Estrogenic modulation of auditory processing: A vertebrate comparison

Frontiers in Neuroendocrinology

Volumn 34, Issue 4, 2013, Pages 285-299

  Caras, Melissa L ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Auditory; Comparative; Estradiol; Estrogen; Hearing; Hormone; Seasonal; Sensory; Steroid

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; NORADRENALIN; TESTOSTERONE;

ANURA; AUDITORY THRESHOLD; DIRECTIONAL HEARING; DISTORTION PRODUCT OTOACOUSTIC EMISSION; ESTROGEN THERAPY; ESTRUS CYCLE; EVOKED BRAIN STEM AUDITORY RESPONSE; FISH; HEARING; HEARING IMPAIRMENT; HUMAN; MENOPAUSE; MENSTRUAL CYCLE; NERVE CELL PLASTICITY; NEUROMODULATION; NOISE INJURY; NONHUMAN; OTITIS MEDIA; OTOACOUSTIC EMISSION; PERCEPTION DEAFNESS; PRIORITY JOURNAL; REVIEW; SEASONAL VARIATION; SEX DIFFERENCE; SONGBIRD; SOUND DETECTION; TAENIOPYGIA GUTTATA; TINNITUS; TURNER SYNDROME; VOCALIZATION;

AUDITORY; COMPARATIVE; ESTRADIOL; ESTROGEN; HEARING; HORMONE; SEASONAL; SENSORY; STEROID;

ANIMALS; AUDITORY PATHWAYS; BRAIN; ESTROGENS; GONADAL STEROID HORMONES; HUMANS; SEXUAL BEHAVIOR; VERTEBRATES;

EID: 84884590518     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2013.07.006     Document Type: Review

References (194)

1. Al-Mana D., Ceranic B., Djahanbakhch O., Luxon L.M. Alteration in auditory function during the ovarian cycle. Hear. Res. 2010, 268:114-122.
2. Andreyko J.L., Jaffe R.B. Use of a gonadotropin-releasing hormone agonist analogue for treatment of cyclic auditory dysfunction. Obstet. Gynecol. 1989, 74:506-509.
3. Appeltants D., Del Negro C., Balthazart J. Noradrenergic control of auditory information processing in female canaries. Behav. Brain Res. 2002, 133:221-235.
4. Arch V.S., Narins P.M. Sexual hearing: the influence of sex hormones on acoustic communication in frogs. Hear. Res. 2009, 252:15-20.
5. Barclay S.R., Harding C.F. Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res. 1990, 523:251-262.
6. Bass A.H. Steroid-dependent plasticity of vocal motor systems: novel insights from teleost fish. Brain Res. Rev. 2008, 57:299-308.
7. Bell A. Circadian and menstrual rhythms in frequency variations of spontaneous otoacoustic emissions from human ears. Hear. Res. 1992, 58:91-100.
8. Berridge C.W., Waterhouse B.D. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 2003, 42:33-84.
9. Brackenbury J.H. Power capabilities of the avian sound-producing system. J. Exp. Biol. 1979, 78:163-166.
10. Brenowitz E.A. Plasticity of the adult avian song control system. Ann. N. Y. Acad. Sci. 2004, 1016:560-585.
11. Brenowitz E.A. Plasticity of the song control system in adult birds. Neuroscience of birdsong 2008, Cambridge University Press, New York, p. 332. P. Zeigler, P. Marler (Eds.).
12. Burns E.M., Arehart K.H., Campbell S.L. Prevalence of spontaneous otoacoustic emissions in neonates. J. Acoust. Soc. Am. 1992, 91:1571.
13. Caras M.L., Brenowitz E., Rubel E.W. Peripheral auditory processing changes seasonally in Gambel's white-crowned sparrow. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 2010, 196:581-599.
14. Caras M.L., O'Brien M., Brenowitz E.B., Rubel E.W. Estradiol selectively enhances auditory function in avian forebrain neurons. J. Neurosci. 2012, 32:17597-17611.
15. Cardin J.A., Schmidt M.F. Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J. Neurosci. 2004, 24:7745-7753.
16. Caruso S., Maiolino L., Rugolo S., Intelisano G., Farina M., Cocuzza S., Serra A. Auditory brainstem response in premenopausal women taking oral contraceptives. Hum. Reprod. 2003, 18:85-89.
17. Caruso S., Maiolino L., Agnello C., Garozzo A., Di Mari L., Serra A. Effects of patch or gel estrogen therapies on auditory brainstem response in surgically postmenopausal women: a prospective, randomized study. Fertil. Steril. 2003, 79:556-561.
18. Chakraborty M., Burmeister S.S. Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of túngara frogs. Horm. Behav. 2010, 58:619-627.
19. Chalifoux J.R., Carter A.G. GABAB receptor modulation of synaptic function. Curr. Opin. Neurobiol. 2011, 21:339-344.
20. Charitidi K., Canlon B. Estrogen receptors in the central auditory system of male and female mice. Neuroscience 2010, 165:923-933.
21. Charitidi K., Meltser I., Tahera Y., Canlon B. Functional responses of estrogen receptors in the male and female auditory system. Hear. Res. 2009, 252:71-78.
22. Charitidi K., Frisina R.D., Vasilyeva O.N., Zhu X., Canlon B. Expression patterns of estrogen receptors in the central auditory system change in prepubertal and aged mice. Neuroscience 2010, 170:1270-1281.
23. Charitidi K., Meltser I., Canlon B. Estradiol treatment and hormonal fluctuations during the estrous cycle modulate the expression of estrogen receptors in the auditory system and the prepulse inhibition of acoustic startle response. Endocrinology 2012, 10.1210/en.2012-1416.
24. Chow R.W., Handelsman D.J., Ng M.K. Minireview: rapid actions of sex steroids in the endothelium. Endocrinology 2010, 151:2411-2422.
25. Chung D.Y., Mason K., Gannon R.P., Willson G.N. The ear effect as a function of age and hearing loss. J. Acoust. Soc. Am. 1983, 73:1277.
26. Clint E.K., Sober E., Garland T., Rhodes J.S. Male superiority in spatial navigation: adaptation or side effect?. Q. Rev. Biol. 2012, 87:289-313.
27. Coffin A.B., Mohr R.A., Sisneros J.A. Saccular-specific hair cell addition correlates with reproductive state-dependent changes in the auditory saccular sensitivity of a vocal fish. J. Neurosci. 2012, 32:1366-1376.
28. Coleman J.R., Campbell D., Cooper W.A., Welsh M.G., Moyer J. Auditory brainstem responses after ovariectomy and estrogen replacement in rat. Hear. Res. 1994, 80:209-215.
29. Cooper W.A., Ross K.C., Coleman J.R. Estrogen treatment and age effects on auditory brainstem responses in the post-breeding Long-Evans rat. Audiology 1999, 38:7-12.
30. Cox J.R. Hormonal influence on auditory function. Ear Hear. 1980, 1:219-222.
31. Dave A.S., Yu A.C., Margoliash D. Behavioral state modulation of auditory activity in a vocal motor system. Science 1998, 282:2250-2254.
32. Dehan C.P., Jerger J. Analysis of gender differences in the auditory brainstem response. Laryngoscope 1990, 100:18-24.
33. Del Negro C., Edeline J.M. Sex and season influence the proportion of thin spike cells in the canary HVc. NeuroReport 2002, 13:2005-2009.
34. Del Negro C., Kreutzer M., Gahr M. Sexually stimulating signals of canary (Serinus canaria) songs: evidence for a female-specific auditory representation in the HVc nucleus during the breeding season. Behav. Neurosci. 2000, 114:526-542.
35. Del Negro C., Lehongre K., Edeline J.M. Selectivity of canary HVC neurons for the bird's own song: modulation by photoperiodic conditions. J. Neurosci. 2005, 25:4952-4963.
36. Ehret G., Koch M. Ultrasound-induced parental behaviour in house mice is controlled by female sex hormones and parental experience. Ethology 1989, 80:81-93.
37. Ehret G., Schmid C. Reproductive cycle-dependent plasticity of perception of acoustic meaning in mice. Physiol. Behav. 2009, 96:428-433.
38. Ehret G., Koch M., Haack B., Markl H. Sex and parental experience determine the onset of an instinctive behavior in mice. Naturwissenschaften 1987, 74:47.
39. Eldredge L., Salamy A. Functional auditory development in preterm and full term infants. Early Hum. Dev. 1996, 45:215-228.
40. Elkind-Hirsch K.E., Wallace E., Stach B.A., Jerger J.F. Cyclic steroid replacement alters auditory brainstem responses in young women with premature ovarian failure. Hear. Res. 1992, 64:93-98.
41. Elkind-Hirsch K.E., Stoner W.R., Stach B.A., Jerger J.F. Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hear. Res. 1992, 60:143-148.
42. Fichtel I., Ehret G. Perception and recognition discriminated in the mouse auditory cortex by c-Fos labeling. NeuroReport 1999, 10:2341-2345.
43. Forlano P.M., Deitcher D.L., Bass A.H. Distribution of estrogen receptor alpha mRNA in the brain and inner-ear of a vocal fish with comparisons to sites of aromatase expression. J. Comp. Neurol. 2005, 483:91-113.
44. Fukui I., Burger R.M., Ohmori H., Rubel E.W. GABAergic inhibition sharpens the frequency tuning and enhances phase locking in chicken nucleus magnocellularis neurons. J. Neurosci. 2010, 30:12075-12083.
45. Galindo-Leon E.E., Lin F.G., Liu R.C. Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations. Neuron 2009, 62:705-716.
46. Gall M.D., Salameh T.S., Lucas J.R. Songbird frequency selectivity and temporal resolution vary with sex and season. Proc. Biol. Sci. 2013, 280:20122296.
47. Gelinas D., Callard G.V. Immunolocalization of aromatase- and androgen receptor-positive neurons in the goldfish brain. Gen. Comp. Endocrinol. 1997, 106:155-168.
48. Goense J.B., Feng A.S. Seasonal changes in frequency tuning and temporal processing in single neurons in the frog auditory midbrain. J. Neurobiol. 2005, 65:22-36.
49. Goh A.Y., Hussain S.S. Sudden hearing loss and pregnancy: a review. J. Laryngol. Otol. 2012, 126:337-339.
50. Green S.H., Bailey E., Wang Q., Davis R.L. The Trk A, B, C's of neurotrophins in the cochlea. Anat Rec (Hoboken) 2012, 295:1877-1895.
51. Grothe B., Koch U. Dynamics of binaural processing in the mammalian sound localization pathway - the role of GABA(B) receptors. Hear. Res. 2011, 279:43-50.
52. Guimaraes P., Zhu X., Cannon T., Kim S., Frisina R.D. Sex differences in distortion product otoacoustic emissions as a function of age in CBA mice. Hear. Res. 2004, 192:83-89.
53. Güngör N., Böke B., Belgin E., Tunçbilek E. High frequency hearing loss in Ullrich-Turner syndrome. Eur. J. Pediatr. 2000, 159:740-744.
54. Gurr P., Owen G., Reid A., Canter R. Tinnitus in pregnancy. Clin. Otolaryngol. Allied Sci. 1993, 18:294-297.
55. Guski R. Acoustic tau: an easy analogue to visual tau?. Ecol. Psychol. 1992, 4:189-197.
56. Haggard M., Gaston J.B. Changes in auditory perception in the menstrual cycle. Br. J. Audiol. 1978, 12:105-118.
57. Hall J.W. New handbook of auditory evoked responses 2007, Allyn and Bacon, Boston, MA.
58. Hederstierna C., Hultcrantz M., Collins A., Rosenhall U. Hearing in women at menopause. Prevalence of hearing loss, audiometric configuration and relation to hormone replacement therapy. Acta Otolaryngol. 2007, 127:149-155.
59. Hederstierna C., Hultcrantz M., Rosenhall U. Estrogen and hearing from a clinical point of view; characteristics of auditory function in women with Turner syndrome. Hear. Res. 2009, 252:3-8.
60. Hederstierna C., Hultcrantz M., Rosenhall U. A longitudinal study of hearing decline in women with Turner syndrome. Acta Otolaryngol. 2009, 129:1434-1441.
61. Helena C.V., de Oliveira Poletini.M., Sanvitto G.L., Hayashi S., Franci C.R., Anselmo-Franci J.A. Changes in alpha-estradiol receptor and progesterone receptor expression in the locus coeruleus and preoptic area throughout the rat estrous cycle. J. Endocrinol. 2006, 188:155-165.
62. Henry K.S., Lucas J.R. Vocally correlated seasonal auditory variation in the house sparrow (Passer domesticus). J. Exp. Biol. 2009, 212:3817-3822.
63. Heritage A.S., Stumpf W.E., Sar M., Grant L.D. Brainstem catecholamine neurons are target sites for sex steroid hormones. Science 1980, 207:1377-1379.
64. Hillery M. Seasonality of two midbrain auditory responses in the treefrog, Hyla chrysoscelis. Copeia 1984, 4:844-852.
65. Huang G.Z., Woolley C.S. Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism. Neuron 2012, 74:801-808.
66. Hudgens E.D., Ji L., Carpenter C.D., Petersen S.L. The gad2 promoter is a transcriptional target of estrogen receptor (ER)alpha and ER beta: a unifying hypothesis to explain diverse effects of estradiol. J. Neurosci. 2009, 29:8790-8797.
67. Hultcrantz M. Ear and hearing problems in Turner's syndrome. Acta Otolaryngol. 2003, 123:253-257.
68. Hultcrantz M., Sylven L. Turner's syndrome and hearing disorders in women aged 16-34. Hear. Res. 1997, 103:69-74.
69. Hultcrantz M., Sylvén L., Borg E. Ear and hearing problems in 44 middle-aged women with Turner's syndrome. Hear. Res. 1994, 76:127-132.
70. Hurley L.M., Devilbiss D.M., Waterhouse B.D. A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr. Opin. Neurobiol. 2004, 14:488-495.
71. Jeong J.K., Burrows K., Tremere L.A., Pinaud R. Neurochemical organization and experience-dependent activation of estrogen-associated circuits in the songbird auditory forebrain. Eur. J. Neurosci. 2011, 34:283-291.
72. Jerger J., Hall J. Effects of age and sex on auditory brainstem response. Archives of Otolaryngology-Head & Neck Surgery 1980, 106:387.
73. Jerger J., Johnson K. Interactions of age, gender, and sensorineural hearing loss on ABR latency. Ear Hear. 1988, 9:168.
74. Jewett D.L., Williston J.S. Auditory-evoked far fields averaged from the scalp of humans. Brain 1971, 94:681-696.
75. Jewett D.L., Romano M.N., Williston J.S. Human auditory evoked potentials: possible brain stem components detected on the scalp. Science 1970, 167:1517-1518.
76. Jönsson R., Rosenhall U., Gause-Nilsson I., Steen B. Auditory function in 70- and 75-year-olds of four age cohorts. A cross-sectional and time-lag study of presbyacusis. Scand. Audiol. 1998, 27:81-93.
77. Kelly M.J., Rønnekleiv O.K. Control of CNS neuronal excitability by estrogens via membrane-initiated signaling. Mol. Cell. Endocrinol. 2009, 308:17-25.
78. Kemp D.T. Stimulated acoustic emissions from within the human auditory system. J. Acoust. Soc. Am. 1978, 64:1386-1391.
79. Kemp D.T. Otoacoustic emissions, their origin in cochlear function, and use. Br. Med. Bull. 2002, 63:223-241.
80. Kenny R., Patil N., Considine N. Sudden (reversible) sensorineural hearing loss in pregnancy. Ir. J. Med. Sci. 2011, 180:79-84.
81. Khaliq F., Tandon O.P., Goel N. Auditory evoked responses in postmenopausal women on hormone replacement therapy. Ind. J. Physiol. Pharmacol. 2003, 47:393-399.
82. Khaliq F., Tandon O.P., Goel N. Differential effects of exogenous estrogen versus a estrogen-progesterone combination on auditory evoked potentials in menopausal women. Ind. J. Physiol. Pharmacol. 2005, 49:345-352.
83. Kilicdag E.B., Yavuz H., Bagis T., Tarim E., Erkan A.N., Kazanci F. Effects of estrogen therapy on hearing in postmenopausal women. Am. J. Obstet. Gynecol. 2004, 190:77-82.
84. Kim S.H., Kang B.M., Chae H.D., Kim C.H. The association between serum estradiol level and hearing sensitivity in postmenopausal women. Obstet. Gynecol. 2002, 99:726-730.
85. Klug A., Bauer E.E., Hanson J.T., Hurley L., Meitzen J., Pollak G.D. Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J. Neurophysiol. 2002, 88:1941-1954.
86. Laws D.W., Moon C.E. Effects of the menstrual cycle on the human acoustic reflex threshold. J. Aud. Res. 1986, 26:197-206.
87. LeBeau F.E., Malmierca M.S., Rees A. Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J. Neurosci. 2001, 21:7303-7312.
88. LeBlanc M.M., Goode C.T., MacDougall-Shackleton E.A., Maney D.L. Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res. 2007, 1171:93-103.
89. Lewald J. Gender-specific hemispheric asymmetry in auditory space perception. Brain Res. Cogn. Brain Res. 2004, 19:92-99.
90. Liu R.C., Schreiner C.E. Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol. 2007, 5:e173.
91. Liu R.C., Linden J.F., Schreiner C.E. Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur. J. Neurosci. 2006, 23:3087-3097.
92. Lucas J.R., Freeberg T.M., Krishnan A., Long G.R. A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 2002, 188:981-992.
93. Lucas J.R., Freeberg T.M., Long G.R., Krishnan A. Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 2007, 193:201-215.
94. Lynch K.S., Wilczynski W. Social regulation of plasma estradiol concentration in a female anuran. Horm. Behav. 2006, 50:101-106.
95. Lynch K.S., Diekamp B., Ball G.F. Colocalization of immediate early genes in catecholamine cells after song exposure in female zebra finches (Taeniopygia guttata). Brain Behav. Evol. 2012, 79:252-260.
96. Maney D., Pinaud R. Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front. Neuroendocrinol. 2011, 32:287-302.
97. Maney D.L., Bernard D.J., Ball G.F. Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci. Lett. 2001, 311:189-192.
98. Maney D.L., Cho E., Goode C.T. Estrogen-dependent selectivity of genomic responses to birdsong. Eur. J. Neurosci. 2006, 23:1523-1529.
99. Maney D.L., Goode C.T., Lange H.S., Sanford S.E., Solomon B.L. Estradiol modulates neural responses to song in a seasonal songbird. J. Comp. Neurol. 2008, 511:173-186.
100. Maruska K.P., Fernald R.D. Steroid receptor expression in the fish inner-ear varies with sex, social status, and reproductive state. BMC Neurosci. 2010, 11:58.
101. Maruska K.P., Ung U.S., Fernald R.D. The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance. PLoS ONE 2012, 7:e37612.
102. Matragrano L.L., Sanford S.E., Salvante K.G., Sockman K.W., Maney D.L. Estradiol-dependent catecholaminergic innervation of auditory areas in a seasonally breeding songbird. Eur. J. Neurosci. 2011, 34:416-425.
103. Matragrano L.L., Sanford S.E., Salvante K.G., Beaulieu M., Sockman K.W., Maney D.L. Estradiol-dependent modulation of serotonergic markers in auditory areas of a seasonally breeding songbird. Behav. Neurosci. 2012, 126:110-122.
104. Matragrano L.L., Beaulieu M., Phillip J.O., Rae A.I., Sanford S.E., Sockman K.W., Maney D.L. Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway. PLoS ONE 2012, 7:e39388.
105. Maurizi M., Ottaviani F., Paludetti G., Almadori G., Pierri F., Rosignoli M. Effects of sex on auditory brainstem responses in infancy and early childhood. Scand. Audiol. 1988, 17:143-146.
106. Mayko Z.M., Roberts P.D., Portfors C.V. Inhibition shapes selectivity to vocalizations in the inferior colliculus of awake mice. Front. Neural Circuits 2012, 6:73.
107. McCarthy M.M., Kaufman L.C., Brooks P.J., Pfaff D.W., Schwartz-Giblin S. Estrogen modulation of mRNA levels for the two forms of glutamic acid decarboxylase (GAD) in female rat brain. J. Comp. Neurol. 1995, 360:685-697.
108. McFadden D. A masculinizing effect on the auditory systems of human females having male co-twins. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:11900-11904.
109. McFadden D. Sex differences in the auditory system. Dev. Neuropsychol. 1998, 14:261-298.
110. McFadden D. Masculinization effects in the auditory system. Arch. Sex. Behav. 2002, 31:99-111.
111. McFadden D. What do sex, twins, spotted hyenas, ADHD, and sexual orientation have in common?. Perspect. Psychol. Sci. 2008, 3:309-323.
112. McFadden D. Masculinization of the mammalian cochlea. Hear. Res. 2009, 252:37-48.
113. McFadden D. Sexual orientation and the auditory system. Front. Neuroendocrinol. 2011, 32:201-213.
114. McFadden D., Champlin C.A. Comparison of auditory evoked potentials in heterosexual, homosexual, and bisexual males and females. J. Assoc. Res. Otolaryngol. 2000, 1:89-99.
115. McFadden D., Loehlin J.C. On the heritability of spontaneous otoacoustic emissions: a twins study. Hear. Res. 1995, 85:181-198.
116. McFadden D., Pasanen E.G. Comparison of the auditory systems of heterosexuals and homosexuals: click-evoked otoacoustic emissions. Proc. Nat. Acad. Sci. 1998, 95:2709-2713.
117. McFadden D., Pasanen E.G. Spontaneous otoacoustic emissions in heterosexuals, homosexuals, and bisexuals. J. Acoust. Soc. Am. 1999, 105:2403-2413.
118. McFadden D., Loehlin J.C., Pasanen E.G. Additional findings on heritability and prenatal masculinization of cochlear mechanisms: click-evoked otoacoustic emissions. Hear. Res. 1996, 97:102-119.
119. McFadden D., Pasanen E.G., Raper J., Lange H.S., Wallen K. Sex differences in otoacoustic emissions measured in rhesus monkeys (Macaca mulatta). Horm. Behav. 2006, 50:274-284.
120. McFadden D., Martin G.K., Stagner B.B., Maloney M.M. Sex differences in distortion-product and transient-evoked otoacoustic emissions compared. J. Acoust. Soc. Am. 2009, 125:239-246.
121. McFadden D., Pasanen E.G., Valero M.D., Roberts E.K., Lee T.M. Effect of prenatal androgens on click-evoked otoacoustic emissions in male and female sheep (Ovis aries). Horm. Behav. 2009, 55:98-105.
122. McFadden D., Hsieh M.D., Garcia-Sierra A., Champlin C.A. Differences by sex, ear, and sexual orientation in the time intervals between successive peaks in auditory evoked potentials. Hear. Res. 2010, 270:56-64.
123. Meitzen J., Thompson C.K. Seasonal-like growth and regression of the avian song control system: neural and behavioral plasticity in adult male Gambel's white-crowned sparrows. Gen. Comp. Endocrinol. 2008, 157:259-265.
124. Mello C.V., Velho T.A., Pinaud R. Song-induced gene expression: a window on song auditory processing and perception. Ann. N. Y. Acad. Sci. 2004, 1016:263-281.
125. Meltser I., Tahera Y., Simpson E., Hultcrantz M., Charitidi K., Gustafsson J.A., Canlon B. Estrogen receptor beta protects against acoustic trauma in mice. J. Clin. Invest. 2008, 118:1563-1570.
126. 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.
127. Miller M.H., Gould W.J. Fluctuating sensorineural hearing impairment associated with the menstrual cycle. J. Audit. Res. 1967, 7:373-385.
128. Miranda J.A., Liu R.C. Dissecting natural sensory plasticity: hormones and experience in a maternal context. Hear. Res. 2009, 252:21-28.
129. Miranda J.A., Wilczynski W. Female reproductive state influences the auditory midbrain response. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 2009, 195:341-349.
130. Motohashi R., Takumida M., Shimizu A., Konomi U., Fujita K., Hirakawa K., Suzuki M., Anniko M. Effects of age and sex on the expression of estrogen receptor alpha and beta in the mouse inner-ear. Acta Otolaryngol. 2010, 130:204-214.
131. Mukhophadhyay S., Biswas S., Vindla S. Severe tinnitus in pregnancy, necessitating caesarean delivery. J. Obstet. Gynaecol. 2007, 27:81-82.
132. Murphy D.D., Cole N.B., Greenberger V., Segal M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J. Neurosci. 1998, 18:2550-2559.
133. Neuhoff J.G., Planisek R., Seifritz E. Adaptive sex differences in auditory motion perception: looming sounds are special. J. Exp. Psychol. Hum. Percept. Perform. 2009, 35:225-234.
134. Noirot I.C., Adler H.J., Cornil C.A., Harada N., Dooling R.J., Balthazart J., Ball G.F. Presence of aromatase and estrogen receptor alpha in the inner-ear of zebra finches. Hear. Res. 2009, 252:49-55.
135. 1-Noradrenegic receptor antagonism disrupts female songbird responses to male song. Neurosci. Lett. 2011, 496:20-24.
136. Penner M.J. Frequency variation of spontaneous otoacoustic emissions during a naturally occurring menstrual cycle, amenorrhea, and oral contraception: a brief report. Ear Hear. 1995, 16:428-432.
137. Peterson R.S., Yarram L., Schlinger B.A., Saldanha C.J. Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc. Biol. Sci. 2005, 272:2089-2096.
138. Phillmore L.S., Veysey A.S., Roach S.P. Zenk expression in auditory regions changes with breeding condition in male Black-capped chickadees (Poecile atricapillus). Behav. Brain Res. 2011, 225:464-472.
139. Price K., Zhu X., Guimaraes P.F., Vasilyeva O.N., Frisina R.D. Hormone replacement therapy diminishes hearing in peri-menopausal mice. Hear. Res. 2009, 252:29-36.
140. Ramekers D., Versnel H., Grolman W., Klis S.F. Neurotrophins and their role in the cochlea. Hear. Res. 2012, 288:19-33.
141. Remage-Healey L., Joshi N.R. Changing neuroestrogens within the auditory forebrain rapidly transform stimulus selectivity in a downstream sensorimotor nucleus. J. Neurosci. 2012, 32:8231-8241.
142. Remage-Healey L., Maidment N.T., Schlinger B.A. Forebrain steroid levels fluctuate rapidly during social interactions. Nat. Neurosci. 2008, 11:1327-1334.
143. Remage-Healey L., Coleman M.J., Oyama R.K., Schlinger B.A. Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3852-3857.
144. Remage-Healey L., Dong S., Maidment N.T., Schlinger B.A. Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain. J. Neurosci. 2011, 31:10034-10038.
145. Remage-Healey L., Dong S.M., Chao A., Schlinger B.A. Sex-specific, rapid neuroestrogen fluctuations and neurophysiological actions in the songbird auditory forebrain. J. Neurophysiol. 2012, 107:1621-1631.
146. Riters L.V., Pawlisch B.A. Evidence that norepinephrine influences responses to male courtship song and activity within song control regions and the ventromedial nucleus of the hypothalamus in female European starlings. Brain Res. 2007, 1149:127-140.
147. Rohmann K.N., Bass A.H. Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish. J. Exp. Biol. 2011, 214:1931-1942.
148. Rudick C.N., Woolley C.S. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J. Neurosci. 2001, 21:6532-6543.
149. Sadagopan S., Wang X. Level invariant representation of sounds by populations of neurons in primary auditory cortex. J. Neurosci. 2008, 28:3415-3426.
150. Sanford S.E., Lange H.S., Maney D.L. Topography of estradiol-modulated genomic responses in the songbird auditory forebrain. Dev. Neurobiol. 2010, 70:73-86.
151. Sator M.O., Franz P., Egarter C., Gruber D.M., Wölfl G., Nagele F. Effects of tibolone on auditory brainstem responses in postmenopausal women - a randomized, double-blind, placebo-controlled trial. Fertil. Steril. 1999, 72:885-888.
152. Schlinger B.A., Remage-Healey L. Neurosteroidogenesis: insights from studies of songbirds. J. Neuroendocrinol. 2012, 24:16-21.
153. Schmidt P.M., Flores Fda T., Rossi A.G., Silveira A.F. Hearing and vestibular complaints during pregnancy. Braz. J. Otorhinolaryngol. 2010, 76:29-33.
154. Sennaroglu G., Belgin E. Main articles audiological findings in pregnancy. J. Laryngol. Otol. 2001, 115:617-621.
155. Serova L.I., Maharjan S., Huang A., Sun D., Kaley G., Sabban E.L. Response of tyrosine hydroxylase and GTP cyclohydrolase I gene expression to estrogen in brain catecholaminergic regions varies with mode of administration. Brain Res. 2004, 1015:1-8.
156. Simonoska R., Stenberg A., Masironi B., Sahlin L., Hultcrantz M. Estrogen receptors in the inner ear during different stages of pregnancy and development in the rat. Acta Otolaryngol. 2009, 129:1175-1181.
157. Simonoska R., Stenberg A.E., Duan M., Yakimchuk K., Fridberger A., Sahlin L., Gustafsson J.A., Hultcrantz M. Inner ear pathology and loss of hearing in estrogen receptor-beta deficient mice. J. Endocrinol. 2009, 201:397-406.
158. Sisneros J.A. Adaptive hearing in the vocal plainfin midshipman fish: getting in tune for the breeding season and implications for acoustic communication. Integr. Zool. 2009, 4:33-42.
159. Sisneros J.A. Seasonal plasticity of auditory saccular sensitivity in the vocal plainfin midshipman fish, Porichthys notatus. J. Neurophysiol. 2009, 102:1121-1131.
160. Sisneros J.A. Steroid-dependent auditory plasticity for the enhancement of acoustic communication: recent insights from a vocal teleost fish. Hear. Res. 2009, 252:9-14.
161. Sisneros J.A., Bass A.H. Seasonal plasticity of peripheral auditory frequency sensitivity. J. Neurosci. 2003, 23:1049-1058.
162. Sisneros J.A., Forlano P.M., Deitcher D.L., Bass A.H. Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 2004, 305:404-407.
163. Snihur A.W., Hampson E. Sex and ear differences in spontaneous and click-evoked otoacoustic emissions in young adults. Brain Cogn. 2011, 77:40-47.
164. Snihur A.W., Hampson E. Oral contraceptive use in women is associated with defeminization of otoacoustic emission patterns. Neuroscience 2012, 210:258-265.
165. Sohrabji F., Lewis D.K. Estrogen-BDNF interactions: implications for neurodegenerative diseases. Front. Neuroendocrinol. 2006, 27:404-414.
166. Souaid J.P., Rappaport J.M. Fluctuating sensorineural hearing loss associated with the menstrual cycle. J. Otolaryngol. 2001, 30:246.
167. Staecker H., Kopke R., Malgrange B., Lefebvre P., Van De Water T.R. NT-3 and/or BDNF therapy prevents loss of auditory neurons following loss of hair cells. NeuroReport 1996, 7:889.
168. Stenberg A.E., Nylén O., Windh M., Hultcrantz M. Otological problems in children with Turner's syndrome. Hear. Res. 1998, 124:85-90.
169. Stenberg A.E., Wang H., Fish J., Schrott-Fischer A., Sahlin L., Hultcrantz M. Estrogen receptors in the normal adult and developing human inner-ear and in Turner's syndrome. Hear. Res. 2001, 157:87-92.
170. Suga N., Zhang Y., Yan J. Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. J. Neurophysiol. 1997, 77:2098-2114.
171. Swanson S.J., Dengerink H.A. Changes in pure-tone thresholds and temporary threshold shifts as a function of menstrual cycle and oral contraceptives. J. Speech Hear. Res. 1988, 31:569-574.
172. Talmadge C.L., Long G.R., Murphy W.J., Tubis A. New off-line method for detecting spontaneous otoacoustic emissions in human subjects. Hear. Res. 1993, 71:170-182.
173. Tandon O.P., Misra R., Tandon I. Brainstem auditory evoked potentials (BAEPs) in pregnant women. Ind. J. Physiol. Pharmacol. 1990, 34:42-44.
174. Tobias J.V. Consistency of sex differences in binaural-beat perception. Int. J. Audiol. 1965, 4:179-182.
175. Tremere L.A., 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.
176. Tremere L.A., Jeong J.K., 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.
177. Tremere L.A., Burrows K., Jeong J.K., Pinaud R. Organization of estrogen-associated circuits in the mouse primary auditory cortex. J. Exp. Neurosci. 2011, 2011:45-60.
178. Tsunoda K., Takahashi S., Takanosawa M., Shimoji Y. The influence of pregnancy on sensation of ear problems-ear problems associated with healthy pregnancy. J. Laryngol. Otol. 1999, 113:318-320.
179. Vasconcelos R.O., Sisneros J.A., Amorim M.C., Fonseca P.J. Auditory saccular sensitivity of the vocal Lusitanian toadfish: low frequency tuning allows acoustic communication throughout the year. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 2011, 197:903-913.
180. Velho T.A., Lu K., Ribeiro S., Pinaud R., Vicario D., Mello C.V. Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds. PLoS ONE 2012, 7:e36276.
181. vom Saal F.S. Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero. J. Anim. Sci. 1989, 67:1824-1840.
182. Vyas A., Harding C., McGowan J., Snare R., Bogdan D. Noradrenergic neurotoxin, N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine hydrochloride (DSP-4), treatment eliminates estrogenic effects on song responsiveness in female zebra finches (Taeniopygia guttata). Behav. Neurosci. 2008, 122:1148-1157.
183. Walkowiak W. The coding of auditory signals in the torus semicircularis of the fire-bellied toad and the grass frog: responses to simple stimuli and to conspecific calls. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 1980, 138:131-148.
184. Watanabe M., Maemura K., Kanbara K., Tamayama T., Hayasaki H. GABA and GABA receptors in the central nervous system and other organs. Int. Rev. Cytol. 2002, 213:1-47.
185. Wharton J.A., Church G.T. Influence of menopause on the auditory brainstem response. Audiology 1990, 29:196-201.
186. Wilczynski W., Allison J.D., Marler C.A. Sensory pathways linking social and environmental cues to endocrine control regions of amphibian forebrains. Brain Behav. Evol. 1993, 42:252-264.
187. Xie R., Meitzen J., Pollak G.D. Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei. J. Neurophysiol. 2005, 94:4019-4037.
188. Yang L., Pollak G.D., Resler C. GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J. Neurophysiol. 1992, 68:1760-1774.
189. Yovanof S., Feng A.S. Effects of estradiol on auditory evoked responses from the frog's auditory midbrain. Neurosci. Lett. 1983, 36:291-297.
190. Zakon H.H. The effects of steroid hormones on electrical activity of excitable cells. Trends Neurosci. 1998, 21:202-207.
191. Zeyl J.N., Love O.P., Higgs D.M. Condition-dependent auditory processing in the round goby (Neogobius melanostomus): links to sex, reproductive condition, and female estrogen levels. J. Exp. Biol. 2013, 216:1075-1084.
192. Zornik E., Kelley D.B. A neuroendocrine basis for the hierarchical control of frog courtship vocalizations. Front. Neuroendocrinol. 2011, 32:353-366.
193. Zuccotti A., Kuhn S., Johnson S.L., Franz C., Singer W., Hecker D., Geisler H.S., Köpschall I., Rohbock K., Gutsche K., Dlugaiczyk J., Schick B., Marcotti W., Rüttiger L., Schimmang T., Knipper M. Lack of brain-derived neurotrophic factor hampers inner hair cell synapse physiology, but protects against noise-induced hearing loss. J. Neurosci. 2012, 32:8545-8553.
194. Zündorf I.C., Karnath H.O., Lewald J. Male advantage in sound localization at cocktail parties. Cortex 2011, 47:741-749.