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The Physiology of Cochlear Presbycusis

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The Aging Auditory System

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 34))

Abstract

The effects of pure aging on the physiology and morphology of the human peripheral auditory system are difficult to study given the variability inherent in genetics and the environment with which the system must cope. Environmental exposures accumulated over a lifetime often combine mild, continuous noise exposures occurring daily, with occasional punctate episodes of very high decibel trauma associated with loud music, power equipment, and small arms fire. Moreover, the human experience includes many drugs that often have unintended side effects on the auditory periphery. Some drugs have well-known ototoxic properties; others are more insidious, like the continuous high-level use of some narcotics. Noise and drug injuries tend to preferentially damage the hair cells in the cochlea.

Genetics must then respond to an individual’s environment, resulting in the very large variability present in the hearing capabilities of elderly humans. It is clear that animal models of age-related hearing loss are required to tease out the effects of aging alone from the effects of environment and genetics. Yet up until ∼25 years ago, much of the research in presbycusis was accomplished by using human temporal bones and clinical data (Bredberg 1968; Schuknecht 1974; Gates et al. 1990; Schuknecht and Gacek 1993). Only in the last 30 years or so have animal models been established where the environment, diet, and genetics are strictly controlled (Keithley and Feldman 1979, 1982; Henry 1982; Keithley et al. 1989; Mills et al. 1990; Hequembourg and Liberman 2001; Ohlemiller and Gagnon 2004; for reviews see Willott 1991; Frisina and Walton 2001, 2006; Gates and Mills 2005; Canlon, Illing, and Walton, Chapter 3). Animals raised under these controlled conditions nonetheless show age-related declines in auditory function, consistent with the notion that presbycusis includes effects unique to aging and is not just the result of the combined effects of noise and other ototoxic factors over a lifetime.

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References

  • Adams J (2008) Noise induced stress responses of the cochlear lateral wall. Abstr Assoc Res Otolaryngol 31:236.

    Google Scholar 

  • Adams J, McCaffery S, Kujawa SG (2007) Effects of acoustic trauma in the spiral ligament. Abstr Assoc Res Otolaryngol 30:243.

    Google Scholar 

  • Bhattacharyya TK, Dayal VS (1985) Age-related cochlear hair cell loss in the chinchilla. Ann Otol Rhinol Laryngol 94:75–80.

    CAS  PubMed  Google Scholar 

  • Bhattacharyya TK, Dayal VS (1989) Influence of age on hair cell loss in the rabbit cochlea. Anat Rec 230:136–145.

    Article  Google Scholar 

  • Bobbin RP (1992) Pharmacologic approach to acoustic trauma in the cochlea. In: Dancer A, Henderson D, Salvi R, Hamernik R (eds) Noise-Induced Hearing Loss. St. Louis: Mosby-Year Book, pp. 38–44.

    Google Scholar 

  • Boettcher FA, Gratton MA, Schmiedt RA (1995) Effects of noise and age on the auditory system. In: Morata T, Dunn D (eds) Occupational Medicine: State of the Art Reviews. Vol. 10, No. 3: Occupational Hearing Loss Philadelphia: Hanley and Belfus, pp. 577–592.

    Google Scholar 

  • Bredberg G (1968) Cellular pattern and nerve supply of the human organ of Corti. Acta Otolaryngol Suppl (Stockh) 236:1–135.

    Google Scholar 

  • Cooper N, Rhode W (1997) Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea. J Neurophysiol 78:261–270.

    CAS  PubMed  Google Scholar 

  • Davis H (1983) An active process in cochlear mechanics. Hear Res 9:79–90.

    Article  CAS  PubMed  Google Scholar 

  • Dayal VS, Bhattacharyya TK (1989) Comparative study of age-related cochlear hair cell loss. Hear Res 15:179–183.

    Google Scholar 

  • Dazart S, Feldman ML, Keithley EM (1996) Cochlear spiral ganglion degeneration in wild-caught mice as a function of age. Hear Res 100:101–106.

    Article  Google Scholar 

  • Dorn PA, Piskorski P, Keefe DH, Neely ST, Gorga MP (1998) On the existence of an age/threshold/frequency interaction in distortion product otoacoustic emissions. J Acoust Soc Am 104:964–971.

    Article  CAS  PubMed  Google Scholar 

  • Dubno JR, Lee FS, Matthews LJ, Ahlstrom JB, Horwitz AR, Mills JH (2008) Longitudinal changes in speech recognition in older persons. J Acoust Soc Am 123:462–475.

    Article  PubMed  Google Scholar 

  • Evans EF, Klinke R (1982) The effects of intracochlear and systemic furosemide on the properties of single cochlear nerve fibres in the cat. J Physiol 331:409–427.

    CAS  PubMed  Google Scholar 

  • Frisina RD, Walton JP (2001) Aging of the mouse central auditory system. In: Willot JP (ed) Handbook of Mouse Auditory Research: From Behavior to Molecular Biology. New York: CRC Press, pp. 339–379.

    Chapter  Google Scholar 

  • Frisina RD, Walton JP (2006) Age-related structural and functional changes in the cochlear nucleus. Hear Res 217:216–233.

    Article  Google Scholar 

  • Gates GA, Mills JH (2005) Presbycusis. Lancet 366:1111–1120.

    Article  PubMed  Google Scholar 

  • Gates GA, Cooper JC, Kannel WB, Miller NJ (1990) Hearing in the elderly: the Framingham cohort, 1983–1985. Ear Hear 11:247–256.

    Article  CAS  PubMed  Google Scholar 

  • Gates GA, Mills DM, Nam B-H, D’Agostino R, Rubel EW (2002) Effects of age on the distortion-product otoacoustic emission growth functions. Hear Res 163:53–60.

    Article  PubMed  Google Scholar 

  • Gratton MA, Schmiedt RA, Schulte BA (1996) Age-related decreases in endocochlear potential are associated with vascular abnormalities in the stria vascularis. Hear Res 94:116–124.

    Article  CAS  PubMed  Google Scholar 

  • Gratton MA, Smythe BJ, Lam CF, Boettcher FA, Schmiedt RA (1997) Decline in the endocochlear potential corresponds to decreased Na,K-ATPase activity in the lateral wall of quiet-aged gerbils. Hear Res 108:9–16.

    Article  CAS  PubMed  Google Scholar 

  • Gruber J, Schaffer S, Halliwell B (2008) The mitochondrial free radical theory of ageing - where do we stand? Front Biosci 13:6554–6579.

    Article  CAS  PubMed  Google Scholar 

  • He N, Schmiedt RA (1996) Effects of aging on the fine structure of the 2f1-f2 acoustic distortion product. J Acoust Soc Am 99:1002–1015.

    Article  CAS  PubMed  Google Scholar 

  • Hellstrom LI, Schmiedt RA (1990) Compound action potential input/output functions in young and quiet-aged gerbils. Hear Res 50:163–174.

    Article  CAS  PubMed  Google Scholar 

  • Hellstrom LI, Schmiedt RA (1991) Rate-level functions of auditory-nerve fibers have similar slopes in young and old gerbils. Hear Res 53:217–221.

    Article  CAS  PubMed  Google Scholar 

  • Hellstrom LI, Schmiedt RA (1996) Measures of tuning and suppression in single-fiber and whole-nerve reponses in young and quiet-aged gerbils. J Acoust Soc Am 100:3275–3285.

    Article  CAS  PubMed  Google Scholar 

  • Henry KR (1982) Age-related auditory loss and genetics: an electrocochleographic comparison of six inbred strains of mice. J Gerontol 37:275–282.

    CAS  PubMed  Google Scholar 

  • Hequembourg S, Liberman MC (2001) Spiral ligament pathology: a major aspect of age-related cochlear degeneration in C57BL/6 mice. J Assoc Res Otolaryngol 2:118–129.

    CAS  PubMed  Google Scholar 

  • Ichimiya I, Suzuki M, Mogi G (2000) Age-related changes in the murine cochlear lateral wall. Hear Res 139:116–122.

    Article  CAS  PubMed  Google Scholar 

  • Jerger J, Chmiel R, Stach B, Spretjnak M (1993) Gender affects audiometric shape in presbyacusis. J Am Acad Audiol 4:42–49.

    CAS  PubMed  Google Scholar 

  • Johnson KR, Erway LC, Cook SA, Willott JF, Zheng QY (1997) A major gene affecting age-related hearing loss in C57BL/6J mice. Hear Res 114:83–92.

    Article  CAS  PubMed  Google Scholar 

  • Johnson LG, Hawkins JE Jr (1972) Sensory and neural degeneration with aging as seen in microdissections of the human inner ear. Ann Otol Rhinol Laryngol 81:179–193.

    Google Scholar 

  • Kawase T, Liberman MC (1992) Spatial organization of the auditory nerve according to spontaneous discharge rate. J Comp Neurol 319:312–318.

    Article  CAS  PubMed  Google Scholar 

  • Keithley EM, Feldman ML (1979) Spiral ganglion cell counts in an age-graded series of rat cochleas. J Comp Neurol 188:429–442.

    Article  CAS  PubMed  Google Scholar 

  • Keithley EM, Feldman ML (1982) Hair cell counts in an age-graded series of rat cochleas. Hear Res 3:249–262.

    Article  Google Scholar 

  • Keithley EM, Ryan AF, Woolf NK (1989) Spiral ganglion cell density in young and old gerbils. Hear Res 38:125–134.

    Article  CAS  PubMed  Google Scholar 

  • Lang H, Schulte BA, Schmiedt RA (2002) Endocochlear potentials and compound action potential recovery functions in the C57BL/6J mouse model. Hear Res 172:118–126.

    Article  CAS  PubMed  Google Scholar 

  • Lang H, Schulte BA, Schmiedt RA (2003) Effects of chronic furosemide treatment and age on cell division in the adult gerbil inner ear. J Assoc Res Otolaryngol 4:164–175.

    Article  CAS  PubMed  Google Scholar 

  • Lang H, Schulte BA, Schmiedt RA (2005) Ouabain induces apoptotic cell death in type I spiral ganglion neurons, but not type II neurons. J Assoc Res Otolaryngol 6:63–74.

    Article  CAS  PubMed  Google Scholar 

  • Lang H, Schulte BA, Schmiedt RA (2006a) Contribution of bone marrow hematopoietic stem cells to adult mouse inner ear: mesenchymal cells and fibrocytes. J Comp Neurol 496:187–201.

    Article  PubMed  Google Scholar 

  • Lang H, Schulte BA, Zhou D, Smythe, N, Spicer SS, Schmiedt RA (2006b) Nuclear factor κB deficiency is associated with auditory nerve degeneration and increased noise-induced hearing loss. J Neurosci 26:3541–3550.

    Article  CAS  PubMed  Google Scholar 

  • Lang H, Schulte BA, Goddard JC, Hedrick M, Schulte JB, Wei L, Schmiedt RA (2008) Transplantation of mouse embryonic stem cells into the cochlea of an auditory-neuropathy animal model: effects of timing after injury. J Assoc Res Otolaryngol 9:225–240.

    Article  PubMed  Google Scholar 

  • Lee FS, Matthews LJ, Dubno JR, Mills JH (2005) Longitudinal study of pure-tone thresholds in older persons. Ear Hear 26:1–11.

    Article  PubMed  Google Scholar 

  • Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455.

    Article  CAS  PubMed  Google Scholar 

  • Marcus DC, Chiba T (1999) K+ and Na+ absorption by outer sulcus epithelial cells. Hear Res 134:48–56.

    Article  CAS  PubMed  Google Scholar 

  • Marcus DC, Wu T, Wangemann P, Kofuji P (2002) KCNJ10 (Kir4.1) potassium channel knockout abolishes endocochlear potential. Am J Physiol Cell Physiol 282:C403-C407.

    CAS  PubMed  Google Scholar 

  • Martinez-Monedero R, Oshima K, Heller S, Edge AS (2007) The potential role of endogenous stem cells in regeneration of the inner ear. Hear Res 227:48–52.

    Article  CAS  PubMed  Google Scholar 

  • McFadden SL, Campo P, Quaranta N, Henderson D (1997a) Age-related decline of auditory function in the chinchilla (Chinchilla laniger). Hear Res 111:114–126.

    Article  CAS  PubMed  Google Scholar 

  • McFadden SL, Quaranta N, Henderson D (1997b) Suprathreshold measures of auditory function in the aging chinchilla. Hear Res 111:127–135.

    Article  CAS  PubMed  Google Scholar 

  • Mills DM (2003) Differential responses to acoustic damage and furosemide in auditory brainstem and otoacoustic emission measures. J Acoust Soc Am 113:914–924.

    Article  PubMed  Google Scholar 

  • Mills DM (2006) Determining the cause of hearing loss: differential diagnosis using a comparison of audiometric and otoacoustic emission responses. Ear Hear 27:508–525.

    Article  PubMed  Google Scholar 

  • Mills DM, Rubel EW (1994) Variation of distortion product otoacoustic emissions with furosemide injection. Hear Res 77:183–199.

    Article  CAS  PubMed  Google Scholar 

  • Mills DM, Schmiedt RA (2004) Metabolic presbycusis: differential changes in auditory brainstem and otoacoustic emission responses with chronic furosemide application in the gerbil. J Assoc Res Otolaryngol 5:1–10.

    Article  PubMed  Google Scholar 

  • Mills DM, Norton SJ, Rubel EW (1993) Vulnerability and adaptation of distortion product otoacoustic emissions to endocochlear potential variation. J Acoust Soc Am 94:2108–2122.

    Article  CAS  PubMed  Google Scholar 

  • Mills JH, Schmiedt RA, Kulish LF (1990) Age-related changes in auditory potentials of Mongolian gerbil. Hear Res 46:201–210.

    Article  CAS  PubMed  Google Scholar 

  • Mills J, Schmiedt R, Schulte B, Dubno J (2006a) Age-related hearing loss: a loss of voltage, not hair cells. Semin Hear 27:228–236.

    Article  Google Scholar 

  • Mills JH, Schmiedt RA, Dubno JR. (2006b) Older and wiser, but losing hearing nonetheless. Hear Health Summer:12–17.

    Google Scholar 

  • Ohlemiller KK, Gagnon PM (2004) Apical-to-basal gradients in age-related cochlear degeneration and their relationship to “primary” loss of cochlear neurons. J Comp Neurol 479:103–116.

    Article  PubMed  Google Scholar 

  • Ohlemiller KK, Lett JM, Gagnon PM (2006) Cellular correlates of age-related endocochlear potential reduction in a mouse model. Hear Res 220:10–26.

    Article  PubMed  Google Scholar 

  • Ohlemiller KK, Rybak-Rice ME, Gagnon PM (2008) Strial microvasculature pathology and age-associated endocochlear potential decline in NOD cogenic mice. Hear Res 244:85–97.

    Article  CAS  PubMed  Google Scholar 

  • Probst R (1990) Otoacoustic emissions: an overview. Adv Otorhinolaryngol 44:1–91.

    CAS  PubMed  Google Scholar 

  • Roberson DW, Rubel EW (1994) Cell division in the gerbil cochlea after acoustic trauma. Am J Otol 15:28–34.

    CAS  PubMed  Google Scholar 

  • Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352.

    CAS  PubMed  Google Scholar 

  • Ruggero MA, Rich NC (1991) Furosemide alters organ of Corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane. J Neurosci 11:1057–1067.

    CAS  PubMed  Google Scholar 

  • Russell IJ (1983) Origin of the receptor potential in inner hair cells of the mammalian cochlea – evidence for Davis’s theory. Nature 301:334–336.

    Article  CAS  PubMed  Google Scholar 

  • Salt AN, Melichar I, Thalmann R (1987) Mechanisms of endocochlear potential generation by the stria vascularis. Laryngoscope 97:984–991.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA (1986) Acoustic distortion in the ear canal. I. Cubic difference tones: effects of acute noise injury. J Acoust Soc Am 79:1481–1490.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA (1989) Spontaneous rates, thresholds, and tuning of auditory nerve fibers in the gerbil: comparisons to cat data. Hear Res 42:23–36.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA (1993) Cochlear potentials in quiet-aged gerbils: does the aging cochlea need a jump start? In: Verrillo R (ed) Sensory Research: Multimodal Perspectives. Hillsdale, NJ: Lawrence Erlbaum and Associates, pp. 91–103.

    Google Scholar 

  • Schmiedt RA (1996) Effects of aging on potassium homeostasis and the endocochlear potential in the gerbil. Hear Res 102:125–132.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA, Zwislocki JJ (1977) Comparison of sound-transmission and cochlear-microphonic characteristics in Mongolian gerbil and guinea pig. J Acoust Soc Am 61:133–149.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA, Mills JH, Adams JC (1990) Tuning and suppression in auditory nerve fibers of aged gerbils raised in quiet or noise. Hear Res 45:221–236.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA, Mills JH, Boettcher FA (1996) Age-related loss of activity of auditory-nerve fibers. J Neurophysiol 76:2799–2803.

    CAS  PubMed  Google Scholar 

  • Schmiedt RA, Okamura H-O, Lang H, Schulte BA (2002a) Ouabain application to the round window of the gerbil cochlea: a model of auditory neuropathy and apoptosis. J Assoc Res Otolaryngol 3:223–233.

    Article  CAS  PubMed  Google Scholar 

  • Schmiedt RA, Lang H, Okamura H-O, Schulte BA (2002b) Effects of furosemide chronically applied to the round window: a model of metabolic presbyacusis. J Neurosci 22:9643–9650.

    CAS  PubMed  Google Scholar 

  • Schuknecht HF (1974) Presbyacusis. In: Pathology of the Ear. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Schuknecht HF, Gacek MR (1993) Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol 102:1–16.

    CAS  PubMed  Google Scholar 

  • Schuknecht HF, Woellner RC (1955) An experimental and clinical study of deafness from lesions of the auditory nerve. J Laryngol Otol 69:75–97.

    Article  CAS  PubMed  Google Scholar 

  • Schulte B (2007) Homeostasis of the inner ear. In: Dallos P (ed) The Senses. Vol. III. Audition. New York: Academic Press, pp. 149–156.

    Google Scholar 

  • Schulte BA, Schmiedt RA (1992) Lateral wall Na,K-ATPase and endocochlear potentials decline with age in quiet-reared gerbils. Hear Res 61:35–46.

    Article  CAS  PubMed  Google Scholar 

  • Sewell WF (1984). The effects of furosemide on the endocochlear potential and auditory-nerve fiber tuning curves in cats. Hear Res 14:305–314.

    Article  CAS  PubMed  Google Scholar 

  • Sha S-H, Kanicki A, Dootz G, Talaska AE, Halsey K, Dolan D, Altschuler R, Schacht J (2008) Age-related auditory pathology in the CBA/J mouse. Hear Res 243:87–94.

    Article  PubMed  Google Scholar 

  • Spicer S, Schulte B (1991) Differentiation of inner ear fibrocytes according to their ion transport related activity. Hear Res 56:53–64.

    Article  CAS  PubMed  Google Scholar 

  • Spicer S, Schulte B (1996) The fine structure of spiral ligament cells relates to ion return to the stria and varies with place-frequency. Hear Res 100:80–100.

    Article  CAS  PubMed  Google Scholar 

  • Spicer S, Gratton M, Schulte B (1997) Expression patterns of ion transport enzymes in spiral ligament fibrocytes change in relation to strial atrophy in the aged gerbil cochlea. Hear Res 111:93–102.

    Article  CAS  PubMed  Google Scholar 

  • Spongr VP, Flood DG, Frisina RD, Salvi RJ (1997) Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their life spans. J Acoust Soc Am 101:3546–3553.

    Article  CAS  PubMed  Google Scholar 

  • Stone JS, Cotanche DA (2007) Hair cell regeneration in the avian auditory epithelium. Int J Dev Biol 51:633–647.

    Article  CAS  PubMed  Google Scholar 

  • Suryadevara A, Schulte B, Schmiedt R, Slepecky N (2001) Auditory nerve fibers in young and aged gerbils: morphometric correlations with endocochlear potential. Hear Res 161:45–53.

    Article  CAS  PubMed  Google Scholar 

  • Tarnowski B, Schmiedt R, Hellstrom L, Lee F, Adams J (1991) Age-related changes in cochleas of Mongolian gerbils. Hear Res 54:123–134.

    Article  CAS  PubMed  Google Scholar 

  • Wangemann P (2002). K+ cycling and the endocochlear potential. Hear Res 165:1–9.

    Article  CAS  PubMed  Google Scholar 

  • Wangemann P, Liu J, Marcus D (1995) Ion transport mechanisms responsible for K+ secretion and the transepithelial voltage across marginal cells of stria vascularis in vitro. Hear Res 84:19–29.

    Article  CAS  PubMed  Google Scholar 

  • Willott JF (1991) Aging and the Auditory System: Anatomy, Physiology, and Psychophysics. San Diego, CA: Singular Publishing Group.

    Google Scholar 

  • Wu R, Hoshino T (1999) Changes in off-lesion endocochlear potential following localized lesion in the lateral wall. Acta Otolaryngol 119:550–554.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

I thank Judy Dubno, Hainan Lang, Jack Mills, Nancy Smythe, and Diana Vincent for their suggestions and encouragement. Studies reported here were supported by Grants R01 AG 14748 from the National Institute on Aging and P01 DC 00422 from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health.

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Schmiedt, R.A. (2010). The Physiology of Cochlear Presbycusis. In: Gordon-Salant, S., Frisina, R., Popper, A., Fay, R. (eds) The Aging Auditory System. Springer Handbook of Auditory Research, vol 34. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0993-0_2

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