title: Estrogenic modulation of auditory processing: a vertebrate comparison.
abstract: Sex-steroid hormones are well-known regulators of vocal motor behavior in several organisms. A large body of evidence now indicates that these same hormones modulate processing at multiple levels of the ascending auditory pathway. The goal of this review is to provide a comparative analysis of the role of estrogens in vertebrate auditory function. Four major conclusions can be drawn from the literature: First, estrogens may influence the development of the mammalian auditory system. Second, estrogenic signaling protects the mammalian auditory system from noise- and age-related damage. Third, estrogens optimize auditory processing during periods of reproductive readiness in multiple vertebrate lineages. Finally, brain-derived estrogens can act locally to enhance auditory response properties in at least one avian species. This comparative examination may lead to a better appreciation of the role of estrogens in the processing of natural vocalizations and mayprovide useful insights toward alleviating auditory dysfunctions emanating from hormonal imbalances.
authors.affiliation: Neurobiology and Behavior Graduate Program, University of Washington, 1959 NE Pacific St., Seattle, WA 98195, USA; Virginia Merrill Bloedel Hearing Research Center, University of Washington, 1959 NE Pacific St., Seattle, WA 98195, USA. Electronic address: mcaras@u.washington.edu.
authors.forename: Melissa L
authors.initials: ML
authors.lastname: Caras
mesh_terms: D000818:Animals; D001306:Auditory Pathways / Q000378:metabolism*; D001921:Brain / Q000378:metabolism*; D004967:Estrogens / Q000378:metabolism*; D012739:Gonadal Steroid Hormones / Q000378:metabolism; D006801:Humans; D012725:Sexual Behavior; D014714:Vertebrates / Q000378:metabolism*
chemical_list: D004967:Estrogens; D012739:Gonadal Steroid Hormones
keywords: Auditory; Comparative; Estradiol; Estrogen; Hearing; Hormone; Seasonal; Sensory; Steroid
references.citation: Ann N Y Acad Sci. 2004 Jun;1016:560-85
references.pmid: 15313795
references.citation: J Neurosci. 2003 Feb 1;23(3):1049-58
references.pmid: 12574435
references.citation: Neuron. 2009 Jun 11;62(5):705-16
references.pmid: 19524529
references.citation: Clin Otolaryngol Allied Sci. 1993 Aug;18(4):294-7
references.pmid: 8877189
references.citation: Hear Res. 2009 Jun;252(1-2):21-8
references.pmid: 19401225
references.citation: Neurosci Lett. 2001 Oct 5;311(3):189-92
references.pmid: 11578826
references.citation: Hear Res. 2009 Jun;252(1-2):29-36
references.pmid: 19269311
references.citation: J Neuroendocrinol. 2012 Jan;24(1):16-21
references.pmid: 21535249
references.citation: Scand Audiol. 1988;17(3):143-6
references.pmid: 3206180
references.citation: Hear Res. 2010 Dec 1;270(1-2):56-64
references.pmid: 20875848
references.citation: J Neurosci. 2012 Jun 20;32(25):8545-53
references.pmid: 22723694
references.citation: J Laryngol Otol. 1999 Apr;113(4):318-20
references.pmid: 10474664
references.citation: Acta Otolaryngol. 2007 Feb;127(2):149-55
references.pmid: 17364346
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2011 Sep;197(9):903-13
references.pmid: 21559971
references.citation: Hear Res. 1994 Jun 1;76(1-2):127-32
references.pmid: 7928705
references.citation: Hear Res. 1995 May;85(1-2):181-98
references.pmid: 7559174
references.citation: J Exp Psychol Hum Percept Perform. 2009 Feb;35(1):225-34
references.pmid: 19170484
references.citation: Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2709-13
references.pmid: 9482952
references.citation: Gen Comp Endocrinol. 1997 May;106(2):155-68
references.pmid: 9169111
references.citation: Horm Behav. 2009 Jan;55(1):98-105
references.pmid: 18834887
references.citation: Curr Opin Neurobiol. 2011 Apr;21(2):339-44
references.pmid: 21376567
references.citation: Behav Neurosci. 2008 Oct;122(5):1148-57
references.pmid: 18823170
references.citation: J Exp Biol. 2009 Dec;212(Pt 23):3817-22
references.pmid: 19915123
references.citation: Hear Res. 1994 Nov;80(2):209-15
references.pmid: 7896579
references.citation: Scand Audiol. 1998;27(2):81-93
references.pmid: 9638827
references.citation: Hear Res. 1993 Dec;71(1-2):170-82
references.pmid: 8113135
references.citation: Science. 1998 Dec 18;282(5397):2250-4
references.pmid: 9856946
references.citation: Acta Otolaryngol. 2003 Jan;123(2):253-7
references.pmid: 12701752
references.citation: Trends Neurosci. 1998 May;21(5):202-7
references.pmid: 9610884
references.citation: J Neurophysiol. 2012 Mar;107(6):1621-31
references.pmid: 22190616
references.citation: Hear Res. 2011 Sep;279(1-2):43-50
references.pmid: 21447375
references.citation: J Acoust Soc Am. 1978 Nov;64(5):1386-91
references.pmid: 744838
references.citation: J Endocrinol. 2006 Feb;188(2):155-65
references.pmid: 16461543
references.citation: J Neurosci. 2011 Jul 6;31(27):10034-8
references.pmid: 21734295
references.citation: Neuroscience. 2010 Feb 3;165(3):923-33
references.pmid: 19925852
references.citation: Ear Hear. 1995 Aug;16(4):428-32
references.pmid: 8549898
references.citation: BMC Neurosci. 2010 Apr 30;11:58
references.pmid: 20433748
references.citation: J Acoust Soc Am. 1999 Apr;105(4):2403-13
references.pmid: 10212421
references.citation: J Exp Biol. 2013 Mar 15;216(Pt 6):1075-84
references.pmid: 23197092
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2007 Feb;193(2):201-15
references.pmid: 17066303
references.citation: J Acoust Soc Am. 1992 Mar;91(3):1571-5
references.pmid: 1564194
references.citation: Behav Brain Res. 2011 Dec 1;225(2):464-72
references.pmid: 21854811
references.citation: Arch Sex Behav. 2002 Feb;31(1):99-111
references.pmid: 11910797
references.citation: J Obstet Gynaecol. 2007 Jan;27(1):81-2
references.pmid: 17365468
references.citation: J Neurobiol. 2005 Oct;65(1):22-36
references.pmid: 16003763
references.citation: Naturwissenschaften. 1987 Jan;74(1):47
references.pmid: 3561521
references.citation: Audiology. 1990;29(4):196-201
references.pmid: 2222288
references.citation: Acta Otolaryngol. 2009 Dec;129(12):1434-41
references.pmid: 19922094
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2002 Dec;188(11-12):981-92
references.pmid: 12471495
references.citation: Brain Res Brain Res Rev. 2003 Apr;42(1):33-84
references.pmid: 12668290
references.citation: PLoS One. 2012;7(6):e39388
references.pmid: 22724011
references.citation: Ann N Y Acad Sci. 2004 Jun;1016:263-81
references.pmid: 15313780
references.citation: Hear Res. 1998 Oct;124(1-2):85-90
references.pmid: 9822905
references.citation: Neuroscience. 2010 Nov 10;170(4):1270-81
references.pmid: 20736049
references.citation: Neuroreport. 1996 Mar 22;7(4):889-94
references.pmid: 8724667
references.citation: Brain Res. 2004 Jul 23;1015(1-2):1-8
references.pmid: 15223360
references.citation: PLoS One. 2012;7(5):e36276
references.pmid: 22574146
references.citation: J Acoust Soc Am. 1983 Apr;73(4):1277-82
references.pmid: 6853839
references.citation: Endocrinology. 2010 Jun;151(6):2411-22
references.pmid: 20392826
references.citation: J Speech Hear Res. 1988 Dec;31(4):569-74
references.pmid: 3230886
references.citation: Hum Reprod. 2003 Jan;18(1):85-9
references.pmid: 12525445
references.citation: Brain Cogn. 2011 Oct;77(1):40-7
references.pmid: 21783304
references.citation: Hear Res. 1992 Feb;58(1):91-100
references.pmid: 1559910
references.citation: Hear Res. 1997 Jan;103(1-2):69-74
references.pmid: 9007575
references.citation: Audiology. 1999 Jan-Feb;38(1):7-12
references.pmid: 10052830
references.citation: Laryngoscope. 1990 Jan;100(1):18-24
references.pmid: 2104552
references.citation: Proc Biol Sci. 2005 Oct 7;272(1576):2089-96
references.pmid: 16191621
references.citation: Neurosci Lett. 1983 Apr 29;36(3):291-7
references.pmid: 6602956
references.citation: Front Neural Circuits. 2012 Oct 11;6:73
references.pmid: 23087616
references.citation: Obstet Gynecol. 1989 Sep;74(3 Pt 2):506-9
references.pmid: 2527349
references.citation: Hear Res. 1992 Dec;64(1):93-8
references.pmid: 1490905
references.citation: J Neurophysiol. 2009 Aug;102(2):1121-31
references.pmid: 19553489
references.citation: J Neurophysiol. 2002 Oct;88(4):1941-54
references.pmid: 12364520
references.citation: J Neurosci. 2009 May 6;29(18):5949-63
references.pmid: 19420261
references.citation: J Anim Sci. 1989 Jul;67(7):1824-40
references.pmid: 2670873
references.citation: Ear Hear. 1980 Jul-Aug;1(4):219-22
references.pmid: 7409360
references.citation: J Neurosci. 2011 Mar 2;31(9):3271-89
references.pmid: 21368039
references.citation: Behav Brain Res. 2002 Jul 18;133(2):221-35
references.pmid: 12110456
references.citation: Curr Opin Neurobiol. 2004 Aug;14(4):488-95
references.pmid: 15321070
references.citation: Neuroreport. 2002 Nov 15;13(16):2005-9
references.pmid: 12438915
references.citation: Brain Res. 2007 Sep 26;1171:93-103
references.pmid: 17764666
references.citation: J Endocrinol. 2009 Jun;201(3):397-406
references.pmid: 19293293
references.citation: Br J Audiol. 1978 Nov;12(4):105-18
references.pmid: 728655
references.citation: Am J Obstet Gynecol. 2004 Jan;190(1):77-82
references.pmid: 14749639
references.citation: Front Neuroendocrinol. 2006 Dec;27(4):404-14
references.pmid: 17069877
references.citation: Brain. 1971;94(4):681-96
references.pmid: 5132966
references.citation: Hear Res. 2009 Jun;252(1-2):71-8
references.pmid: 19450435
references.citation: Q Rev Biol. 2012 Dec;87(4):289-313
references.pmid: 23397795
references.citation: J Comp Neurol. 1999 Apr 28;407(1):115-29
references.pmid: 10213192
references.citation: J Neurophysiol. 1997 Apr;77(4):2098-114
references.pmid: 9114258
references.citation: Brain Behav Evol. 1993;42(4-5):252-64
references.pmid: 8252377
references.citation: Eur J Neurosci. 2011 Aug;34(3):416-25
references.pmid: 21714815
references.citation: Neuron. 2012 Jun 7;74(5):801-8
references.pmid: 22681685
references.citation: J Neurosci. 2001 Sep 1;21(17):6532-43
references.pmid: 11517242
references.citation: Proc Biol Sci. 2013 Jan 22;280(1751):20122296
references.pmid: 23193125
references.citation: J Laryngol Otol. 2012 Apr;126(4):337-9
references.pmid: 22309465
references.citation: J Neurosci. 2001 Sep 15;21(18):7303-12
references.pmid: 11549740
references.citation: Horm Behav. 2010 Sep;58(4):619-27
references.pmid: 20600046
references.citation: Horm Behav. 2006 Jun;50(1):101-6
references.pmid: 16545384
references.citation: J Neurosci. 2004 Sep 1;24(35):7745-53
references.pmid: 15342742
references.citation: Hear Res. 2004 Jun;192(1-2):83-9
references.pmid: 15157966
references.citation: Hear Res. 2009 Jun;252(1-2):15-20
references.pmid: 19272318
references.citation: Int Rev Cytol. 2002;213:1-47
references.pmid: 11837891
references.citation: Hear Res. 2009 Jun;252(1-2):9-14
references.pmid: 19168118
references.citation: J Exp Biol. 2011 Jun 1;214(Pt 11):1931-42
references.pmid: 21562181
references.citation: Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11900-4
references.pmid: 8265645
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2010 Aug;196(8):581-99
references.pmid: 20563817
references.citation: Ear Hear. 1988 Aug;9(4):168-76
references.pmid: 3169397
references.citation: J Neurosci. 2012 Jan 25;32(4):1366-76
references.pmid: 22279221
references.citation: J Neurosci. 1998 Apr 1;18(7):2550-9
references.pmid: 9502814
references.citation: J Acoust Soc Am. 2009 Jan;125(1):239-46
references.pmid: 19173411
references.citation: J Comp Neurol. 2005 Feb 28;483(1):91-113
references.pmid: 15672394
references.citation: Science. 1970 Mar 13;167(3924):1517-8
references.pmid: 5415287
references.citation: Front Neuroendocrinol. 2011 Aug;32(3):353-66
references.pmid: 21192966
references.citation: J Neurophysiol. 1992 Nov;68(5):1760-74
references.pmid: 1479443
references.citation: Endocrinology. 2012 Sep;153(9):4412-21
references.pmid: 22778224
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2009 Apr;195(4):341-9
references.pmid: 19184041
references.citation: Ir J Med Sci. 2011 Mar;180(1):79-84
references.pmid: 20665123
references.citation: Neuroscience. 2012 May 17;210:258-65
references.pmid: 22410343
references.citation: J Comp Neurol. 1995 Oct 2;360(4):685-97
references.pmid: 8801259
references.citation: Neurosci Lett. 2011 May 27;496(1):20-4
references.pmid: 21463661
references.citation: Br Med Bull. 2002;63:223-41
references.pmid: 12324396
references.citation: Neuroreport. 1999 Aug 2;10(11):2341-5
references.pmid: 10439460
references.citation: J Neurosci. 2009 Jul 8;29(27):8790-7
references.pmid: 19587286
references.citation: Integr Zool. 2009 Mar;4(1):33-42
references.pmid: 21392275
references.citation: Hear Res. 2001 Jul;157(1-2):87-92
references.pmid: 11470188
references.citation: Brain Res Cogn Brain Res. 2004 Mar;19(1):92-9
references.pmid: 14972362
references.citation: Front Neuroendocrinol. 2011 Apr;32(2):201-13
references.pmid: 21310172
references.citation: Brain Res. 2007 May 29;1149:127-40
references.pmid: 17379191
references.citation: Nat Neurosci. 2008 Nov;11(11):1327-34
references.pmid: 18820691
references.citation: PLoS Biol. 2007 Jul;5(7):e173
references.pmid: 17564499
references.citation: Indian J Physiol Pharmacol. 1990 Jan;34(1):42-4
references.pmid: 2361723
references.citation: J Aud Res. 1986 Jul;26(3):197-206
references.pmid: 3680149
references.citation: Hear Res. 1992 Jul;60(2):143-8
references.pmid: 1639724
references.citation: J Laryngol Otol. 2001 Aug;115(8):617-21
references.pmid: 11535140
references.citation: Obstet Gynecol. 2002 May;99(5 Pt 1):726-30
references.pmid: 11978279
references.citation: Dev Neurobiol. 2010 Feb;70(2):73-86
references.pmid: 19885833
references.citation: Science. 1980 Mar 21;207(4437):1377-9
references.pmid: 7355296
references.citation: Eur J Pediatr. 2000 Oct;159(10):740-4
references.pmid: 11039128
references.citation: J Neurosci. 2005 May 18;25(20):4952-63
references.pmid: 15901776
references.citation: Indian J Physiol Pharmacol. 2005 Jul-Sep;49(3):345-52
references.pmid: 16440855
references.citation: Hear Res. 2009 Jun;252(1-2):3-8
references.pmid: 19095053
references.citation: Brain Behav Evol. 2012;79(4):252-60
references.pmid: 22572406
references.citation: Hear Res. 1996 Aug;97(1-2):102-19
references.pmid: 8844191
references.citation: J Assoc Res Otolaryngol. 2000 Aug;1(1):89-99
references.pmid: 11548240
references.citation: Arch Otolaryngol. 1980 Jul;106(7):387-91
references.pmid: 7387524
references.citation: Hear Res. 2010 Sep 1;268(1-2):114-22
references.pmid: 20685243
references.citation: J Neurophysiol. 2005 Dec;94(6):4019-37
references.pmid: 16135548
references.citation: J Exp Neurosci. 2011 Oct 25;2011(5):45-60
references.pmid: 22545003
references.citation: Eur J Neurosci. 2011 Jul;34(2):283-91
references.pmid: 21707790
references.citation: Science. 2004 Jul 16;305(5682):404-7
references.pmid: 15256672
references.citation: J Neurosci. 2012 Jun 13;32(24):8231-41
references.pmid: 22699904
references.citation: J Otolaryngol. 2001 Aug;30(4):246-50
references.pmid: 11771038
references.citation: Fertil Steril. 2003 Mar;79(3):556-61
references.pmid: 12620439
references.citation: Gen Comp Endocrinol. 2008 Jul;157(3):259-65
references.pmid: 18457836
references.citation: J Comp Neurol. 2008 Nov 10;511(2):173-86
references.pmid: 18770869
references.citation: Mol Cell Endocrinol. 2009 Sep 24;308(1-2):17-25
references.pmid: 19549588
references.citation: Acta Otolaryngol. 2010 Feb;130(2):204-14
references.pmid: 19479455
references.citation: Hear Res. 2009 Jun;252(1-2):37-48
references.pmid: 19272340
references.citation: Indian J Physiol Pharmacol. 2003 Oct;47(4):393-9
references.pmid: 15266950
references.citation: Behav Neurosci. 2000 Jun;114(3):526-42
references.pmid: 10883803
references.citation: Cortex. 2011 Jun;47(6):741-9
references.pmid: 20828679
references.citation: Eur J Neurosci. 2006 Jun;23(11):3087-97
references.pmid: 16819999
references.citation: Early Hum Dev. 1996 Jul 19;45(3):215-28
references.pmid: 8855395
references.citation: Braz J Otorhinolaryngol. 2010 Jan-Feb;76(1):29-33
references.pmid: 20339686
references.citation: J Clin Invest. 2008 Apr;118(4):1563-70
references.pmid: 18317592
references.citation: Brain Res. 1990 Jul 23;523(2):251-62
references.pmid: 1698105
references.citation: J Neurosci. 2010 Sep 8;30(36):12075-83
references.pmid: 20826670
references.citation: Hear Res. 2012 Jun;288(1-2):19-33
references.pmid: 22465680
references.citation: Horm Behav. 2006 Aug;50(2):274-84
references.pmid: 16678823
references.citation: Fertil Steril. 1999 Nov;72(5):885-8
references.pmid: 10560994
references.citation: Front Neuroendocrinol. 2011 Aug;32(3):287-302
references.pmid: 21146556
references.citation: Perspect Psychol Sci. 2008 Jul;3(4):309-23
references.pmid: 26158951
references.citation: J Neurosci. 2012 Dec 5;32(49):17597-611
references.pmid: 23223283
references.citation: J Neurosci. 2008 Mar 26;28(13):3415-26
references.pmid: 18367608
references.citation: Physiol Behav. 2009 Mar 2;96(3):428-33
references.pmid: 19061908
references.citation: Behav Neurosci. 2012 Feb;126(1):110-22
references.pmid: 21942431
references.citation: Brain Res Rev. 2008 Mar;57(2):299-308
references.pmid: 17524490
references.citation: Anat Rec (Hoboken). 2012 Nov;295(11):1877-95
references.pmid: 23044862
references.citation: PLoS One. 2012;7(5):e37612
references.pmid: 22624055
references.citation: Acta Otolaryngol. 2009 Nov;129(11):1175-81
references.pmid: 19863307
references.citation: Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3852-7
references.pmid: 20133597
references.citation: Eur J Neurosci. 2006 Mar;23(6):1523-9
references.pmid: 16553615
references.citation: Hear Res. 2009 Jun;252(1-2):49-55
references.pmid: 19397967