Closing the Gap Between Neurobiology and Human Presbycusis: Behavioral and Evoked Potential Studies of Age-Related Hearing Loss in Animal Models and in Humans

  • James R. Ison
  • Kelly L. Tremblay
  • Paul D. Allen
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 34)


Any reader who has grown up with a pet dog cannot have failed to notice that the effects of advancing age in dogs are not very different from those apparent in aging grandparents, except that in calendar time they appear more rapidly. Although domesticated animals may present a special case compared with wild animals that hardly survive to the age of sexual maturity, a few wild animals do survive and they also exhibit these common effects of human aging. Very close to human sympathies are the observations of elderly chimpanzees by naturalists who, having followed their stable groups for many years, write that the rare creature that has successfully survived the challenges of the wild exhibits the same thinning hair, slow movements, and sagging and wrinkled facial skin as the elderly human (Hill et al. 2001). And given the laboratory studies of hearing in old monkeys (Bennett et al. 1983) and examinations of cochlear pathology in postmortem studies of aged pet dogs (Shimada et al. 1998), this wrinkled and slowly moving chimpanzee and the graying and arthritic dear old pet must both suffer from poor hearing as do elderly humans.


Hearing Loss Hair Cell Inferior Colliculus Absolute Threshold Endocochlear Potential 
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.



This work was supported in part by National Institutes of Health Grants DC 007705 from the National Institute on Deafness and Communication Disorders to KLT and AG 09524 from the Institute on Aging and DC 05409 from the Institute on Deafness and Communication Disorders to JRI and PDA.


  1. Allen PD, Eddins DA (2009) Cluster analysis reveals presbycusis phenotypes that group subjects by degree and configuration of hearing loss. Assoc Res Otolaryngol Abstr 32:140.Google Scholar
  2. Allen PD, Bell J, Dargani N, Moore CA, Tyler CM, Ison JR (2003) kvcn1 knockout mice have a profound deficit in discriminating sound source location. Soc Neurosci Abstr 29:183Google Scholar
  3. Barsz K, Ison JR, Snell KB, Walton JP (2002) Behavioral and neural measures of auditory temporal acuity in aging humans and mice. Neurobiol Aging 23:565–578.PubMedCrossRefGoogle Scholar
  4. Bennett CL, Davis RT, Miller JM (1983) Demonstration of presbycusis across repeated measures in a nonhuman primate species. Behav Neurosci 97:602–607.PubMedCrossRefGoogle Scholar
  5. Bergman M, Blumenfeld VG, Cascardo D, Dash B, Levitt H, Margulies MK (1976) Age-related decrement in hearing for speech. Sampling and longitudinal studies. J Gerontol 31:533–588.PubMedGoogle Scholar
  6. Bertoli S, Smurzynski J, Probst R (2002) Temporal resolution in young and elderly subjects as measured by mismatch negativity and a psychoacoustic gap detection task. Clin Neurophys 113:396–406.CrossRefGoogle Scholar
  7. Birch LM, Warfield D, Rubin RJ, Mikaelian DO (1968) Behavioral measurements of pure tone thresholds in normal CBA-J mice. J Aud Res 8:459–468.Google Scholar
  8. Boettcher FA (2002) Presbyacusis and the auditory brainstem response. J Speech Lang Hear Res 45:1249–1261.PubMedCrossRefGoogle Scholar
  9. Boettcher FA, Mills JH, Norton BL (1993) Age-related changes in auditory evoked potentials of gerbils. I. Response amplitudes. Hear Res 71:137–145.CrossRefGoogle Scholar
  10. Bohne BA, Gruner MM, Harding GW (1990) Morphological correlates of aging in the chinchilla cochlea. Hear Res 48:79–91.PubMedCrossRefGoogle Scholar
  11. Bowen GP, Taylor MK, Lin D, Ison JR (2003) Auditory cortex lesions impair both temporal acuity and intensity discrimination in the rat, suggesting a common mechanism for sensory processing. Cerebral Cort 13:815–822.CrossRefGoogle Scholar
  12. Brant LJ, Fozard JL (1990) Age changes in pure-tone hearing thresholds in a longitudinal study of normal human aging. J Acoust Soc Am 88:813–820.PubMedCrossRefGoogle Scholar
  13. Brown CH (1984) Directional hearing in aging rats. Exp Aging Res 10:35–38.PubMedGoogle Scholar
  14. Buchtel HA, Stewart JD (1989) Auditory agnosia: apperceptive or associative disorder? Brain Lang 37:12–25.PubMedCrossRefGoogle Scholar
  15. Burkard RF, Sims D (2001) The human auditory brainstem response to high click rates: aging effects. Am J Audiol 10:53–61.PubMedCrossRefGoogle Scholar
  16. Caine ED, Weingartner H, Ludlow CL, Cudahy EA, Wehry S (1981) Qualitative analysis of scopolamine-induced amnesia. Psychopharmacology 74:74–80.PubMedCrossRefGoogle Scholar
  17. Casey MA (1990) The effects of aging on neuron number in the rat superior olivary complex. Neurobiol Aging 11:391–394.PubMedCrossRefGoogle Scholar
  18. Casey MA, Feldman ML (1985) Aging in the rat medial nucleus of the trapezoid body. III. Alterations in capillaries. Neurobiol Aging 6:39–46.CrossRefGoogle Scholar
  19. Cody AR, Russell IJ (1987) The response of hair cells in the basal turn of the guinea-pig cochlea to tones. J Physiol 383:551–569.PubMedGoogle Scholar
  20. Dayal VS, Bhattacharyya TK (1986) Comparative study of age-related cochlear hair cell loss. Ann Otol Rhinol Laryngol 95:510–513.PubMedGoogle Scholar
  21. Di Girolamo S, Quaranta N, Picciotti P, Torsello A, Wolf F (2001) Age-related histopathological changes of the stria vascularis: an experimental model. Audiology 40:322–326.PubMedCrossRefGoogle Scholar
  22. Einsiedel LJ, Luff AR (1992) Alterations in the contractile properties of motor units within the ageing rat medial gastrocnemius. J Neurol Sci 112:170–177.PubMedCrossRefGoogle Scholar
  23. Erway LC, Willott JF, Archer JR, Harrison DE (1993) Genetics of age-related hearing loss in mice:I. Inbred and F1 hybrid strains. Hear Res 65:125–132PubMedCrossRefGoogle Scholar
  24. Fay RR (1988) Hearing in Vertebrates: A Psychophysics Database. Winnetka, IL: Hill-Fay Associates.Google Scholar
  25. Finlayson PG (2002) Paired-tone stimuli reveal reductions and alterations in temporal processing in inferior colliculus neurons of aged animals. J Assoc Res Otolaryngol 3:321–331.PubMedCrossRefGoogle Scholar
  26. Ford JM, Roth WT, Isaacks BG, White PM, Hood SH, Pfefferbaum A (1995) Elderly men and women are less responsive to startling noises: N1, P3 and blink evidence. Biol Psychol 39:57–80.PubMedCrossRefGoogle Scholar
  27. Gates GA, Couropmitree NN, Myers RH (1999) Genetic associations in age-related hearing thresholds. Arch Otolaryngol 125:654–659.Google Scholar
  28. Gelfand SA, Ross L, Miller S (1988) Sentence reception in noise from one versus two sources: effects of aging and hearing loss. J Acoust Soc Am 83:248–256.CrossRefGoogle Scholar
  29. Gleich O, Hamann I, Klump GM, Kittel M, Strutz J (2003) Boosting GABA improves impaired auditory temporal resolution in the gerbil. NeuroReport 14:1877–1880.PubMedCrossRefGoogle Scholar
  30. Gordon-Salant S, Fitzgibbons PJ (1995) Recognition of multiply degraded speech by young and elderly listeners. J Speech Hear Res 38:1150–1156.PubMedGoogle Scholar
  31. Gratton MA, Schulte BA (1995) Alterations in microvasculature are associated with atrophy of the stria vascularis in quiet-aged gerbils. Hear Res 82:44–52.PubMedCrossRefGoogle Scholar
  32. Guimaraes P, Zhu X, Cannon T, Kim S, Frisina RD (2004) Sex differences in distortion product otoacoustic emissions as a function of age in CBA mice. Hear Res 192:83–89.PubMedCrossRefGoogle Scholar
  33. Halling DC, Humes LE (2000) Factors affecting the recognition of reverberant speech by elderly listeners. J. Speech Lang. & Hear. Res. 43:414–431.Google Scholar
  34. Harris KC, Mills JH, He N-J, Dubno JR (2008) Age-related differences in sensitivity to small changes in frequency assessed with cortical evoked potentials. Hear Res 243:47–56.PubMedCrossRefGoogle Scholar
  35. Harrison J, Buchwald J (1982) Auditory brainstem responses in the aged cat. Neurobiol Aging 3:163–171.PubMedCrossRefGoogle Scholar
  36. Harrison JM, Irving R (1966) Visual and nonvisual auditory systems in mammals. Anatomical evidence indicates two kinds of auditory pathways and suggests two kinds of hearing in mammals. Science 154:738–743.PubMedCrossRefGoogle Scholar
  37. Hawkins JEJ, Miller JM, Rouse RC, Davis JA, Rarey K (1985) Inner ear histopathology in aging rhesus monkeys (Macaca mulatta). In: Davis RT, Leathers CW (eds) Behavior and Pathology of Aging in Rhesus Monkeys. New York: Alan R. Liss, pp. 137–154.Google Scholar
  38. He NJ, Mills JH, Dubno JR (2007) Frequency modulation detection: effects of age, psychophysical method, and modulation waveform. J Acoust Soc Am 122:467–477.PubMedCrossRefGoogle Scholar
  39. Heffner RS, Heffner HE (1988) Sound localization and use of binaural cues by the gerbil (Meriones unguiculatus). Beh Neurosci 102:422–428.CrossRefGoogle Scholar
  40. Heffner HE, Koay G, Heffner RS (2006) Behavioral assessment of hearing in mice - conditioned suppression. Curr Protoc Neurosci 8:Unit 8.21D.Google Scholar
  41. Heffner RS, Koay G, Heffner HE (2001) Sound-localization acuity changes with age in C57BL/6J mice. In: Willott JF (ed) Handbook of Mouse Auditory Research: From Behavior to Molecular Biology. New York: CRC Press, pp. 31–35.CrossRefGoogle Scholar
  42. Helfert RH, Sommer TJ, Meeks J, Hofstetter P, Hughes LF (1999) Age-related synaptic changes in the central nucleus of the inferior colliculus of Fischer-344 rats. J Comp Neurol 406:285–298.PubMedCrossRefGoogle Scholar
  43. Helfert RH, Krenning J, Wilson TS, Hughes LF (2003) Age-related synaptic changes in the anteroventral cochlear nucleus of Fischer-344 rats. Hear Res 183:18–28.PubMedCrossRefGoogle Scholar
  44. Hellstrom LI, Schmiedt RA (1991) Rate/level functions of auditory-nerve fibers in young and quiet-aged gerbils. Hear Res 53:217–222.PubMedCrossRefGoogle Scholar
  45. Henry KR (2004) 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 190:141–148.PubMedCrossRefGoogle Scholar
  46. Henry KR, McGinn M, Chole R (1980) Age-related auditory loss in the Mongolian gerbil. Arch Otorhinolaryngol 228:233–238.PubMedCrossRefGoogle Scholar
  47. Herman GE, Warren LR, Wagener JW (1977) Auditory lateralization: age differences in sensitivity to dichotic time and amplitude cues. J Gerontol 32:187–191.Google Scholar
  48. 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
  49. Hill K, Boesch C, Goodall J, Pusey A, Williams J, Wrangham R (2001) Mortality rates among wild chimpanzees. J Human Evol 40:437–450.CrossRefGoogle Scholar
  50. Hoffman HS, Ison JR (1992) Reflex modification and the analysis of sensory processing in developmental and comparative research. In: Campbell BA, Hayne H, Richardson R (eds) Attention and Information Processing in Infants and Adults: Perspectives from Human and Animal Research. Hillsdale, NJ: Lawrence Erlbaum Associates, pp. 83–111.Google Scholar
  51. Humes LE (2005) Do ‘auditory processing’ tests measure auditory processing in the elderly? Ear Hear 26:109–119.PubMedCrossRefGoogle Scholar
  52. Humes LE, Watson BU, Christensen LA, Cokely CG, Halling DC, Lee L. (1994) Factors associated with individual differences in clinical measures of speech recognition among the elderly. J Speech Hear Res 37:465–474.PubMedGoogle Scholar
  53. Hunter KP, Willott JF (1987) Aging and the auditory brainstem response in mice with severe or minimal presbycusis. Hear Res 30:207–218.PubMedCrossRefGoogle Scholar
  54. Ichimiya I, Suzuki M, Mogi G (2000) Age-related changes in the murine cochlear lateral wall. Hear Res 139:116–122.PubMedCrossRefGoogle Scholar
  55. Ingham NJ, Comis SD, Withington DJ (1999) Hair cell loss in the aged guinea pig cochlea. Acta Otolaryngol 119:42–47.PubMedGoogle Scholar
  56. Ison JR, Bowen GP (2000) Scopolamine reduces sensitivity to auditory gaps in the rat, suggesting a cholinergic contribution to temporal acuity. Hear Res 145:169–176.PubMedCrossRefGoogle Scholar
  57. Ison JR, Agrawal P (1998). The effect of spatial separation of signal and noise on masking in the free field as a function of signal frequency and age in the mouse. J Acoust Soc Am 104:1689–1695.PubMedCrossRefGoogle Scholar
  58. Ison JR, Agrawal P, Pak J, Vaughn WJ (1998) Changes in temporal acuity with age and with hearing impairment in the mouse: a study of the acoustic startle reflex and its inhibition by brief decrements in noise level. J Acoust Soc Am 104:1696 –1704.PubMedCrossRefGoogle Scholar
  59. Ison, JR, Allen, PD (2007) Pre- but not post-menopausal female CBA/CaJ mice show less prepulse inhibition than male mice of the same age. Behavioral Brain Res. 185:76–81.CrossRefGoogle Scholar
  60. Ison JR, Allen PD, Rivoli PJ, Moore JA (2005) The behavioral response of mice to gaps in noise depends on its spectral components and its bandwidth. J Acoust Soc Am 117:3944–3951.PubMedCrossRefGoogle Scholar
  61. Ison JR, Allen PD, O’Neill WE (2007) Age-related hearing loss in C57BL/6J mice has both frequency-specific and non-frequency-specific components that produce a hyperacusis-like exaggeration of the acoustic startle reflex. J Assoc Res Otolayngol 8:539–550.CrossRefGoogle Scholar
  62. Jerger J, Chmiel R, Stach B, Spretnjak M (1993) Gender affects audiometric shape in presbyacusis. J Am Acad Audiol 4:42–49.PubMedGoogle Scholar
  63. Jero J, Coling DE, Lalwani AK (2001) The use of Preyer’s reflex in evaluation of hearing in mice. Acta Otolaryngol 121:585–589.PubMedCrossRefGoogle Scholar
  64. Jewett DL, Romano MN, Williston JS (1970) Human auditory evoked potentials: possible brain stem components detected on the scalp. Science 167:1517–1518.PubMedCrossRefGoogle Scholar
  65. Jimenez AM, Stagner BB, Martin GK, Lonsbury-Martin BL (1999) Age-related loss of distortion product otoacoustic emissions in four mouse strains. Hear Res 138:91–105.PubMedCrossRefGoogle Scholar
  66. Johnsson LG, Hawkins JEJ (1972) Sensory and neural degeneration with aging, as seen in microdissections of the human inner ear. Ann Otol Rhinol Laryngol 81:179–193.PubMedGoogle Scholar
  67. Joris PX, Carney LH, Smith PH, Yin TC (1994) Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71:1022–1036.Google Scholar
  68. Kazee AM, Han LY, Spongr VP, Walton JP, Salvi RJ, Flood DG (1995) Synaptic loss in the central nucleus of the inferior colliculus correlates with sensorineural hearing loss in the C57BL/6 mouse model of presbycusis. Hear Res 89:109–120.PubMedCrossRefGoogle Scholar
  69. Keithley EM, Feldman ML (1982) Hair cell counts in an age-graded series of rat cochleas. Hear Res 8:249–262.PubMedCrossRefGoogle Scholar
  70. Kelly JB, Masterton B (1977) The auditory sensitivity of the albino rat. J Comp Physiol Psychol 91:930–936.PubMedCrossRefGoogle Scholar
  71. Kemp DT (1978) Stimulated acoustic emissions from within the human auditory system. J Acoust Soc Am 64:1386–1391.PubMedCrossRefGoogle Scholar
  72. Kopp-Scheinpflug C, Fuchs K, Lippe WR, Tempel BL, Rubsamen R (2003) Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J Neurosci 23:9199–9207.PubMedGoogle Scholar
  73. Krauter EE, Wallace JE, Campbell BA (1981) Sensory-motor function in the aging rat. Behav Neural Biol 31:367-392.PubMedCrossRefGoogle Scholar
  74. Kujawa SG, Liberman MC (2006) Acceleration of age-related hearing loss by early noise exposure: evidence of a misspent youth. J Neurosci 26:2115–2123.PubMedCrossRefGoogle Scholar
  75. Lang H, Schulte BA, Schmiedt RA (2002) Endocochlear potentials and compound action potential recovery: functions in the C57BL/6J mouse. Hear Res 172:118–126.PubMedCrossRefGoogle Scholar
  76. Lavoie BA, Mehta R, Thornton AR (2008) Linear and nonlinear changes in the auditory brainstem response of aging humans. Clin Neurophysiol 119:772–785.PubMedCrossRefGoogle Scholar
  77. Long GR (1994) Psychoacoustics. In: Fay RR, Popper AN (eds) Comparative Hearing: Mammals. New York: Springer-Verlag, pp. 18–56.Google Scholar
  78. Lutz J, Hemminger F, Stahl R, Dietrich O, Hempel M, Reiser M, Jager L (2007) Evidence of subcortical and cortical aging of the acoustic pathway: a diffusion tensor imaging (DTI) study. Acad Radiol 14:692–700.PubMedCrossRefGoogle Scholar
  79. May BJ, Kimar S, Prosen CA (2006) Auditory filter shapes of CBA/CaJ mice: behavioral assessments. J Acoust Soc Am 120:321–330.PubMedCrossRefGoogle Scholar
  80. McCullough BJ, Tempel BL (2004) Haplo-insufficiency revealed in deafwaddler mice when tested for hearing loss and ataxia. Hear Res 195:90–102.PubMedCrossRefGoogle Scholar
  81. McFadden SL, Willott JF (1994a) Responses of inferior colliculus neurons in C57BL/6J mice with and without sensorineural hearing loss: effects of changing the azimuthal location of an unmasked pure-tone stimulus. Hear Res 78:115–131.PubMedCrossRefGoogle Scholar
  82. McFadden SL, Willott JF (1994b) Responses of inferior colliculus neurons in C57BL/6J mice with and without sensorineural hearing loss: effects of changing the azimuthal location of a continuous noise masker on responses to contralateral tones. Hear Res 78:132–148.PubMedCrossRefGoogle Scholar
  83. McFadden SL, Campo P, Quaranta N, Henderson D (1997) Age-related decline of auditory function in the chinchilla (Chinchilla laniger). Hear Res 111:114–126.PubMedCrossRefGoogle Scholar
  84. Mendelson JR, Ricketts C (2001) Age-related temporal processing speed deterioration in auditory cortex. Hear Res 157:84–94.CrossRefGoogle Scholar
  85. Mikaelian DO, Warfield D, Norris BA (1974) Genetic progressive hearing loss in the C57/b16 mouse: relation of behavioral responses to cochlear pathology. Acta Otolaryngol 77:327–334.PubMedCrossRefGoogle Scholar
  86. Mills JH, Schmiedt RA, Kulish LF (1990) Age-related changes in auditory potentials of Mongolian gerbil. Hear Res 46:201–210.PubMedCrossRefGoogle Scholar
  87. Mrak RE, Griffin ST, Graham DI (1997) Aging-associated changes in human brain. J Neuropathol Exp Neurol 56:1269–1275.PubMedCrossRefGoogle Scholar
  88. Nabelek AK, Robinson PK (1982) Monaural and binaural speech perception in reverberation for listeners of various ages. J Acoust Soc Am 71:1242–1248.PubMedCrossRefGoogle Scholar
  89. Nelson EG, Hinojosa R (2006) Presbycusis: a human temporal bone study of individuals with downward sloping audiometric patterns of hearing loss and review of the literature. Laryngoscope 116:1–12.PubMedCrossRefGoogle Scholar
  90. Oeken J, Lenk A, Bootz F (2000) Influence of age and presbyacusis on DPOAE. Acta Otolaryngol 120:396–403.PubMedCrossRefGoogle Scholar
  91. Ohlemiller KK, Lett JM, Gagnon PM (2006) Cellular correlates of age-related endocochlear potential reduction in a mouse model. Hear Res 220:10–26.PubMedCrossRefGoogle Scholar
  92. Patterson RD, Nimmo-Smith I, Weber DL, Milroy R (1982) The deterioration of hearing with age: frequency selectivity, the critical ratio, the audiogram, and speech threshold. J Acoust Soc Am 72:1788–1803.PubMedCrossRefGoogle Scholar
  93. Pearson JD, Morrell CH, Gordon-Salant S, Brant LJ, Metter EJ, Klein LL, Fozard JL (1995) Gender differences in a longitudinal study of age-associated hearing loss. J Acoust Soc Am 97:1196–1205.PubMedCrossRefGoogle Scholar
  94. Pickles JO, Comis SD (1973) The role of centrifugal pathways to the cochlear nucleus and the detection of signals in noise. J Neurophysiol 36:1131–1137.PubMedGoogle Scholar
  95. Prosen CA, Moody DB (1991) Low-frequency detection and discrimination following apical hair cell destruction. Hear Res 57:142–152.PubMedCrossRefGoogle Scholar
  96. Rivoli P, Moore J, O’Neill W, Allen P, Ison J (2005) Colony-wide analysis of mouse auditory brainstem responses (II): maturational, gender and aging effects in C57BL/6J and CBA/CaJ mice. Assoc Res Otolaryngol Abstr 28:433.Google Scholar
  97. Roosa DBStJ (1885) Presbykousis. Trans Am Otol Soc 3:449–460.Google Scholar
  98. Ross B, Tremblay KL, Picton TW (2007) Aging in binaural hearing begins in mid-life: evidence from cortical auditory-evoked responses to changes in interaural phase. J Neurosci 27:11172–11178.PubMedCrossRefGoogle Scholar
  99. Ryan A (1976) Hearing sensitivity in the mongolian gerbil, Meriones unguiculatis. J Acoust Soc Am 59:1222–1228.PubMedCrossRefGoogle Scholar
  100. Schmiedt RA (1993) Cochlear potentials in quiet-aged gerbils: does the aging cochlea need a jump start? In: Verillo RT (ed) Sensory Research: Multimodel Perspectives Hillsdale, NJ: Erlbaum Associates, pp. 91–103.Google Scholar
  101. 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.PubMedCrossRefGoogle Scholar
  102. Shimada A, Ebisu M, Morita T, Takeuchi T, Umemura T (1998) Age-related changes in the cochlea and cochlear nuclei of dogs. J Vet Med Sci 60:41–48.PubMedCrossRefGoogle Scholar
  103. Snell KB (1997) Age-related changes in temporal gap detection. J Acoust Soc Am 101:2214–2220.PubMedCrossRefGoogle Scholar
  104. Snell KB, Ison JR, Frisina DR (1994) The effects of signal frequency and absolute bandwidth on gap detection in noise. J Acoust Soc Am 96:1458–1464.PubMedCrossRefGoogle Scholar
  105. 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.PubMedCrossRefGoogle Scholar
  106. Spruijt BM, van Hooff JA, Gispen WH (1992) Ethology and neurobiology of grooming behavior. Physiol Rev 72:825–852.PubMedGoogle Scholar
  107. Stebbins WC (1990) Perception in animal behavior. In: Berkley MA, Stebbins WC (eds) Comparative Perception New York: John Wiley & Sons, pp 1–26.Google Scholar
  108. Stenqvist M (2000) Age-related hearing changes and effects of exotoxin on inner ear function in aging rat. A frequency-specific auditory brainstem response study. ORL J Otorhinolaryngol Relat Spec 62:13–19.PubMedGoogle Scholar
  109. Tarnowski BI, Schmiedt RA, Hellstrom LI, Lee FS, Adams JC (1991) Age-related changes in cochleas of mongolian gerbils. Hear Res 54:123–134.PubMedCrossRefGoogle Scholar
  110. Torre P, Fowler CG (2000) Age-related changes in auditory function of rhesus monkeys (Macaca mulatta). Hear Res 142:131–140.PubMedCrossRefGoogle Scholar
  111. Tremblay KL, Burkard RF (2007) The aging auditory system: confounding effects of hearing loss on AEPs In: Burkard R, Don M, Eggermont JJ (eds) Auditory Evoked Potentials: Basic Principles and Clinic Application. Baltimore, MD: Lippincott Williams and Wilkins, pp. 403–425.Google Scholar
  112. Tremblay KL, Piskosz M, Souza P (2002) Aging alters the neural representation of speech cues. NeuroReport 13:1865–1870.PubMedCrossRefGoogle Scholar
  113. Tremblay KL, Piskosz M, Souza P (2003) Effects of age and age-related hearing loss on the neural representation of speech cues. Clin Neurophys 114:1332–1343.CrossRefGoogle Scholar
  114. Van Eyken E, Van Camp G, Van Laer L (2007) The complexity of age-related hearing impairment: Contributing environmental and genetic factors. Audiol. Neurotol. 12:345–358.CrossRefGoogle Scholar
  115. Vaughan DW (1977) Age-related deterioration of pyramidal cell basal dendrites in rat auditory cortex. J Comp Neurol 171:501–515.PubMedCrossRefGoogle Scholar
  116. Walton JP, Frisina RD, O’Neill WE (1998) Age-related alteration in processing of temporal sound features in the auditory midbrain of the CBA mouse. J Neurosci 18:2764–2776.PubMedGoogle Scholar
  117. Walton JP, Simon H, Frisina RD (2002) Age-related alterations in the neural coding of envelope periodicities. J Neurophysiol 88:565–578.PubMedGoogle Scholar
  118. Walton JP, Barsz K, Wilson WW (2008) Sensorineural hearing loss and neural correlates of temporal acuity in the inferior colliculus of the C57BL/6 mouse. J Assoc Res Otolaryngol 9:90–101.PubMedCrossRefGoogle Scholar
  119. Willott JF (1986) Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice. J Neurophysiol 56:391–408.PubMedGoogle Scholar
  120. Willott JF (1996) Auditory system plasticity in the adult C57BL/6J mouse. In: Salvi RJ, Henderson D, Fiorino F, Colletti V (eds) Auditory system Plasticity and Regeneration New York: Thieme Medical Publishers, Inc, pp. 297–316.Google Scholar
  121. Willott JF, Bross LS (1990) Morphology of the octopus cell area of the cochlear nucleus in young and aging C57BL/6J and CBA/J mice. J Comp Neurol 300:61–81.PubMedCrossRefGoogle Scholar
  122. Willott JF, Carlson S (1995) Modification of the acoustic startle response in hearing-impaired C57BL/6J mice: prepulse augmentation and prolongation of prepulse inhibition. Behav Neurosci 109: 396–403.PubMedCrossRefGoogle Scholar
  123. Willott JF, Jackson LM, Hunter KP (1987) Morphometric study of the anteroventral cochlear nucleus of two mouse models of presbycusis. J Comp Neurol 260: 472–480.PubMedCrossRefGoogle Scholar
  124. Willott JF, Aitkin LM, McFadden SL (1993) Plasticity of auditory cortex associated with sensorineural hearing loss in adult C57BL/6J mice. J Comp Neurol 329:402–411.PubMedCrossRefGoogle Scholar
  125. Yerkes RM (1905) The sense of hearing in frogs. J Comp Neurol Psychol 15:279–304.CrossRefGoogle Scholar
  126. Yerkes RM (1907) The Dancing Mouse. New York: The MacMillan Company.CrossRefGoogle Scholar
  127. Zettel ML, Zhu X, O’Neill WE, Frisina RD (2007) Age-related decline in Kv3.1b expression in the mouse auditory brainstem correlates with functional deficits in the medial olivocochlear efferent system. J Assoc Res Otolaryngol 8:280–293.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • James R. Ison
    • 1
  • Kelly L. Tremblay
    • 2
  • Paul D. Allen
    • 3
  1. 1.Department of Brain & Cognitive SciencesUniversity of RochesterRochesterUSA
  2. 2.Department of Speech & Hearing SciencesUniversity of WashingtonSeattleUSA
  3. 3.Department of Neurobiology & AnatomyUniversity of RochesterRochesterUSA

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