Effects of sex, gonadal hormones, and augmented acoustic environments on sensorineural hearing loss and the central auditory system: Insights from research on C57BL/6J mice

Hearing Research

Volumn 252, Issue 1-2, 2009, Pages 89-99

  Willott, James F ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

ABR; Augmented acoustic environment; Cochleograms; Gonadal hormones; Hair cells; Hearing loss; Mouse; Sex differences

Indexed keywords

ANDROGEN; STEROID HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY NERVOUS SYSTEM; C57BL 6 MOUSE; COCHLEAR NUCLEUS; CONTROLLED STUDY; DISEASE MODEL; DISEASE SEVERITY; ENVIRONMENTAL EXPOSURE; FEMALE; GONADECTOMY; HAIR CELL; HEARING LOSS; HORMONE BLOOD LEVEL; LOW FREQUENCY NOISE; MALE; MOUSE; NONHUMAN; ORCHIECTOMY; OVARIECTOMY; PERCEPTION DEAFNESS; PRESBYACUSIS; PRIORITY JOURNAL; SEX DIFFERENCE;

ANIMALS; AUDITORY CORTEX; AUDITORY THRESHOLD; COCHLEA; COCHLEAR NUCLEUS; DISEASE MODELS, ANIMAL; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; GONADAL STEROID HORMONES; HAIR CELLS, AUDITORY; HEARING LOSS, SENSORINEURAL; MALE; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NOISE; OVARIECTOMY; SEX CHARACTERISTICS; SPIRAL GANGLION;

EID: 67349226390     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2008.12.002     Document Type: Article

References (103)

1. Arnold A.P. Genetically triggered sexual differentiation of brain and behavior. Horm. Behav. 30 (1996) 495-505
2. Barron A.M., Fuller S.J., Verdile G., and Martins R.N. Reproductive hormones modulate oxidative stress in Alzheimer's disease. Antioxid. Redox Signal. 11-12 (2006) 2047-2059
3. Blecher S.R., and Erickson R.P. Genetics of sexual development: a new paradigm. Am. J. Med. Genet. A 143 (2007) 3054-3068
4. Bocklandt S., and Vilain E. Sex differences in brain and behavior: hormones versus genes. Adv. Genet. 59 (2007) 245-266
5. Brown J.N., Miller J.M., and Nuttall A.L. Age-related changes in cochlear vascular conductance in mice. Hear. Res. 86 (1995) 189-194
6. Caruso S., Maiolino L., Rugolo S., Intelisano G., Farina M., Cocuzza S., and Serra A. Auditory brainstem response in premenopausal women taking oral contraceptives. Hum. Reprod. 18 (2003) 85-89
7. Caruso S., Maiolino L., Agnello A., Garozzo A., Di Mari L., and Serra A. Effects of patch or gel estrogen therapies on auditory brainstem response in surgically postmenopausal women: a prospective, randomized study. Fertil. Steril. 79 (2003) 556-561
8. Charalampopoulos I., Alexaki V.I., Tsatsanis C., Minas V., Dermitzaki E., Lasaridis I., Vardouli L., Stournaras C., Margioris A.N., Castanas E., and Gravanis A. Neurosteroids as endogenous inhibitors of neuronal cell apoptosis in aging. Ann. NY Acad. Sci. 1088 (2006) 139-152
9. Cohen G.M., and Grasso J.S. Further observations on the degeneration of spiral ganglia in aging C57BL/6 mice. Assoc. Res. Otolaryngol. Abstr. 10 (1987) 12
10. Cohen G.M., and Bullers S. Age- and condition-related changes in levels of neuron specific enolase in spiral ganglion neurons of C57BL/6 mice. Assoc. Res. Otolaryngol. Abstr. 12 (1989) 357
11. Coleman J.R., Campbell D., Cooper W.A., Welsh M.G., and Moyer J. Auditory brainstem responses after ovariectomy and estrogen replacement in rat. Hear. Res. 80 (1994) 209-215
12. Colvin I., and Luxon L.M. Clinical diagnosis of noise-induced hearing loss. In: Luxon L.M., and Prasher D. (Eds). Noise and Its Effects (2007), Whurr, Chichester 182-231
13. Davis R.R. Noise-induced hearing loss. In: Willott J.F. (Ed). Handbook of Mouse Auditory Research: From Behavior to Molecular Biology (2001), CRC Press, Boca Raton 477-488
14. Davis R.R., Kozel P., and Erway L.C. Genetic influences in individual susceptibility to noise: a review. Noise Health 5 (2003) 19-28
15. Di Palma F., Holme R.H., Bryda E.C., Belyantseva I.A., Pellegrino R., Kachar B., Steel K.P., and Noben-Trauth K. Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat. Genet. 27 (2001) 103-107
16. Di Palma F., Pellegrino R., and Noben-Trauth K. Genomic structure, alternative splice forms and normal and mutant alleles of cadherin 23 (Cdh23). Gene 281 (2001) 31-41
17. Dluzen D., Jain R., and Liu B. Modulatory effects of testosterone on 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity. J. Neurochem. 62 (1994) 94-101
18. Easton A., Dwyer E., and Pfaff D.W. Estradiol and orexin-2 saporin actions on multiple forms of behavioral arousal in female mice. Behav. Neurosci. 120 (2006) 1-9
19. Erway L.C., Willott J.F., Archer J.R., and Harrison D. Genetics of age-related hearing loss in mice. I. Inbred and F1 hybrid strains. Hear. Res. 65 (1993) 125-132
20. Erway L.C., Zheng Q.Y., and Johnson K.R. Inbred strains of mice for genetics of hearing in mammals: searching for genes for hearing loss. In: Willott J.F. (Ed). Handbook of Mouse Auditory Research: From Behavior to Molecular Biology (2001), CRC Press, Boca Raton 429-440
21. Frisina R.D., and Walton J.P. Aging of the mouse central auditory system. In: Willott J.F. (Ed). Handbook of Mouse Auditory Research: From Behavior to Molecular Biology (2001), CRC Press, Boca Raton 339-380
22. Garcia-Segura L.M., Azcoitia I., and DonCarlos L.L. Neuroprotection by estradiol. Prog. Neurobiol. 63 (2001) 29-60
23. Glorig, A., 1957. Wisconsin state fail hearing survey. Am. Acad. Opthalmol. Otolaryngol.
24. Guimaraes P., Frisina S.T., Mapes F., Tadros S.F., Frisina D.R., and Frisina R.D. Progestin negatively affects hearing in aged women. Proc. Natl. Acad. Sci. USA 103 (2006) 14246-14249
25. Haack B., Markl H., and Ehret G. Sound communication between parent and offspring. In: Willott J.F. (Ed). The Auditory Psychobiology of the Mouse (1983), Charles C. Thomas, Springfield 57-97
26. Harding G.W., Bohne B.A., and Vos J.D. The effect of an age-related hearing loss gene (Ahl) on noise-induced hearing loss and cochlear damage from low-frequency noise. Hear. Res. 204 (2004) 90-100
27. Harris J.A., and Rubel E.W. Afferent regulation of neuron number in the cochlear nucleus: cellular and molecular analyses of a critical period. Hear. Res 216-217 (2006) 127-137
28. Henderson D., Bielefeld E.C., Harris K.C., and Hu B.H. The role of oxidative stress in noise-induced hearing loss. Ear Hear. 27 (2006) 1-19
29. Henry K.R. Ageing and audition. In: Willott J.F. (Ed). The Auditory Psychobiology of the Mouse (1983), Charles C. Thomas, Springfield 470-493
30. Henry K.R. Sex- and age-related elevation of cochlear nerve envelope response (CNER) and auditory brainstem response (ABR) thresholds in C57BL/6 mice. Hear. Res. 170 (2002) 107-115
31. Henry K.R. Males lose hearing earlier in mouse models of late-onset age-related hearing loss; females lose hearing earlier in mouse models of early-onset hearing loss. Hear. Res. 190 (2004) 141-148
32. Hequembourg S., and Liberman M.C. Spiral ligament pathology: a major aspect of age-related cochlear degeneration in C57BL/6 mice. J. Assoc. Res. Otolaryngol. 2 (2001) 118-129
33. Hinchcliffe R., and Jones W.I. Hearing levels of a suburban Jamaican population. Int. Audiol. 7 (1968) 239-258
34. Holme R.H., and Steel K.P. Progressive hearing loss and increased susceptibility to noise-induced hearing loss in mice carrying a Cdh23 but not a Myo7a mutation. J. Assoc. Res. Otolaryngol. 5 (2003) 66-79
35. Hultcrantz M., and Li H.S. Inner ear morphology in CBA/Ca and C57BL/6J mice in relationship to noise, age and phenotype. Eur. Arch. Otorhinolaryngol. 250 (1993) 257-264
36. Hultcrantz M., Simonoska R., and Stenberg A.E. Estrogen and hearing: a summary of recent investigations. Acta Otolaryngol. 126 (2006) 10-14
37. Humes L.E. Noise-induced hearing loss as influenced by other agents and by some physical characteristics of the individual. J. Acoust. Soc. Am. 76 (1984) 1318-1329
38. Idrizbegovic E., Bogdanovic N., Viberg A., and Canlon B. Auditory peripheral influences on calcium binding protein immunoreactivity in the cochlear nucleus during aging in the C57BL/6J mouse. Hear. Res. 179 (2003) 33-42
39. Jiang H., Talaska A.E., Schacht J., and Sha S.H. Oxidative imbalance in the aging inner ear. Neurobiol. Aging 28 (2007) 1605-1612
40. Johnson K.R., Erway L.C., Cook S.A., Willott J.F., and Zheng Q.Y. A major gene affecting age-related hearing loss in C57BL/6J mice. Hear. Res. 114 (1997) 83-92
41. Kilicdag E.B., Yavuz H., Bagis T., Tarim E., Erikan A.N., and Kazanci F. Effects of estrogen therapy on hearing in postmenopausal women. Am. J. Obstet. Gynecol. 190 (2004) 77-82
42. Kim J., Morest D.K., and Bohne B.A. Degeneration of axons in the brainstem of the chinchilla after auditory overstimulation. Hear. Res. 103 (1997) 169-191
43. Kim J.J., Gross J., Morest D.K., and Potashner S.J. Quantitative study of degeneration and new growth of axons and synaptic endings in the chinchilla cochlear nucleus after acoustic overstimulation. J. Neurosci. Res. 77 (2004) 829-842
44. Kim S.H., Kang B.M., Chae H.D., and Kim C.H. The association between serum estradiol level and hearing sensitivity in postmenopausal women. Obstet. Gynecol. 99 (2002) 726-730
45. Kimonides V.G., Khatibi N.H., Svendsen C.N., Sofroniew M.V., and Herbert J. Dehydroepiandosterone (HEA) and DHEA-sulphate (DHEAS) protect hippocampal neurons against excitatory amino acid-induced neurotoxicity. Proc. Natl. Acad. Sci. USA 95 (1998) 1852-1857
46. Kimonides V.G., Spillantini M.G., Sofroniew M.V., Fawcett J.W., and Herbert J. Dehydroepiandosterone antagonizes the neurotoxic effects of corticosterone and translocation of stress-activated protein kinase 3 in hippocampal primary cultures. Neuroscience 89 (1999) 429-436
47. Koch M., and Ehret G. Estradiol and parental experience, but not prolactin are necessary for ultrasound recognition and pup-retrieving in the mouse. Physiol. Behav. 45 (1989) 771-776
48. Laugel G.R., Dengerink H.A., and Wright J.W. Ovarian steroid and vasoconstrictor effects on cochlear blood flow. Hear. Res. 31 (1987) 245-251
49. Laugel G.R., Wright J.W., and Dengerink H.A. Angiotensin II and progesterone effects on laser Doppler measures of cochlear blood flow. Acta Otolaryngol. 106 (1988) 34-39
50. Lee J.H., and Marcus D.C. Estrogen acutely inhibits ion transport by isolated stria vascularis. Hear. Res. 158 (2001) 123-130
51. Le Prell C.G., Dolan D.F., Schacht J., Miller J.M., Lomax M.I., and Altschuler R.A. Pathways for protection from noise induced hearing loss. Noise Health 5 (2003) 1-17
52. Li H., Klein G., Sun P., and Buchan A.M. Dehydroepiandosterone (DHEA) reduces neuronal injury in a rat model of global cerebral ischemia. Brain Res. 888 (2001) 263-266
53. Li H.S., and Borg E. Age-related loss of auditory sensitivity in two mouse genotypes. Acta Otolaryngol. 111 (1991) 827-834
54. Li H.S., Hultcrantz M., and Borg E. Influence of age on noise-induced permanent threshold shifts in CBA/Ca and C57BL/6J mice. Audiology 32 (1993) 195-204
55. Maney D.L., Cho E., and Goode C.T. Estrogen-dependent selectivity of genomic responses to birdsong. Eur. J. Neurosci. 23 (2006) 1523-1529
56. McFadden D. Masculinization effects in the auditory system. Arch. Sex. Behav. 31 (2002) 99-111
57. McFadden S.L., Henselman L.W., and Zheng X.Y. Sex differences in auditory sensitivity of chinchillas before and after exposure to impulse noise. Ear Hear. 20 (1999) 164-174
58. Mishizen A., Ikonomovic M., and Armstrong D.A. Glutamate receptors in aging and Alzheimer's disease. In: Hof P.R., and Mobbs C.V. (Eds). Functional Neurobiology of Aging (2001), Academic Press, San Diego 283-314
59. Moscicki E.K., Elkins E.F., Baum H.M., and McNamara P. Hearing loss in the elderly: an epidemiologic study of the Framingham heart study cohort. Ear Hear. 6 (1985) 184-190
60. Muly S.M., Gross J.S., and Potashner S.J. Noise trauma alters d-[3H]aspartate release and AMPA binding in chinchilla cochlear nucleus. J. Neurosci. Res. 75 (2004) 585-596
61. Nelson J.F., Felicio L.S., Osterburg H.H., and Finch C.E. Altered profiles of estradiol and progesterone associated with prolonged estrus cycles and persistent vaginal cornification in aging C57BL/6J mice. Biol. Reprod. 24 (1981) 784-794
62. Nelson J.F., Felicio L.S., Osterburg H.H., and Finch C.E. Differential contributions of ovarian and extraovarian factors to age-related reductions in plasm estradiol and progesterone during the estrous cycle of C57BL/6J mice. Endocrinology 130 (1992) 805-810
63. Nelson J.F., Felicio L.S., Randall P.K., Sims C., and Finch C.E. A longitudinal study of estrus cyclicity in aging C57BL/6J mice. I. Cycle frequency, length and vaginal cytology. Biol. Reprod. 27 (1982) 327-339
64. Nelson J.F., Karelus K., Bergman M.D., and Felicio L.S. Neuroendocrine involvement in aging: evidence from studies of reproductive aging and caloric restriction. Neurobiol. Aging 16 (1995) 837-843
65. Nelson J.F., Latham K.R., and Finch C.E. Plasma testosterone levels in C57BL/6J male mice: effects of age and disease. Acta Endodrinol. 80 (1975) 742-744
66. Noben-Trauth K., Zheng Q.Y., and Johnson K.R. Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat. Genet. 35 (2003) 21-23
67. Noreña A.J., and Eggermont J.J. Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization. J. Neurosci. 25 (2005) 699-705
68. Numan M. Brain mechanisms and parental behavior. In: Adler N., Pfaff D., and Goy R.W. (Eds). Handbook of Behavioral Neurobiology vol. 7 (1985), Plenum Press, New York 537-605
69. Ohlemiller K.K., and Gagnon P.M. Apical-to-basal gradients in age-related cochlear degeneration and their relationship to "primary" loss of cochlear neurons. J. Comp. Neurol. 479 (2004) 103-116
70. Ou H.C., Bohne B.A., and Harding G.W. Noise damage in the C57BL/CBA cochlea. Hear. Res. 145 (2000) 111-122
71. Picazo O., Azcoitia I., and Garcia-Segura L.M. Neuroprotective and neurotoxic effects of estrogens. Brain Res. 990 (2003) 20-27
72. Pike C.J. Testosterone attenuates beta-amyloid toxicity in cultured hippocampal neurons. Brain Res. 919 (2001) 160-165
73. Potashner S.J., Suneja S.K., and Benson C.G. Regulation of d-aspartate release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp. Neurol. 148 (1997) 222-235
74. Pujol R., and Puel J.L. Excitotoxicity, synaptic repair, and functional recovery in the mammalian cochlea: a review of recent findings. Ann. NY Acad. Sci. 884 (1999) 249-254
75. Pujol R., Rebillard G., Puel J., Lenoir M., Eybalin M., and Recasens M. Glutamate neurotoxicity in the cochlea: a possible consequence of ischaemic or anoxic conditions occurring in aging. Acta Otolaryngol. Suppl. 476 (1990) 32-36
76. Pouliot W.A., Handa R.J., and Beck S.G. Androgen modulates N-methyl-d-aspartate-mediated depolarization in CA1 hippocampal pyramidal cells. Synapse 23 (1996) 10-19
77. Rosenblatt, J.S. Mayer, A.D. Siegel, H.I. 1985. Maternal behavior among the nonprimate mammals, in: Adler N., Pfaff, D., Goy, R.W. (Eds.), Handbook of Behavioral Neurobiology, vol. 7. Plenum Press, New York, pp. 229-298.
78. Saunders J.C., Adler H.J., Cohen Y.E., Smullen S., and Kazahaya K. Morphometric changes in the chick nucleus magnocellularis following acoustic overstimulation. J. Comp. Neurol. 390 (1998) 412-426
79. Scallet A.C. Estrogens: neuroprotective or neurotoxic?. Ann. NY Acad. Sci. 890 (1999) 121-132
80. Seidman M.D. Effects of dietary restriction and antioxidants on presbyacusis. Laryngoscope 110 (2000) 727-738
81. Seidman M.D., Shivapuja B.G., and Quirk W.S. The protective effects of allopurinol and superoxide dismutase on noise-induced cochlear damage. Otolaryngol. Head Neck Surg. 109 (1993) 1052-1056
82. Shen H., Zhang B., Shin J.H., Lei D., Du Y., Gao X., Wang Q., Ohlemiller K.K., Piccirillo J., and Bao J. Prophylactic and therapeutic functions of T-type calcium blockers against noise-induced hearing loss. Hear. Res. 226 (2007) 52-60
83. Shone G., Altschuler R.A., Miller J.M., and Nuttall A.L. The effect of noise exposure on the aging ear. Hear. Res. 56 (1991) 173-178
84. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp Neurol. 294 (1990) 76-95
85. Smittkamp S.E., and Durham D. Contributions of age, cochlear integrity, and auditory environment to avian cochlear nucleus metabolism. Hear. Res. 195 (2004) 79-89
86. Spongr V.P., Flood D.G., Frisina R.D., and Salvi R.J. Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their life spans. J. Acoust. Soc. Am. 101 (1997) 3546-3553
87. Staecker H., Zheng Q.Y., and Van De Water T.R. Oxidative stress in aging in the C57B16/J mouse cochlea. Acta Otolaryngol. 211 (2001) 666-672
88. Stenberg A.E., Wang H., Sahlin L., and Hultcrantz M. Mapping of estrogen receptors alpha and beta in the inner ear of mouse and rat. Hear. Res. 136 (1999) 29-34
89. Toran-Allerand C.D., Singh M., and Setalo Jr. G. Novel mechanisms of estrogen action in the brain: new players in an old story. Front. Neuroendocrinol. 20 (1999) 97-121
90. Vazquez A.E., Jimenez A.M., Martin G.K., Luebke A.E., and Lonsbury-Martin B.L. Evaluating cochlear function and the effects of noise exposure in the B6.CAST + Ahl mouse with distortion product otoacoustic emissions. Hear. Res. 194 (2004) 87-96
91. Willott J.F. Aging and the auditory system. In: Mohr U., Dungworth D.L., Capen C.C., Carlton W.W., Sundberg J.P., and Ward J.M. (Eds). Pathobiology of the Aging Mouse, ILSI Monographs on the Pathobiology of Aging Animals (1996), ILSI Press, Washington, DC 179-204
92. Willott J.F., and Bross L.S. Morphological changes in the anteroventral cochlear nucleus that accompany sensorineural hearing loss in DBA/2J and C57BL/6J mice. Brain Res. Dev. Brain Res. 91 (1996) 218-226
93. Willott J.F., and Bross L.S. Effects of prolonged exposure to an augmented acoustic environment on the auditory system of middle-aged C57BL/6J mice. cochlear and central histology and sex differences. J. Comp. Neurol. 472 (2004) 358-370
94. Willott J.F., Bross L.S., and McFadden S.L. Morphology of the cochlear nucleus in CBA/J mice with chronic, severe sensorineural cochlear pathology induced during adulthood. Hear. Res. 74 (1994) 1-21
95. Willott J.F., Erway L.C., Archer J.R., and Harrison D. Genetics of age-related hearing loss in mice. II. Strain differences and effects of caloric restriction on cochlear pathology and evoked response thresholds. Hear. Res. 88 (1995) 143-155
96. Willott J.F., Jackson L.M., and Hunter K.P. Morphometric study of the anteroventral cochlear nucleus of two mouse models of presbycusis. J. Comp. Neurol. 260 (1987) 472-480
97. Willott J.F., and Turner J.G. Prolonged exposure to an augmented acoustic environment ameliorates age-related auditory changes in C57BL/6J and DBA/2J mice. Hear. Res. 135 (1999) 78-88
98. Willott J.F., VandenBosche J., Shimizu T., and Ding D. Effects of exposing DBA/2J mice to a high-frequency augmented acoustic environment on the cochlea and anteroventral cochlear nucleus. Hear. Res. 216-217 (2006) 138-145
99. Willott J.F., VandenBosche J., Shimizu T., Ding D., and Salvi R. Effects of exposing gonadectomized and intact C57BL/6J mice to a high-frequency augmented acoustic environment: auditory brainstem response thresholds and cytocochleograms. Hear. Res. 221 (2006) 73-81
100. Willott J.F., VandenBosche J., Shimizu T., Ding D., and Salvi R. Effects of exposing C57BL/6J mice to high- and low-frequency augmented acoustic environments: auditory brainstem response thresholds, cytocochleograms, anterior cochlear nucleus morphology and the role of gonadal hormones. Hear. Res. 235 (2008) 60-71
101. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., and Böttner M. Minireview: neuroprotective effects of estrogen-new insights into mechanisms of action. Endocrinology 142 (2001) 969-973
102. Zheng Q.Y., Yan D., Ouyang X.M., Du L.L., Yu H., Chang B., Johnson K.R., and Liu X.Z. Digenic inheritance of deafness caused by mutations in genes encoding cadherin 23 and protocadherin 15 in mice and humans. Hum. Mol. Genet. 14 (2005) 103-111
103. Zhu X., Vasilyeva O.N., Kim S., Jacobson M., Romney J., Waterman M.S., Tuttle D., and Frisina R.D. Auditory efferent feedback system deficits precede age-related hearing loss: contralateral suppression of otoacoustic emissions in mice. J. Comp. Neurol. 503 (2007) 593-604