Mechanistic basis and functional roles of long-term plasticity in auditory neurons induced by a brain-generated estrogen

Journal of Neuroscience

Volumn 32, Issue 46, 2012, Pages 16478-16495

  Tremere, Liisa A ^a   Kovaleski, Ryan F ^a   Burrows, Kaiping ^b   Jeong, Jin Kwon ^c   Pinaud, Raphael ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; ESTROGEN; ESTROGEN RECEPTOR BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; PROTEIN C FOS; PROTEIN ZENK; UNCLASSIFIED DRUG;

ACOUSTIC NERVE FIBER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY DISCRIMINATION; AUDITORY STIMULATION; CONTROLLED STUDY; EVOKED AUDITORY RESPONSE; FEMALE; IMMUNOPRECIPITATION; MALE; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPIKE; TAENIOPYGIA GUTTATA; WAKEFULNESS; WESTERN BLOTTING;

ACOUSTIC STIMULATION; ALGORITHMS; ANIMALS; AUDITORY CORTEX; BRAIN CHEMISTRY; DATA INTERPRETATION, STATISTICAL; ELECTRODES, IMPLANTED; ELECTROPHYSIOLOGICAL PHENOMENA; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; FINCHES; HEARING; MALE; MAP KINASE KINASE KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONAL PLASTICITY; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION;

EID: 84869058976     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3233-12.2012     Document Type: Article

References (59)

1. Balthazart J, Ball GF (2006) Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29:241-249. rossRef Medline
2. Balthazart J, Baillien M, Charlier TD, Ball GF (2003) Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 17:1591-1606. CrossRef Medline
3. Beato M, Herrlich P, Schutz G (1995) Steroid hormone receptors: many actors in search of a plot. Cell 83:851-857. CrossRef Medline
4. Bernard DJ, Bentley GE, Balthazart J, Turek FW, Ball GF (1999) Androgenreceptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology 140:4633-4643. CrossRef Medline
5. Besnard A, Galan-Rodriguez B, Vanhoutte P, Caboche J (2011) Elk-1 a transcription factor with multiple facets in the brain. Front Neurosci 5:35. Medline
6. Bishop CM (2006) Pattern recognition and machine learning. New York: Springer.
7. Bolhuis JJ, Gahr M (2006) Neural mechanisms of birdsong memory. Nat Rev Neurosci 7:347-357. CrossRef Medline
8. Cheng HY, Clayton DF (2004) Activation and habituation of extracellula signal-regulated kinase phosphorylation in zebra finch auditory forebrai n during song presentation. J Neurosci 24:7503-7513. CrossRef Medline
9. Clayton DF (2000) The genomic action potential. Neurobiol Learn Mem 74:185-216. CrossRef Medline
10. Cornil CA, Ball GF, Balthazart J (2006) Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 1126:2-26. CrossRef Medline
11. Ferrer I, Blanco R, Carmona M, Puig B, Domínguez I, Vinals F (2002) Active, phosphorylation-dependent MAP kinases, MAPK/ERK, SAPK/JNK and p38, and specific transcription factor substrates are differentially express ed following systemic administration of kainic acid to the adult rat. Acta Neuropathol 103:391-407. CrossRef Medline
12. Fields RD, Eshete F, Stevens B, Itoh K (1997) Action potential-dependent regulation of gene expression: temporal specificity in ca2β, cAMPresponsive element binding proteins, and mitogen-activated protein kinase signaling. J Neurosci 17:7252-7266. Medline
13. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, Berger TW (1999) 17betaestradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81:925-929. Medline
14. Gahr M (1996) Developmental changes in the distribution of oestrogen receptor mRNA expressing cells in the forebrain of female, male and masculinizedfemale zebra finches. Neuroreport 7:2469-2473. CrossRef Medline
15. Gahr M, Gutinger HR, Kroodsma DE (1993) Estrogen receptors in the avian brain: survey reveals general distribution and forebrain areas unique to songbirds. J Comp Neurol 327:112-122. CrossRef Medline
16. Heimovics SA, Prior NH, Maddison CJ, Soma KK (2012) Rapid and widespread effects of 17beta-estradiol on intracellular signaling in the male songbird brain: a seasonal comparison. Endocrinology 153:1364-1376.CrossRef Medline
17. Hu JY, Chen Y, Schacher S (2007) Protein kinase C regulates local synthesis and secretion of a neuropeptide required for activity-dependent longterm synaptic plasticity. J Neurosci 27:8927-8939. CrossRef Medline
18. Jacobs EC, Arnold AP, Campagnoni AT (1996) Zebra finch estrogen receptor cDNA: cloning and mRNA expression. J Steroid Biochem Mol Biol 59:135-145. CrossRef Medline
19. Jacobs EC, Arnold AP, Campagnoni AT (1999) Developmental regulation of the distribution of aromatase- and estrogen-receptor- mRNAexpressingcells in the zebra finch brain. Dev Neurosci 21:453-472.CrossRef Medline
20. Jeong JK, Burrows K, Tremere LA, Pinaud R (2011) Neurochemical organizationand experience-dependent activation of estrogen-associated circuits in the songbird auditory forebrain. Eur J Neurosci 34:283-291.CrossRef Medline
21. Kroodsma DE, Miller EH (1982) Acoustic communication in birds. New York: Academic.
22. London SE, Clayton DF (2008) Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11:579-586. CrossRef Medline
23. Maney DL, Pinaud R (2011) Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front Neuroendocrinol 32:287-302. CrossRef Medline
24. McCarthy MM (2008) Estradiol and the developing brain. Physiol Rev 88: 91-124. CrossRef Medline
25. McCarthy MM, Schwarz JM, Wright CL, Dean SL (2008) Mechanisms mediating oestradiol modulation of the developing brain. J Neuroendocrinol 20:777-783. CrossRef Medline
26. Meitzen J, Mermelstein PG (2011) Estrogen receptors stimulate brain region specific metabotropic glutamate receptors to rapidly initiate signal transduction pathways. J Chem Neuroanat 42:236-241. CrossRef Medline
27. Mello CV, Velho TA, Pinaud R (2004) Song-induced gene expression: a window on song auditory processing and perception. Ann N Y Acad Sci 1016:263-281. CrossRef Medline
28. Metzdorf R, Gahr M, Fusani L (1999) Distribution of aromatase, estrogen receptor, and androgen receptormRNAin the forebrain of songbirds and nonsongbirds. J Comp Neurol 407:115-129. CrossRef Medline
29. Orban PC, Chapman PF, Brambilla R (1999) Is the Ras-MAPK signaling pathway necessary for long-term memory formation? Trends Neurosci 22:38-44. CrossRef Medline
30. Perlman WR, Arnold AP (2003) Expression of estrogen receptor and aromatase mRNAs in embryonic and posthatch zebra finch brain. J Neurobiol 55:204-219. CrossRef Medline
31. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ (2005) Aromatase is presynaptic and sexually dimorphic in the adult zebra finch brain. Proc Biol Sci 272:2089-2096. CrossRef Medline
32. Peyssonnaux C, Eychene A (2001) The Raf/MEK/ERK pathway: new concepts of activation. Biol Cell 93:53-62. CrossRef Medline
33. Pinaud R (2005) Critical calcium-regulated biochemical and gene expression programs involved in experience-dependent plasticity. In: Plasticityin the visual system: from genes to circuits (Pinaud R, Tremere LA, De Weerd P, eds), pp 153-180. New York: Springer.
34. Pinaud R, Tremere LA (2012) Control of central auditory processing by a brain-generated oestrogen. Nat Rev Neurosci 13:521-527. CrossRef Medline
35. Pinaud R, Osorio C, Alzate O, Jarvis ED (2008a) Profiling of experienceregulated proteins in the songbird auditory forebrain using quantitative proteomics. Eur J Neurosci 27:1409-1422. CrossRef Medline
36. Pinaud R, Terleph TA, Tremere LA, Phan ML, Dagostin AA, Leao RM, Mello CV, Vicario DS (2008b) Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain. J Neurophysiol 100:441-455. CrossRef Medline
37. Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327-1334. CrossRef Medline
38. Remage-Healey L, Coleman MJ, Oyama RK, Schlinger BA (2010) Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc Natl Acad SciU S A107:3852-3857. CrossRef Medline
39. Remage-Healey L, Dong SM, Chao A, Schlinger BA (2012) Sex-specific, rapid neuroestrogen fluctuations and neurophysiological actions in the songbird auditory forebrain. J Neurophysiol 107:1621-1631. CrossRef Medline
40. Rohmann KN, Schlinger BA, Saldanha CJ (2007) Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. Dev Neurobiol 67:1-9. CrossRef Medline
41. Rosvall KA, Bergeon Burns CM, Barske J, Goodson JL, Schlinger BA, Sengelaub DR, Ketterson ED (2012) Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution. Proc Biol Sci 279:3547-3555. CrossRef Medline
42. Saldanha CJ, Coomaralingam L (2005) Overlap and co-expression of estrogen synthetic and responsive neurons in the songbird brain-a doublelabel immunocytochemical study. Gen Comp Endocrinol 141:66-75.CrossRef Medline
43. Saldanha CJ, Remage-Healey L, Schlinger BA (2011) Synaptocrine signaling: steroid synthesis and action at the synapse. Endocr Rev 32:532-549.CrossRef Medline
44. Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10. Medline
45. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183. CrossRef Medline
46. Tora L, White J, Brou C, Tasset D, Webster N, Scheer E, Chambon P (1989) The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell 59:477-487. CrossRef Medline
47. 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. CrossRef Medline
48. Tremere LA, Jeong JK, Pinaud R (2009) Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticityassociated gene expression. J Neurosci 29:5949-5963. CrossRef Medline
49. Tremere LA, Terleph TA, Jeong JK, Pinaud R (2010) Bilateral multielectrode neurophysiological recordings coupled to local pharmacology in awake songbirds. Nat Protoc 5:191-200. CrossRef Medline
50. Tremere LA, Burrows K, Jeong JK, Pinaud R (2011) Organization of estrogen-associated circuits in the mouse primary auditory cortex. J Exp Neurosci 5:45-60. Medline
51. Truss M, Beato M (1993) Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr Rev 14:459-479.CrossRef Medline
52. Vates GE, Broome BM, Mello CV, Nottebohm F (1996) Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366:613-642. CrossRef Medline
53. Velho TA, Mello CV (2008) Synapsins are late activity-induced genes regulated by birdsong. J Neurosci 28:11871-11882. CrossRef Medline
54. Velho TA, Pinaud R, Rodrigues PV, Mello CV (2005) Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22:1667-1678. CrossRef Medline
55. Vina J, Gambini J, Lopez-Grueso R, Abdelaziz KM, Jove M, Borras C (2011) Females live longer than males: role of oxidative stress. Curr Pharm Des 17:3959-3965. Medline
56. Wade J, Schlinger BA, Hodges L, Arnold AP (1994) Fadrozole: a potent and specific inhibitor of aromatase in the zebra finch brain. Gen Comp Endocrinol 94:53-61. CrossRef Medline
57. Woolley CS (2007) Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657-680. CrossRef Medline
58. Yague JG, Munoz A, de Monasterio-Schrader P, Defelipe J, Garcia-Segura LM, Azcoitia I (2006) Aromatase expression in the human temporal cortex. Neuroscience 138:389-401. CrossRef Medline
59. Yague JG, Wang AC, Janssen WG, Hof PR, Garcia-Segura LM, Azcoitia I, Morrison JH (2008) Aromatase distribution in the monkey temporal neocortex and hippocampus. Brain Res 1209:115-127. CrossRef Medline