Advertisement

The Physiology of Cochlear Presbycusis

  • Richard A. SchmiedtEmail author
Chapter
Part of the Springer Handbook of Auditory Research book series (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.

Keywords

Hair Cell Basilar Membrane Compound Action Potential Endocochlear Potential Hair Cell Loss 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

References

  1. Adams J (2008) Noise induced stress responses of the cochlear lateral wall. Abstr Assoc Res Otolaryngol 31:236.Google Scholar
  2. Adams J, McCaffery S, Kujawa SG (2007) Effects of acoustic trauma in the spiral ligament. Abstr Assoc Res Otolaryngol 30:243.Google Scholar
  3. Bhattacharyya TK, Dayal VS (1985) Age-related cochlear hair cell loss in the chinchilla. Ann Otol Rhinol Laryngol 94:75–80.PubMedGoogle Scholar
  4. Bhattacharyya TK, Dayal VS (1989) Influence of age on hair cell loss in the rabbit cochlea. Anat Rec 230:136–145.CrossRefGoogle Scholar
  5. 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
  6. 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
  7. Bredberg G (1968) Cellular pattern and nerve supply of the human organ of Corti. Acta Otolaryngol Suppl (Stockh) 236:1–135.Google Scholar
  8. 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.PubMedGoogle Scholar
  9. Davis H (1983) An active process in cochlear mechanics. Hear Res 9:79–90.CrossRefPubMedGoogle Scholar
  10. Dayal VS, Bhattacharyya TK (1989) Comparative study of age-related cochlear hair cell loss. Hear Res 15:179–183.Google Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.PubMedGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. Frisina RD, Walton JP (2006) Age-related structural and functional changes in the cochlear nucleus. Hear Res 217:216–233.CrossRefGoogle Scholar
  17. Gates GA, Mills JH (2005) Presbycusis. Lancet 366:1111–1120.CrossRefPubMedGoogle Scholar
  18. Gates GA, Cooper JC, Kannel WB, Miller NJ (1990) Hearing in the elderly: the Framingham cohort, 1983–1985. Ear Hear 11:247–256.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. Gruber J, Schaffer S, Halliwell B (2008) The mitochondrial free radical theory of ageing - where do we stand? Front Biosci 13:6554–6579.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. Hellstrom LI, Schmiedt RA (1990) Compound action potential input/output functions in young and quiet-aged gerbils. Hear Res 50:163–174.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. Henry KR (1982) Age-related auditory loss and genetics: an electrocochleographic comparison of six inbred strains of mice. J Gerontol 37:275–282.PubMedGoogle Scholar
  28. 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.PubMedGoogle Scholar
  29. Ichimiya I, Suzuki M, Mogi G (2000) Age-related changes in the murine cochlear lateral wall. Hear Res 139:116–122.CrossRefPubMedGoogle Scholar
  30. Jerger J, Chmiel R, Stach B, Spretjnak M (1993) Gender affects audiometric shape in presbyacusis. J Am Acad Audiol 4:42–49.PubMedGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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
  33. Kawase T, Liberman MC (1992) Spatial organization of the auditory nerve according to spontaneous discharge rate. J Comp Neurol 319:312–318.CrossRefPubMedGoogle Scholar
  34. Keithley EM, Feldman ML (1979) Spiral ganglion cell counts in an age-graded series of rat cochleas. J Comp Neurol 188:429–442.CrossRefPubMedGoogle Scholar
  35. Keithley EM, Feldman ML (1982) Hair cell counts in an age-graded series of rat cochleas. Hear Res 3:249–262.CrossRefGoogle Scholar
  36. Keithley EM, Ryan AF, Woolf NK (1989) Spiral ganglion cell density in young and old gerbils. Hear Res 38:125–134.CrossRefPubMedGoogle Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. Lee FS, Matthews LJ, Dubno JR, Mills JH (2005) Longitudinal study of pure-tone thresholds in older persons. Ear Hear 26:1–11.CrossRefPubMedGoogle Scholar
  44. Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455.CrossRefPubMedGoogle Scholar
  45. Marcus DC, Chiba T (1999) K+ and Na+ absorption by outer sulcus epithelial cells. Hear Res 134:48–56.CrossRefPubMedGoogle Scholar
  46. 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.PubMedGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar
  49. McFadden SL, Quaranta N, Henderson D (1997b) Suprathreshold measures of auditory function in the aging chinchilla. Hear Res 111:127–135.CrossRefPubMedGoogle Scholar
  50. Mills DM (2003) Differential responses to acoustic damage and furosemide in auditory brainstem and otoacoustic emission measures. J Acoust Soc Am 113:914–924.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefPubMedGoogle Scholar
  52. Mills DM, Rubel EW (1994) Variation of distortion product otoacoustic emissions with furosemide injection. Hear Res 77:183–199.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. Mills JH, Schmiedt RA, Kulish LF (1990) Age-related changes in auditory potentials of Mongolian gerbil. Hear Res 46:201–210.CrossRefPubMedGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. Mills JH, Schmiedt RA, Dubno JR. (2006b) Older and wiser, but losing hearing nonetheless. Hear Health Summer:12–17.Google Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. Ohlemiller KK, Lett JM, Gagnon PM (2006) Cellular correlates of age-related endocochlear potential reduction in a mouse model. Hear Res 220:10–26.CrossRefPubMedGoogle Scholar
  60. 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.CrossRefPubMedGoogle Scholar
  61. Probst R (1990) Otoacoustic emissions: an overview. Adv Otorhinolaryngol 44:1–91.PubMedGoogle Scholar
  62. Roberson DW, Rubel EW (1994) Cell division in the gerbil cochlea after acoustic trauma. Am J Otol 15:28–34.PubMedGoogle Scholar
  63. Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352.PubMedGoogle Scholar
  64. 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.PubMedGoogle Scholar
  65. 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.CrossRefPubMedGoogle Scholar
  66. Salt AN, Melichar I, Thalmann R (1987) Mechanisms of endocochlear potential generation by the stria vascularis. Laryngoscope 97:984–991.CrossRefPubMedGoogle Scholar
  67. 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.CrossRefPubMedGoogle Scholar
  68. Schmiedt RA (1989) Spontaneous rates, thresholds, and tuning of auditory nerve fibers in the gerbil: comparisons to cat data. Hear Res 42:23–36.CrossRefPubMedGoogle Scholar
  69. 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
  70. Schmiedt RA (1996) Effects of aging on potassium homeostasis and the endocochlear potential in the gerbil. Hear Res 102:125–132.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefPubMedGoogle Scholar
  72. 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.CrossRefPubMedGoogle Scholar
  73. Schmiedt RA, Mills JH, Boettcher FA (1996) Age-related loss of activity of auditory-nerve fibers. J Neurophysiol 76:2799–2803.PubMedGoogle Scholar
  74. 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.CrossRefPubMedGoogle Scholar
  75. 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.PubMedGoogle Scholar
  76. Schuknecht HF (1974) Presbyacusis. In: Pathology of the Ear. Cambridge, MA: Harvard University Press.Google Scholar
  77. Schuknecht HF, Gacek MR (1993) Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol 102:1–16.PubMedGoogle Scholar
  78. Schuknecht HF, Woellner RC (1955) An experimental and clinical study of deafness from lesions of the auditory nerve. J Laryngol Otol 69:75–97.CrossRefPubMedGoogle Scholar
  79. 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
  80. 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.CrossRefPubMedGoogle Scholar
  81. Sewell WF (1984). The effects of furosemide on the endocochlear potential and auditory-nerve fiber tuning curves in cats. Hear Res 14:305–314.CrossRefPubMedGoogle Scholar
  82. 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.CrossRefPubMedGoogle Scholar
  83. Spicer S, Schulte B (1991) Differentiation of inner ear fibrocytes according to their ion transport related activity. Hear Res 56:53–64.CrossRefPubMedGoogle Scholar
  84. 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.CrossRefPubMedGoogle Scholar
  85. 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.CrossRefPubMedGoogle Scholar
  86. 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.CrossRefPubMedGoogle Scholar
  87. Stone JS, Cotanche DA (2007) Hair cell regeneration in the avian auditory epithelium. Int J Dev Biol 51:633–647.CrossRefPubMedGoogle Scholar
  88. 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.CrossRefPubMedGoogle Scholar
  89. Tarnowski B, Schmiedt R, Hellstrom L, Lee F, Adams J (1991) Age-related changes in cochleas of Mongolian gerbils. Hear Res 54:123–134.CrossRefPubMedGoogle Scholar
  90. Wangemann P (2002). K+ cycling and the endocochlear potential. Hear Res 165:1–9.CrossRefPubMedGoogle Scholar
  91. 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.CrossRefPubMedGoogle Scholar
  92. Willott JF (1991) Aging and the Auditory System: Anatomy, Physiology, and Psychophysics. San Diego, CA: Singular Publishing Group.Google Scholar
  93. Wu R, Hoshino T (1999) Changes in off-lesion endocochlear potential following localized lesion in the lateral wall. Acta Otolaryngol 119:550–554.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Otolaryngology-Head and Neck SurgeryMedical University of South CarolinaCharlestonUSA

Personalised recommendations