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Discharge patterns of chicken cochlear ganglion neurons following kanamycin-induced hair cell loss and regeneration

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Abstract

Hair cells in the basal, high frequency region (>1100 Hz) of the chicken cochlea were destroyed with kanamycin (400 mg/kg/d × 10 d) and allowed to regenerate. Afterwards, single unit recordings were made from cochlear ganglion neurons at various times post-treatment. During the first few weeks post-treatment, only neurons with low characteristic frequencies (<1100 Hz) responded to sound. Despite the fact that the low frequency region of the cochlea was not destroyed, neurons with low characteristic frequencies had elevated thresholds, abnormally broad U-shaped or W-shaped tuning curves and low spontaneous discharge rates. At 2 days post-treatment, the spontaneous discharge rates of some acoustically unresponsive units fluctuated in a rhythmical manner. As recovery time increased, thresholds decreased, tuning curves narrowed and developed a symmetrical V-shape, spontaneous rate increased and neurons with higher characteristic frequencies began to respond to sound. In addition, the proportion of interspike interval histograms with regularly spaced peaks increased. These improvements progressed along a low-to-high characteristic frequency gradient. By 10–20 weeks post-treatment, the thresholds and tuning curves of neurons with characteristic frequencies below 2000 Hz were within normal limits; however, the spontaneous discharge rates of the neurons were still significantly lower than those from normal animals.

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Abbreviations

KM:

kanamycin

BrdU:

bromodeoxyuridine

CF:

characteristic frequency

CAP:

compound action potential

ISI:

interspike interval

References

  • Aran J-M, Hiel H, Hayashida T, Erre J-P, Aurousseau C, Guilahaume A, Dulon D (1992a) Noise, aminoglycosides and diuretics. In: Dancer A, Henderson D, Salvi RJ, Hamernik RP (eds) Effects of noise on the auditory system. Mosby Year Book, St. Louis, pp 188–195

    Google Scholar 

  • Aran JM, Dulon D, Hiel H, Aurousseau CA, Erre J-P (1992b) Persistence of gentamicin in cochlear sensory and supporting cells. Symposium: The molecular biology of hearing and deafness. La Jolla, CA, May 1–4

  • Chen L, Salvi RJ, Hashino E (1993) Recovery of CAP threshold and amplitude in adult chickens following kanamycin ototoxicity. Hearing Res 69:15–24

    Google Scholar 

  • Corwin JT, Cotanche DA (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240:1772–1774

    Google Scholar 

  • Cotanche DA (1987a) Regeneration of hair cell stereocilliary bunles in the chick cochlea following severe acoustic trauma. Hearing Res 30:181–196

    Google Scholar 

  • Cotanche DA (1987b) Regeneration of the tectorial membrane in the chick cochlea following severe acoustic trauma. Hearing Res 30:197–206

    Google Scholar 

  • Cotanche DA, Saunders JC, Tilney LG (1987) Hair cell damage produced by acoustic trauma in the chick cochlea. Hearing Res 25:267–286

    Google Scholar 

  • Cruz R, Lambert P, Rubel EW (1987) Light microscopic evidence of hair cell regeneration after gentamicin toxicity in chick cochlea. Arch Otolaryngol Head Neck Surg 113:1058–1062

    Google Scholar 

  • Dretchen KL, Sokol MD, Gergis SD, Long JP (1973) Relative effects of streptomycin on motor nerve terminal and endplate. Eur J Pharmacol 22:10–16

    Google Scholar 

  • Duckert LG, Rubel EW (1990) Ultrastructural observations on regenerating hair cells in the chick basilar papilla. Hearing Res 48:1058–1062

    Google Scholar 

  • Duckert LG, Rubel EW (1993) Morphological correlates of functional recovery in the chicken inner ear after gentamycin treatment. J Comp Neurol 331:75–96

    Google Scholar 

  • Dulon D, Zajic G, Aran J-M, Schacht J (1989) Aminoglycoside antibiotics impair calcium entry but not viability and motility in isolated cochlear outer hair cells. J Neurosci Res 24:338–346

    Google Scholar 

  • Forge A, Fradis M (1985) Structural abnormalities in the stria vascularis following chronic gentamicin treatment. Hearing Res 20:233–244

    Google Scholar 

  • Fuchs PA, Sokolowski BHA (1990) The acquisition during development of Ca-activated potassium currents by cochlear hair cells of the chick. Proc R Soc Lond B 241:122–126

    Google Scholar 

  • Fuchs PA, Nagai T, Evans MG (1988) Electrical tuning in hair cells isolated from the chick cochlea. J Neurosci 8:2460–2467

    Google Scholar 

  • Gratzner HG (1982) Monoclonal antibody to 5-bromoand 5-iodo-deoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475

    Google Scholar 

  • Gummer AW, Smolders JWT, Klinke R (1987) Basilar membrane motion in the pigeon measured with the Mössbauer technique. Hearing Res 29:63–92

    Google Scholar 

  • Hashino E, Salvi RJ (1993) Changing spatial patterns of DNA replication in the noise damaged chick cochlea. J Cell Sci 105:23–31

    Google Scholar 

  • Hashino E, Sokabe M (1989) Kanamycin induced low-frequency hearing loss in the budgerigar (Melopsittacus undulatus). J Acoust Soc Am 85:289–294

    Google Scholar 

  • Hashino E, Sokabe M, Tanaka Y (1988) Frequency specific suscepibility to acoustic trauma in budgerigar (Melopsittacus undulatus). J Acoust Soc Am 83:2450–2453

    Google Scholar 

  • Hashino E, Tanaka Y, Sokabe M (1991) Hair cell damage and recovery following chronic application of kanamycin in the chick cochlea. Hearing Res 52:356–368

    Google Scholar 

  • Hashino E, Sokabe, M, Tanaka Y (1992a) Function-structure correlation during recovery from aminoglycoside ototoxicity in avian auditory system. In: Dancer A, Henderson D, Salvi RJ, Hamernik RP (eds) Effects of noise on the auditory system. Mosby Year Book, St. Louis, pp 238–246

    Google Scholar 

  • Hashino E, Tanaka Y, Salvi RJ, Sokabe M (1992b) Hair cell regeneration in the adult budgerigar after kanamycin ototoxicity. Hearing Res 59:46–58

    Google Scholar 

  • Inoue T, Osatake H, Takahashi H (1989) A new freeze-drying instrument using t-butyl alcohol for scanning electron microscopy. J Electron Microsc 38:319–320

    Google Scholar 

  • Johnsson LG, Hawkins Jr JE (1972) Striai atrophy in clinical and experimental deafness. Laryngoscope 82:1105–1125

    Google Scholar 

  • Kiang NYS, Liberman MC, Levine RA (1976) Auditory-nerve activity in cats exposed to ototoxic drugs and high-intensity sounds. Ann Otol Rhinol Laryngol 85:752–768

    Google Scholar 

  • Kössl M, Richardson GP, Russell IJ (1989) Stereocilia bundle stiffness: Effects of neomycin sulfate, A21387 and Concanavalin A. Hearing Res 44:217–230

    Google Scholar 

  • Kroese A, Van den Bercken J (1982) Effects of ototoxic antibiotics on sensory cell functioning. Hearing Res 6:183–197

    Google Scholar 

  • Kroese ABA, Das A, Hudspeth AJ (1989) Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics. Hearing Res 37:203–218

    Google Scholar 

  • Liberman MC, Kiang NYS (1978) Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. Acta Otolaryngol Suppl 358:1–63

    Google Scholar 

  • Liberman MC, Dodds LW, Learson DA (1986) Structure-function correlation in noise-damaged ears: A light and electron microscopic study. In: Salvi RJ, Henderson D, Hamernik RP, Colletti V (eds) Basic and applied aspects of noise-induced hearing loss. Plenum Press, New York, pp 163–177

    Google Scholar 

  • Lippe W, Rubel EW (1985) Ontogeny of tonotopic organization of brain stem auditory nuclei in the chicken: Implication for the development of the place principle. J Comp Neurol 237:273–289

    Google Scholar 

  • Manley GA, Brix J, Kaiser A (1987) Developmental stability of the tonotopic organization of the chick's basilar papilla. Science 237:655–666

    Google Scholar 

  • Manley GA, Gleich O, Kaiser A, Brix J (1989) Functional differentiation of sensory cells in the avian auditory periphery. J Comp Physiol A 164:289–296

    Google Scholar 

  • Manley GA, Kaiser A, Brix J, Gleich O (1991) Activity patterns of primary auditory-nerve fibres in chickens: Development of fundamental properties. Hearing Res 57:1–15

    Google Scholar 

  • McFadden EA, Saunders JC (1989) Recovery of auditory function following intense sound exposure in the neonatal chick. Hearing Res 41:205–216

    Google Scholar 

  • Norton SJ, Rubel EW (1990) Active and passive ADP components in mammalian and avian ears. In: Geisler D, Dallos P, Mathews J, Ruggero M (eds) Mechanics and biophysics of hearing. Springer, Berlin Heidelberg New York, pp 219–226

    Google Scholar 

  • Norton S, Tucci D, Rubel EW (1990) Comparison of acoustic and neural responses from avian ears following gentamicin. Abstr Assoc Res Otolaryngol 73:62

    Google Scholar 

  • Pittinger C, Adamson R (1972) Antibiotic blockade of neuromuscular function. Annu Rev Pharmacol 12:169–184

    Google Scholar 

  • Raphael Y (1991) Pure-tone overstimulation protects surviving avian hair cells from acoustic trauma. Hearing Res 53:173–184

    Google Scholar 

  • Romand R (1979) Development of auditory nerve activity in kittens. Brain Res 173:554–556

    Google Scholar 

  • Rubel EW (1992) Regeneration of hair cells in the avian inner ear. In: Dancer A, Henderson D, Salvi RJ, Hamernik RP (eds) Effects of noise on the auditory system. Mosby Year Book, St. Louis, pp 204–227

    Google Scholar 

  • Rubel EW, Lippe WR, Ryals BM (1984) Development of the place principle. Ann Oto Rhinol Laryngol 93:609–615

    Google Scholar 

  • Ryals BM, Rubel EW (1982) Pattern of hair cell loss in chick basilar papilla after intense auditory stimulation. Exposure duration and survival time. Acta Otolaryngol 92:31–41

    Google Scholar 

  • Ryals BM, Rubel EW (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240:1774–1776

    Google Scholar 

  • Ryals BM, Ten Eyck B, Westbrook EW (1990) Ganglion cell loss continues during hair cell regeneration. Hearing Res 43:81–90

    Google Scholar 

  • Ryals BM, Stalford MD, Becker DG, Lambert PR (1993) Ultrastructural changes in the tegmentum vasculosum parallel changes in auditory function after acoustic trauma. Abstr Assoc Res Otolaryngol 171:43

    Google Scholar 

  • Salvi RJ, Perry J, Hamernik RP, Henderson D (1982) Relationships between cochlear pathologies and auditory nerve and behavioral responses following acoustic trauma. In: Hamernik RP, Henderson D, Salvi RJ (eds) New perspectives on noise-induced hearing loss. Raven Press, New York, pp 165–188

    Google Scholar 

  • Salvi RJ, Hamernik RP, Henderson D (1983) Response patterns of auditory nerve fibers during temporary threshold shift. Hearing Res 10:37–67

    Google Scholar 

  • Salvi RJ, Saunders SS, Powers NL, Boettcher FA (1992) Discharge patterns of cochlear ganglion neurons in the chicken. J Comp Physiol A 170:227–241

    Google Scholar 

  • Saunders JC, Tilney LG (1982) Species differences in susceptibility to noise induced hearing loss. In: Hamernik RP, Henderson D, Salvi RJ (eds) New perspectives on noise-induced hearing loss. Raven Press, New York, pp 229–248

    Google Scholar 

  • Schacht J (1986) Molecular mechanisms of drug-induced hearing loss. Hearing Res 22:297–304

    Google Scholar 

  • Schacht J, Weiner N (1986) Aminoglycoside-induced hearing loss: A molecular hypothesis. ORL — J Oto-Rhino-Laryngol 48:116–123

    Google Scholar 

  • Schmidt RS, Fernandez C (1962) Labyrinth D.C. potentials in repesentative vertebrates. J Cell Comp Physiol 9:311–322

    Google Scholar 

  • Sewell WF (1984a) The relation between the endocochlear potential and spontaneous activity in auditory nerve fibers in the cat. J Physiol (Lond) 347:685–696

    Google Scholar 

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

    Google Scholar 

  • Tran Ba Huy P, Bernard P, Schacht J (1986) Kinetics of gentamicin uptake and release in the rat. Comparison of inner ear tissues and fluids with other organs. J Clin Invest 77:1492–1500

    Google Scholar 

  • Tucci DL, Rubel EW (1990) Physiologic status of regenerated hair cells in the avian inner ear following aminoglycoside ototoxicity. Otolaryngol Head Neck Surg 103:443–450

    Google Scholar 

  • Von Düring M, Andres KH, Simon K (1985) The comparative anatomy of the basilar papillae in birds. Fortschr Zool 30:681–685

    Google Scholar 

  • Vossieck T, Klinke R (1990) A method for changing the avian endocochlear potential by current injection. Eur Arch Otolaryngol 248:11–14

    Google Scholar 

  • Wersäll J, Bjorkroth B, Flock Å, Lundquist PG (1973) Experiments on ototoxic effects of antibiotics. Adv Oto-Rhino-Laryngol 20:14–41

    Google Scholar 

  • Woolf NK, Ryan AF (1985) Ontogeny of neural discharge patterns in the ventral cochlear nucleus of the Mongolian gerbil. Dev Brain Res 17:131–147

    Google Scholar 

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Authors and Affiliations

  1. Hearing Research Laboratory, Department of Communicative Disorders & Sciences, 215 Parker Hall, State University of New York at Buffalo, 14214, Buffalo, NY, USA

    R. J. Salvi, S. S. Saunders, E. Hashino & L. Chen

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  1. R. J. Salvi
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  2. S. S. Saunders
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  3. E. Hashino
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  4. L. Chen
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Salvi, R.J., Saunders, S.S., Hashino, E. et al. Discharge patterns of chicken cochlear ganglion neurons following kanamycin-induced hair cell loss and regeneration. J Comp Physiol A 174, 351–369 (1994). https://doi.org/10.1007/BF00240217

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