Morphological Correlates of Regeneration and Repair in the Inner Ear

  • Jason R. Meyers
  • Jeffrey T. Corwin
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 33)


Hair Cell Sensory Epithelium Hair Bundle Hair Cell Loss Acoustic Trauma 
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.


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  1. Adler HJ, Raphael Y (1996) New hair cells arise from supporting cell conversion in the acoustically damaged chick inner ear. Neurosci Lett 205:17–20.PubMedCrossRefGoogle Scholar
  2. Adler HJ, Komeda M, Raphael Y (1997) Further evidence for supporting cell conversion in the damaged avian basilar papilla. Int J Dev Neurosci 15:375–385.PubMedCrossRefGoogle Scholar
  3. Assad JA, Shepherd GM, Corey DP (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7:985–994.PubMedCrossRefGoogle Scholar
  4. Avallone B, Porritiello M, Esposito D, Mutone R, Balsamo G, Marmo F (2003) Evidence for hair cell regeneration in the crista ampullaris of the lizard Podarcis sicula. Hear Res 178:79–88.PubMedCrossRefGoogle Scholar
  5. Baird RA, Torres MA, Schuff NR (1993) Hair cell regeneration in the bullfrog vestibular otolith organs following aminoglycoside toxicity. Hear Res 65:164–174.PubMedCrossRefGoogle Scholar
  6. Baird RA, Burton MD, Fashena DS, Naeger RA (2000) Hair cell recovery in mitotically blocked cultures of the bullfrog saccule. Proc Natl Acad Sci USA 97:11722–11729.PubMedCrossRefGoogle Scholar
  7. Balak KJ, Corwin JT, Jones JE (1990) Regenerated hair cells can originate from supporting cell progeny: evidence from phototoxicity and laser ablation experiments in the lateral line system. J Neurosci 10:2502–2512.PubMedGoogle Scholar
  8. Berggren D, Liu W, Frenz D, Van De Water T (2003) Spontaneous hair-cell renewal following gentamicin exposure in postnatal rat utricular explants. Hear Res 180:114–125.PubMedCrossRefGoogle Scholar
  9. Bhave SA, Stone JS, Rubel EW, Coltrera MD (1995) Cell cycle progression in gentamicin-damaged avian cochleas. J Neurosci 15:4618–4628.PubMedGoogle Scholar
  10. Bhave SA, Oestele EC, Coltrera MD (1998) Macrophage and microglia-like cells in the avian inner ear. J Comp Neurol 398:241–256.PubMedCrossRefGoogle Scholar
  11. Bilak M, Kim J, Potashner SJ, Bohne BA, Morest DK (1997) New growth of axons in the cochlear nucleus of adult chinchillas after acoustic trauma. Exp Neurol 147:256–268.PubMedCrossRefGoogle Scholar
  12. Bohne BA, Harding GW (1992) Neural regeneration in the noise-damaged chinchilla cochlea. Laryngoscope 102:693–703.PubMedCrossRefGoogle Scholar
  13. Bredberg G (1968) Cellular pattern and nerve supply of the human organ of Corti. Acta Otolaryngol Suppl 236:1–135.Google Scholar
  14. Caveda L, Martin-Padura I, Navarro P, Breviario F, Corada M, Gulino D, Lampugnani MG, Dejana E (1996) Inhibition of cultured cell growth by vascular endothelial cadherin (cadherin-5/VE-cadherin). J Clin Invest 98:886–893.PubMedCrossRefGoogle Scholar
  15. Chardin S, Romand R (1995) Regeneration and mammalian auditory hair cells. Science 267:707–711.PubMedCrossRefGoogle Scholar
  16. Chardin S, Romand R (1997) Factors modulating supernumerary hair cell production in the postnatal rat cochlea in vitro. Int J Dev Neurosci 15:497–507.PubMedCrossRefGoogle Scholar
  17. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276:1425–1428.PubMedCrossRefGoogle Scholar
  18. Clark JA, Pickles JO (1996) The effects of moderate and low levels of acoustic over-stimulation on stereocilia and their tip links in the guinea pig. Hear Res 99:119–128.PubMedCrossRefGoogle Scholar
  19. Corwin JT (1981) Postembryonic production and aging in inner ear hair cells in sharks. J Comp Neurol 201:541–553.PubMedCrossRefGoogle Scholar
  20. Corwin JT (1983) Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity. J Comp Neurol 217:345–356.PubMedCrossRefGoogle Scholar
  21. Corwin JT (1985) Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc Natl Acad Sci USA 82:3911–3915.PubMedCrossRefGoogle Scholar
  22. Corwin JT, Cotanche DA (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772–1774.PubMedCrossRefGoogle Scholar
  23. Corwin JT, Jones JE, Katayama A, Kelley MW, Warchol ME (1991) Hair cell regeneration: the identities of progenitor cells, potential triggers and instructive cues. Ciba Found Symp 160:103–120; discussion 120–130.PubMedGoogle Scholar
  24. Cotanche DA (1987) Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear Res 30:181–195.PubMedCrossRefGoogle Scholar
  25. Cotanche DA, Dopyera CE (1990) Hair cell and supporting cell response to acoustic trauma in the chick cochlea. Hear Res 46:29–40.PubMedCrossRefGoogle Scholar
  26. Cotanche DA, Saunders JC, Tilney LG (1987) Hair cell damage produced by acoustic trauma in the chick cochlea. Hear Res 25:267–286.PubMedCrossRefGoogle Scholar
  27. Cotanche DA, Messana EP, Ofsie MS (1995) Migration of hyaline cells into the chick basilar papilla during severe noise damage. Hear Res 91:148–159.PubMedCrossRefGoogle Scholar
  28. Daudet N, Vago P, Ripoll C, Humbert G, Pujol R, Lenoir M (1998) Characterization of atypical cells in the juvenile rat organ of Corti after aminoglycoside ototoxicity. J Comp Neurol 401:145–162.PubMedCrossRefGoogle Scholar
  29. Daudet N, Ripoll C, Lenoir M (2002) Transforming growth factor-alpha-induced cellular changes in organotypic cultures of juvenile, amikacin-treated rat organ of corti. J Comp Neurol 442:6–22.PubMedCrossRefGoogle Scholar
  30. Davies D, Magnus C, Corwin JT (2007) Developmental changes in cell-extracellular matrix interactions limit proliferation in the mammalian inner ear. Eur J Neurosci 25:985–998.PubMedCrossRefGoogle Scholar
  31. Engstrom B, Flock A, Borg E (1983) Ultrastructural studies of stereocilia in noise-exposed rabbits. Hear Res 12:251–264.PubMedCrossRefGoogle Scholar
  32. Ernest S, Rauch GJ, Haffter P, Geisler R, Petit C, Nicolson T (2000) Mariner is defective in myosin VIIA: a zebrafish model for human hereditary deafness. Hum Mol Genet 9:2189–2196.PubMedCrossRefGoogle Scholar
  33. Fagotto F, Gumbiner BM (1996) Cell contact-dependent signaling. Dev Biol 180:445–454.PubMedCrossRefGoogle Scholar
  34. Fischer AJ, Reh TA (2000) Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev Biol 220:197–210.PubMedCrossRefGoogle Scholar
  35. Folkman J, Moscona A (1978) Role of cell shape in growth control. Nature 273:345–349.PubMedCrossRefGoogle Scholar
  36. Forge A (1985) Outer hair cell loss and supporting cell expansion following chronic gentamicin treatment. Hear Res 19:171–182.PubMedCrossRefGoogle Scholar
  37. Forge A, Li L, Corwin JT, Nevill G (1993) Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 259:1616–1619.PubMedCrossRefGoogle Scholar
  38. Forge A, Li L, Nevill G (1998) Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. J Comp Neurol 397:69–88.PubMedCrossRefGoogle Scholar
  39. Fredelius L (1988) Time sequence of degeneration pattern of the organ of Corti after acoustic overstimulation. A transmission electron microscopy study. Acta Otolaryngol 106:373–385.Google Scholar
  40. Fredelius L, Rask-Andersen H (1990) The role of macrophages in the disposal of degene-ration products within the organ of corti after acoustic overstimulation. Acta Otolaryngol 109:76–82.PubMedCrossRefGoogle Scholar
  41. Gailit J, Clark RA (1994) Wound repair in the context of extracellular matrix. Curr Opin Cell Biol 6:717–725.PubMedCrossRefGoogle Scholar
  42. Gale JE, Meyers JR, Periasamy A, Corwin JT (2002) Survival of bundleless hair cells and subsequent bundle replacement in the bullfrog’s saccule. J Neurobiol 50:81–92.PubMedCrossRefGoogle Scholar
  43. Geleoc GS, Holt JR (2003) Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat Neurosci 6:1019–1020.PubMedCrossRefGoogle Scholar
  44. Girod DA, Duckert LG, Rubel EW (1989) Possible precursors of regenerated hair cells in the avian cochlea following acoustic trauma. Hear Res 42:175–194.PubMedCrossRefGoogle Scholar
  45. Gu R, Marchionni M, Corwin JT (1996) Glial growth factor enhances supporting cell proliferation in rodent vestibular epithelia cultured in isolation. Soc Neurosci Abstr 21:520.Google Scholar
  46. Gu R, Marchionni M, Corwin JT (1997) Age-related decreases in proliferation within isolated mammalian vestibular epithelia cultured in control and glial growth factor 2 medium. Assoc Res Otolaryngol Abstr 20:98.Google Scholar
  47. Gu R, Montcouquiol M, Marchionni M, Corwin JT (2007) Proliferative responses to growth factors decline rapidly during postnatal maturation of mammalian hair cell epithelia. Eur J Neurosci 25:1363–1372.PubMedCrossRefGoogle Scholar
  48. Hashino E, Salvi RJ (1993) Changing spatial patterns of DNA replication in the noise-damaged chick cochlea. J Cell Sci 105 (Pt 1):23–31.Google Scholar
  49. Hennig AK, Cotanche DA (1998) Regeneration of cochlear efferent nerve terminals after gentamycin damage. J Neurosci 18:3282–3296.PubMedGoogle Scholar
  50. Hirose K, Discolo CM, Keasler JR, Ransohoff R (2005) Mononuclear phagocytes migrate into the murine cochlea after acoustic trauma. J Comp Neurol 489:180–194.PubMedCrossRefGoogle Scholar
  51. Huang S, Ingber DE (1999) The structural and mechanical complexity of cell-growth control. Nat Cell Biol 1:E131–138.PubMedCrossRefGoogle Scholar
  52. Hume CR, Kirkegaard M, Oesterle EC (2003) ErbB expression: the mouse inner ear and maturation of the mitogenic response to heregulin. J Assoc Res Otolaryngol 4:422–443.PubMedCrossRefGoogle Scholar
  53. Husbands JM, Steinberg SA, Kurian R, Saunders JC (1999) Tip-link integrity on chick tall hair cell stereocilia following intense sound exposure. Hear Res 135:135–145.PubMedCrossRefGoogle Scholar
  54. Itoh M, Chitnis AB (2001) Expression of proneural and neurogenic genes in the zebrafish lateral line primordium correlates with selection of hair cell fate in neuromasts. Mech Dev 102:263–266.PubMedCrossRefGoogle Scholar
  55. Izumikawa M, Minoda R, Kawamoto K, Abrashkin KA, Swiderski DL, Dolan DF, Brough DE, Raphael Y (2005) Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 11:271–276.PubMedCrossRefGoogle Scholar
  56. Johns PR (1977) Growth of the adult goldfish eye. III. Source of the new retinal cells. J Comp Neurol 176:343–357.PubMedCrossRefGoogle Scholar
  57. Johnston LA, Edgar BA (1998) Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394:82–84.PubMedCrossRefGoogle Scholar
  58. Jones JE, Corwin JT (1993) Replacement of lateral line sensory organs during tail regeneration in salamanders: identification of progenitor cells and analysis of leukocyte activity. J Neurosci 13:1022–1034.PubMedGoogle Scholar
  59. Jones JE, Corwin JT (1996) Regeneration of sensory cells after laser ablation in the lateral line system: hair cell lineage and macrophage behavior revealed by time-lapse video microscopy. J Neurosci 16:649–662.PubMedGoogle Scholar
  60. J⊝rgensen JM, Mathiesen C (1988) The avian inner ear. Continuous production of hair cells in vestibular sensory organs, but not in the auditory papilla. Naturwissenschaften 75:319–320.CrossRefGoogle Scholar
  61. J⊝rgensen JM, Flock Å (1976) Non-innervated sense organs of the lateral line: development in the regenerating tail of the salamander Ambystoma mexicanum. J Neurocytol 5:33–41.Google Scholar
  62. Kaltenbach JA, Falzarano PR (1994) Postnatal development of the hamster cochlea. I. Growth of hair cells and the organ of Corti. J Comp Neurol 340:87–97.PubMedCrossRefGoogle Scholar
  63. Kaltenbach JA, Falzarano PR, Simpson TH (1994) Postnatal development of the hamster cochlea. II. Growth and differentiation of stereocilia bundles. J Comp Neurol 350:187–198.PubMedCrossRefGoogle Scholar
  64. Katayama A, Corwin JT (1989) Cell production in the chicken cochlea. J Comp Neurol 281:129–135.PubMedCrossRefGoogle Scholar
  65. Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y (2003) Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 23:4395–4400.PubMedGoogle Scholar
  66. Kelley MW, Xu XM, Wagner MA, Warchol ME, Corwin JT (1993) The developing organ of Corti contains retinoic acid and forms supernumerary hair cells in response to exogenous retinoic acid in culture. Development 119:1041–1053.PubMedGoogle Scholar
  67. Kil J, Warchol ME, Corwin JT (1997) Cell death, cell proliferation, and estimates of hair cell life spans in the vestibular organs of chicks. Hear Res 114:117–126.PubMedCrossRefGoogle Scholar
  68. Kimura K, Usui-Ishihara A, Usui K (1997) G2 arrest of cell cycle ensures a determination process of sensory mother cell formation in g. Dev Genes Evol 207:199–202.CrossRefGoogle Scholar
  69. Kirkegaard M, J⊝rgensen JM (2001) The inner ear macular sensory epithelia of the Daubenton’s bat. J Comp Neurol 438:433–444.PubMedCrossRefGoogle Scholar
  70. Lambert PR, Gu R, Corwin JT (1997) Analysis of small hair bundles in the utricles of mature guinea pigs. Am J Otol 18:637–643.PubMedGoogle Scholar
  71. Lanford PJ, Presson JC, Popper AN (1996) Cell proliferation and hair cell addition in the ear of the goldfish, Carassius auratus. Hear Res 100:1–9.PubMedCrossRefGoogle Scholar
  72. Lawner BE, Harding GW, Bohne BA (1997) Time course of nerve-fiber regeneration in the noise-damaged mammalian cochlea. Int J Dev Neurosci 15:601–617.PubMedCrossRefGoogle Scholar
  73. Ledent V (2002) Postembryonic development of the posterior lateral line in zebrafish. Development 129:597–604.PubMedGoogle Scholar
  74. Lefebvre PP, Malgrange B, Staecker H, Moonen G, Van de Water TR (1993) Retinoic acid stimulates regeneration of mammalian auditory hair cells. Science 260:692–695.PubMedCrossRefGoogle Scholar
  75. Lefebvre PP, Malgrange B, Thiry M, Van De Water TR, Moonen G (2000) Epidermal growth factor upregulates production of supernumerary hair cells in neonatal rat organ of corti explants. Acta Otolaryngol 120:142–145.PubMedCrossRefGoogle Scholar
  76. Lenoir M, Vago P (1997) Does the organ of Corti attempt to differentiate new hair cells after antibiotic intoxication in rat pups? Int J Dev Neurosci 15:487–495.PubMedCrossRefGoogle Scholar
  77. Lewis ER, Li CW (1973) Evidence concerning the morphogenesis of saccular receptors in the bullfrog (Rana catesbeiana). J Morphol 139:351–361.PubMedCrossRefGoogle Scholar
  78. Li CW, Lewis ER (1979) Structure and development of vestibular hair cells in the larval bullfrog. Ann Otol Rhinol Laryngol 88:427–437.PubMedGoogle Scholar
  79. Li H, Liu H, Heller S (2003) Pluripotent stem cells from the adult mouse inner ear. Nat Med 9:1293–1299.PubMedCrossRefGoogle Scholar
  80. Li L, Forge A (1997) Morphological evidence for supporting cell to hair cell conversion in the mammalian utricular macula. Int J Dev Neurosci 15:433–446.PubMedCrossRefGoogle Scholar
  81. Li L, Nevill G, Forge A (1995) Two modes of hair cell loss from the vestibular sensory epithelia of the guinea pig inner ear. J Comp Neurol 355:405–417.PubMedCrossRefGoogle Scholar
  82. Lippe WR, Westbrook EW, Ryals BM (1991) Hair cell regeneration in the chicken cochlea following aminoglycoside toxicity. Hear Res 56:203–210.PubMedCrossRefGoogle Scholar
  83. Lombarte A, Popper AN (1994) Quantitative analyses of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the European hake, Merluccius merluccius (Gadiformes, Teleostei). J Comp Neurol 345:419–428.PubMedCrossRefGoogle Scholar
  84. Lombarte A, Yan HY, Popper AN, Chang JS, Platt C (1993) Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hear Res 64:166–174.PubMedCrossRefGoogle Scholar
  85. Marsh RR, Xu LR, Moy JP, Saunders JC (1990) Recovery of the basilar papilla following intense sound exposure in the chick. Hear Res 46:229–237.PubMedCrossRefGoogle Scholar
  86. Martin P (1997) Wound healing—aiming for perfect skin regeneration. Science 276:75–81.PubMedCrossRefGoogle Scholar
  87. Matsui JI, Oesterle EC, Stone JS, Rubel EW (2000) Characterization of damage and regeneration in cultured avian utricles. J Assoc Res Otolaryngol 1:46–63.PubMedCrossRefGoogle Scholar
  88. Matsui JI, Ogilvie JM, Warchol ME (2002) Inhibition of caspases prevents ototoxic and ongoing hair cell death. J Neurosci 22:1218–1227.PubMedGoogle Scholar
  89. Matsui JI, Haque A, Huss D, Messana EP, Alosi JA, Roberson DW, Cotanche DA, Dickman JD, Warchol ME (2003) Caspase inhibitors promote vestibular hair cell survival and function after aminoglycoside treatment in vivo. J Neurosci 23:6111–6122.PubMedGoogle Scholar
  90. Mbiene JP, Sans A (1986) Differentiation and maturation of the sensory hair bundles in the fetal and postnatal vestibular receptors of the mouse: a scanning electron microscopy study. J Comp Neurol 254:271–278.PubMedCrossRefGoogle Scholar
  91. Meyers JR, Corwin JT (2007) Shape change controls supporting cell proliferation in lesioned mammalian balance epithelium. J Neurosci 27:4313–4325.PubMedCrossRefGoogle Scholar
  92. Montcouquiol M, Corwin JT (2001a) Brief treatments with forskolin enhance s-phase entry in balance epithelia from the ears of rats. J Neurosci 21:974–982.Google Scholar
  93. Montcouquiol M, Corwin JT (2001b) Intracellular signals that control cell proliferation in mammalian balance epithelia: key roles for phosphatidylinositol-3 kinase, mammalian target of rapamycin, and S6 kinases in preference to calcium, protein kinase C, and mitogen-activated protein kinase. J Neurosci 21:570–580.Google Scholar
  94. Nakagawa T, Yamane H, Shibata S, Takayama M, Sunami K, Nakai Y (1997) Two modes of auditory hair cell loss following acoustic overstimulation in the avian inner ear. ORL J Otorhinolaryngol Relat Spec 59:303–310.PubMedGoogle Scholar
  95. Osborne MP, Comis SD (1990a) Action of elastase, collagenase and other enzymes upon linkages between stereocilia in the guinea-pig cochlea. Acta Otolaryngol 110:37–45.CrossRefGoogle Scholar
  96. Osborne MP, Comis SD (1990b) High resolution scanning electron microscopy of stereocilia in the cochlea of normal, postmortem, and drug-treated guinea pigs. J Electron Microsc Tech 15:245–260.CrossRefGoogle Scholar
  97. Paige GD (1992) Senescence of human visual-vestibular interactions. 1. Vestibulo-ocular reflex and adaptive plasticity with aging. J Vestib Res 2:133–151.PubMedGoogle Scholar
  98. Pickles JO, Comis SD, Osborne MP (1984) Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear Res 15:103–112.PubMedCrossRefGoogle Scholar
  99. Pickles JO, Comis SD, Osborne MP (1987a) The effect of chronic application of kanamycin on stereocilia and their tip links in hair cells of the guinea pig cochlea. Hear Res 29:237–244.CrossRefGoogle Scholar
  100. Pickles JO, Osborne MP, Comis SD (1987b) Vulnerability of tip links between stereocilia to acoustic trauma in the guinea pig. Hear Res 25:173–183.CrossRefGoogle Scholar
  101. Popper AN, Hoxter B (1984) Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hear Res 15:133–142.PubMedCrossRefGoogle Scholar
  102. Popper AN, Hoxter B (1990) Growth of a fish ear. II. Locations of newly proliferated sensory hair cells in the saccular epithelium of Astronotus ocellatus. Hear Res 45:33–40.PubMedCrossRefGoogle Scholar
  103. Presson JC, Popper AN (1990) Possible precursors to new hair cells, support cells, and Schwann cells in the ear of a post-embryonic fish. Hear Res 46:9–21.PubMedCrossRefGoogle Scholar
  104. Presson JC, Smith T, Mentz L (1995) Proliferating hair cell precursors in the ear of a postembryonic fish are replaced after elimination by cytosine arabinoside. J Neurobiol 26:579–584.PubMedCrossRefGoogle Scholar
  105. Presson JC, Lanford PJ, Popper AN (1996) Hair cell precursors are ultrastructurally indistinguishable from mature support cells in the ear of a postembryonic fish. Hear Res 100:10–20.PubMedCrossRefGoogle Scholar
  106. Puel JL, Pujol R, Tribillac F, Ladrech S, Eybalin M (1994) Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity. J Comp Neurol 341:241–256.PubMedCrossRefGoogle Scholar
  107. Raphael Y (1992) Evidence for supporting cell mitosis in response to acoustic trauma in the avian inner ear. J Neurocytol 21:663–671.PubMedCrossRefGoogle Scholar
  108. Ricci AJ, Kachar B, Gale J, Van Netten SM (2006) Mechano-electrical transduction: new insights into old ideas.J Membr Biol 209:71–88.PubMedCrossRefGoogle Scholar
  109. Roberson DF, Weisleder P, Bohrer PS, Rubel EW (1992) Ongoing production of sensory cells in the vestibular epithelium of the chick. Hear Res 57:166–174.PubMedCrossRefGoogle Scholar
  110. Roberson DW, Kreig CS, Rubel EW (1996) Light microscopic evidence that direct transdifferentiation gives rise to new hair cells in regenerating avian auditory epithelium. Audit Neurosci 2:195–205.Google Scholar
  111. Roberson DW, Alosi JA, Cotanche DA (2004) Direct transdifferentiation gives rise to the earliest new hair cells in regenerating avian auditory epithelium. J Neurosci Res 78:461–471PubMedCrossRefGoogle Scholar
  112. Romand R, Chardin S, Le Calvez S (1996) The spontaneous appearance of hair cell-like cells in the mammalian cochlea following aminoglycoside ototoxicity. NeuroReport 8:133–137.PubMedCrossRefGoogle Scholar
  113. Rosenhall U (1972) Vestibular macular mapping in man. Ann Otol Rhinol Laryngol 81:339–351.PubMedGoogle Scholar
  114. Rosenhall U (1973) Degenerative patterns in the aging human vestibular neuro-epithelia. Acta Otolaryngol 76:208–220.PubMedCrossRefGoogle Scholar
  115. Ruben RJ (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol:Suppl 220:221–244.Google Scholar
  116. Ryals BM, Rubel EW (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774–1776.PubMedCrossRefGoogle Scholar
  117. Ryals BM, Westbrook EW (1990) Hair cell regeneration in senescent quail. Hear Res 50:87–96.PubMedCrossRefGoogle Scholar
  118. Ryals BM, Westbrook EW (1994) TEM analysis of neural terminals on autoradiographically identified regenerated hair cells. Hear Res 72:81–88.PubMedCrossRefGoogle Scholar
  119. Sage C, Huang M, Karimi K, Gutierrez G, Vollrath MA, Zhang DS, Garcia-Anoveros J, Hinds PW, Corwin JT, Corey DP, Chen ZY (2005) Proliferation of functional hair cells in vivo in the absence of the retinoblastoma protein. Science 307:1114–1118.PubMedCrossRefGoogle Scholar
  120. Sans A, Chat M (1982) Analysis of temporal and spatial patterns of rat vestibular hair cell differentiation by tritiated thymidine radioautography. J Comp Neurol 206:1–8.PubMedCrossRefGoogle Scholar
  121. Schneider ME, Belyantseva IA, Azevedo RB, Kachar B (2002) Rapid renewal of auditory hair bundles. Nature 418:837–838.PubMedCrossRefGoogle Scholar
  122. Shou J, Zheng JL, Gao WQ (2003) Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol Cell Neurosci 23:169–179.PubMedCrossRefGoogle Scholar
  123. Sobkowicz HM, Slapnick SM, August BK (1995) The kinocilium of auditory hair cells and evidence for its morphogenetic role during the regeneration of stereocilia and cuticular plates. J Neurocytol 24:633–653.PubMedCrossRefGoogle Scholar
  124. Song J, Yan HY, Popper AN (1995) Damage and recovery of hair cells in fish canal (but not superficial) neuromasts after gentamicin exposure. Hear Res 91:63–71.PubMedCrossRefGoogle Scholar
  125. Speidel C (1947) Correlated studies of sense organs and nerves of the lateral-line in living frog tadpoles I. Regeneration of denervated organs. J Comp Neurol 87:27–55.CrossRefGoogle Scholar
  126. Steyger PS, Burton M, Hawkins JR, Schuff NR, Baird RA (1997) Calbindin and parvalbumin are early markers of non-mitotically regenerating hair cells in the bullfrog vestibular otolith organs. Int J Dev Neurosci 15:417–432.PubMedCrossRefGoogle Scholar
  127. Stone JS, Cotanche DA (1994) Identification of the timing of S phase and the patterns of cell proliferation during hair cell regeneration in the chick cochlea. J Comp Neurol 341:50–67.PubMedCrossRefGoogle Scholar
  128. Stone LS (1933) The development of lateral-line sense organs in amphibians observed in living and vital-stained preparations. J Comp Neurol 57:507–540.CrossRefGoogle Scholar
  129. Stone LS (1937) Further experimental studies of the development of lateral-line sense organs in amphibians observed in living preparations. J Comp Neurol 68:83–115.CrossRefGoogle Scholar
  130. Straznicky K, Gaze RM (1971) The growth of the retina in Xenopus laevis: an autoradiographic study. J Embryol Exp Morphol 26:67–79.PubMedGoogle Scholar
  131. Strominger RN, Bohne BA, Harding GW (1995) Regenerated nerve fibers in the noise-damaged chinchilla cochlea are not efferent. Hear Res 92:52–62.PubMedCrossRefGoogle Scholar
  132. Sun H, Salvi RJ, Ding DL, Hashino DE, Shero M, Zheng XY (2000) Excitotoxic effect of kainic acid on chicken otoacoustic emissions and cochlear potentials. J Acoust Soc Am 107:2136–2142.PubMedCrossRefGoogle Scholar
  133. Sun H, Hashino E, Ding DL, Salvi RJ (2001) Reversible and irreversible damage to cochlear afferent neurons by kainic acid excitotoxicity. J Comp Neurol 430:172–181.PubMedCrossRefGoogle Scholar
  134. Tanaka EM, Gann AA, Gates PB, Brockes JP (1997) Newt myotubes reenter the cell cycle by phosphorylation of the retinoblastoma protein. J Cell Biol 136:155–165.PubMedCrossRefGoogle Scholar
  135. Taylor RR, Forge A (2005) Hair cell regeneration in sensory epithelia from the inner ear of a urodele amphibian. J Comp Neurol 484:105–120.PubMedCrossRefGoogle Scholar
  136. Tilney LG, Tilney MS, Saunders JS, DeRosier DJ (1986) Actin filaments, stereocilia, and hair cells of the bird cochlea. III. The development and differentiation of hair cells and stereocilia. Dev Biol 116:100–118.PubMedCrossRefGoogle Scholar
  137. Wang Y, Raphael Y (1996) Re-innervation patterns of chick auditory sensory epithelium after acoustic overstimulation. Hear Res 97:11–18.PubMedCrossRefGoogle Scholar
  138. Wang Z, Li H (2000) Microglia-like cells in rat organ of Corti following aminoglycoside ototoxicity. NeuroReport 11:1389–1393.PubMedCrossRefGoogle Scholar
  139. Warchol ME (1995) Supporting cells in isolated sensory epithelia of avian utricles proliferate in serum-free culture. NeuroReport 6:981–984.PubMedCrossRefGoogle Scholar
  140. Warchol ME (1997) Macrophage activity in organ cultures of the avian cochlea: demonstration of a resident population and recruitment to sites of hair cell lesions. J Neurobiol 33:724–734.PubMedCrossRefGoogle Scholar
  141. Warchol ME (1999) Immune cytokines and dexamethasone influence sensory regeneration in the avian vestibular periphery. J Neurocytol 28:889–900.PubMedCrossRefGoogle Scholar
  142. Warchol ME (2002) Cell density and N-cadherin interactions regulate cell proliferation in the sensory epithelia of the inner ear. J Neurosci 22:2607–2616.PubMedGoogle Scholar
  143. Warchol ME, Corwin JT (1996) Regenerative proliferation in organ cultures of the avian cochlea: identification of the initial progenitors and determination of the latency of the proliferative response. J Neurosci 16:5466–5477.PubMedGoogle Scholar
  144. Warchol ME, Lambert PR, Goldstein BJ, Forge A, Corwin JT (1993) Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science 259:1619–1622.PubMedCrossRefGoogle Scholar
  145. Weisleder P, Rubel EW (1993) Hair cell regeneration after streptomycin toxicity in the avian vestibular epithelium. J Comp Neurol 331:97–110.PubMedCrossRefGoogle Scholar
  146. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239:1142–1145.PubMedCrossRefGoogle Scholar
  147. Witte MC, Montcouquiol M, Corwin JT (2001) Regeneration in avian hair cell epithelia: identification of intracellular signals required for S-phase entry. Eur J Neurosci 14:829–838.PubMedCrossRefGoogle Scholar
  148. Wright A, Davis A, Bredberg G, Ulehlova L, Spencer H (1987) Hair cell distributions in the normal human cochlea. Acta Otolaryngol Suppl 444:1–48.PubMedGoogle Scholar
  149. Wright M (1947) Regeneration and degeneration experiments on lateral line nerves and sense organs in anurans. J Exp Zool 105:221–257.CrossRefPubMedGoogle Scholar
  150. Zakir M, Dickman JD (2006) Regeneration of vestibular otolith afferents after ototoxic damage. J Neurosci 26:2881–2893.PubMedCrossRefGoogle Scholar
  151. Zhao Y, Yamoah EN, Gillespie PG (1996) Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proc Natl Acad Sci USA 93:15469–15474.PubMedCrossRefGoogle Scholar
  152. Zheng JL, Gao WQ (2000) Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3:580–586.PubMedCrossRefGoogle Scholar
  153. Zheng JL, Keller G, Gao WQ (1999) Immunocytochemical and morphological evidence for intracellular self-repair as an important contributor to mammalian hair cell recovery. J Neurosci 19:2161–2170.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Jason R. Meyers
  • Jeffrey T. Corwin

There are no affiliations available

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