Coleman MJ, Oyama RK, SchlingerBA 2010 Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc Nat Acad Sci USA 107:3852-3857.
137. Krahe R, Gabbiani F 2004 Burst firing in sensory systems. Nat Rev Neurosci 5:13-23.
138. Tremere LA, Jeong JK, Pinaud R 2009 Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29:5949-5963.
139. Tremere LA, Pinaud R 2011 Brain-generated estradiol drives long-term optimization of auditory coding to enhance the discrimination of communication signals. J Neurosci 31:3271-3289.
140. Holveck M, Riebel K 2007 Preferred songs predict preferred males: consistency and repeatability of zebra finch females across three test contexts. Animal Behav 74:297-309.
141. Gobes SM, Bolhuis JJ 2007 Birdsong memory: A neural dissociation between song recognition and production. Curr Biol 17:789-793.
142. Schlinger BA, Amur-Umarjee S, Campagnoni AT, Arnold AP 1995 5β-Reductase and other androgen-metabolizing enzymes in primary cultures of developing zebra finch telencephalon. J Neuroendocrinol 7:187-192.
143. López-Muñoz F, Alamo C 2009 Monoaminergic neurotransmission: the history of the discovery of antidepressants from 1950s until today. Curr Pharm Des 15:1563-1586.
144. Do Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, Tsutsui K, Tonon MC, Pelletier G, Vaudry H 2009 Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol 30:259-301.
145. Jäntti SE, Tammimäki A, Raattamaa H, Piepponen P, Kostiainen R, Ketola RA 2010 Determination of steroids and their intact glucuronide conjugates in mouse brain by capillary liquid chromatography-tandem mass spectrometry. Anal Chem 82:3168-3175.
146. Caldwell JD, Suleman F, ChouSH, Shapiro RA, Herbert Z, Jirikowski GF 2006 Emerging roles of steroid-binding globulins. Horm Metab Res 38:206-218.
147. McLeod JF, Cooke NE 1989 The vitamin D-binding protein, α-fetoprotein, albumin multigene family: detection of transcripts in multiple tissues. J Biol Chem 264:21760-21769.
148. Srivastava DP, Woolfrey KM, Liu F, Brandon NJ, Penzes P 2010 Estrogen receptor B activity modulates synaptic signaling and structure. J Neurosci 30:13454-13460.
149. Tsutsui K, Matsunaga M, Miyabara H, Ukena K 2004 Identification and mode of action of a novel neurosteroid stimulating locomotor activity. Zool Sci 21:1201-1202.
150. Tsutsui K, Haraguchi S, Matsunaga M, Koyama T, Do Rego JL, Vaudry H 2010 Identification of 7α-hydroxypregnenolone, a novel bioactive amphibian neurosteroid stimulating locomotor activity, and its physiological roles in the regulation of locomotion. Gen Comp Endocrinol 168:275-279.
151. Majewska MD 1992 Neurosteroids: endogenous bimodal modulators of the GABAA receptor. Mechanism of action and physiological significance. Prog Neurobiol 38:379-395.
152. Tabori NE, Stewart LS, Znamensky V, Romeo RD, Alves SE, McEwen BS, Milner TA 2005 Ultrastructural evidence that androgen receptors are located at extranuclear sites in the rat hippocampal formation. Neuroscience 130:151-163.
153. Smejkalova T, Woolley CS 2010 Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism. J Neurosci 30:16137-16148.