Semin Hear 2003; 24(2): 135-146
DOI: 10.1055/s-2003-39840
Copyright © 2002 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Functional Changes in Peripheral and Central Auditory Pathways following Selective Inner Hair Cell Loss

Richard J. Salvi, Dalian Ding, Jian Wang, Sandra L. McFadden, Wei Sun
  • Center for Hearing and Deafness, University at Buffalo, Buffalo, New York
Further Information

Publication History

Publication Date:
11 June 2003 (online)

ABSTRACT

When the inner hair cells of the cochlea are destroyed, the neural activity conveyed to the central auditory system is reduced. How does the central auditory system respond when it is deprived of information? To address this question, inner hair cells in the chinchilla cochlea were selectively destroyed with carboplatin. Inner hair cell lesions had no effect on distortion product otoacoustic emissions or the cochlear microphonic potential, showing that the outer hair cells were functionally intact. Recordings from single auditory nerve fibers showed that the surviving inner hair cells and type I neurons had normal thresholds and sharp tuning. The only notable deficit was a reduction of the compound action potential from the auditory nerve in proportion to the amount of inner hair cell loss. Despite reduced input from the cochlea and auditory nerve, the local field potentials in the inferior colliculus and the auditory cortex were not consistently reduced. In fact, potentials in the auditory cortex were frequently larger than normal. Enhancement of the cortical potential may be due to loss of γ-aminobutyric acid (GABA)-mediated inhibition. The data show that when the inner hair cells of the cochlea are damaged, the central auditory system increases its gain to compensate for a reduced sensory input.

REFERENCES

  • 1 Spoendlin H. The innervation of the organ of Corti.  J Laryngol Otol . 1967;  81 717-738
  • 2 Robertson D. Horseradish peroxidase injection of physiologically characterized afferent and efferent neurons in the guinea pig spiral ganglion.  Hear Res . 1984;  15 113-121
  • 3 Brownell W E, Bader C R, Bertrand D, de Ribaupierre Y. Evoked mechanical responses of isolated cochlear outer hair cells.  Science . 1985;  227 194-196
  • 4 Santos-Sacchi J. Reversible inhibition of voltage-dependent outer hair cell motility and capacitance.  J Neurosci . 1991;  11 3096-3110
  • 5 Dallos P. Outer hair cells: the inside story.  Ann Otol Rhinol Laryngol . 1997;  168(Suppl) 16-22
  • 6 Liberman M C. The cochlear frequency map for the cat: labeling auditory-nerve fibers of known characteristic frequency.  J Acoust Soc Am . 1982;  72 1441-1449
  • 7 Ryan A, Dallos P. Effect of absence of cochlear outer hair cells on behavioural auditory threshold.  Nature . 1975;  253 44-46
  • 8 Dallos P, Harris D, Ozdamar O, Ryan A. Behavioral, compound action potential, and single unit thresholds: relationship in normal and abnormal ears.  J Acoust Soc Am . 1978;  64 151-157
  • 9 Salvi R J, Perry J, Hamernik R P, Henderson D. Relationship 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 New York: Raven Press 1982: 165-188
  • 10 Wake M, Takeno S, Ibrahim D, Harrison R. Selective inner hair cell ototoxicity induced by carboplatin.  Laryngoscope . 1994;  104 488-493
  • 11 Ding D L, Wang J, Salvi R J. Selective loss of inner hair cells and type I ganglion neurons in carboplatin-treated chinchillas: mechanisms of damage and protection. In: Henderson D, Salvi RJ, Quaranta A, McFadden SL, Burkard RF, eds. Ototoxicity: Basic Science and Clinical Applications New York: New York Academy of Sciences 1999: 884:152-170
  • 12 Jardine D, Sun W, Ding D, Salvi R J. How many inner hair cells do we need to hear?.  Assoc Res Otolaryngol Abstr . 2000;  845 237
  • 13 Probst R, Lonsbury-Martin B L, Martin G K. A review of otoacoustic emissions.  J Acoust Soc Am . 1991;  89 2027-2067
  • 14 Brown A M, McDowell B, Forge A. Acoustic distortion products can be used to monitor the effects of chronic gentamicin treatment.  Hear Res . 1989;  42 143-156
  • 15 Schrott A, Puel J L, Rebillard G. Cochlear origin of 2f1-f2 distortion products assessed by using 2 types of mutant mice.  Hear Res . 1991;  52 245-253
  • 16 Trautwein P, Hofstetter P, Wang J, Salvi R, Nostrant A. Selective inner hair cell loss does not alter distortion product otoacoustic emissions.  Hear Res . 1996;  96 71-82
  • 17 Hofstetter P, Ding D, Powers N, Salvi R J. Quantitative relationship of carboplatin dose to magnitude of inner and outer hair cell loss and the reduction in distortion product otoacoustic emission amplitude in chinchillas.  Hear Res . 1997;  112 199-215
  • 18 Dallos P, Billone M C, Durrant J D, Wang C, Raynor S. Cochlear inner and outer hair cells: functional differences.  Science . 1972;  177 356-358
  • 19 Wang J, Powers N L, Hofstetter P. Effects of selective inner hair cell loss on auditory nerve fiber threshold, tuning and spontaneous and driven discharge rate.  Hear Res . 1997;  107 67-82
  • 20 Qiu C, Salvi R, Ding D, Burkard R. Inner hair cell loss leads to enhanced response amplitudes in auditory cortex of unanesthetized chinchillas: evidence for increased system gain.  Hear Res . 2000;  139 153-171
  • 21 McFadden S L, Kasper C, Ostrowski J, Ding D, Salvi R J. Effects of inner hair cell loss on inferior colliculus evoked potential thresholds, amplitudes and forward masking functions in chinchillas.  Hear Res . 1998;  120 121-132
  • 22 Prieto J J, Peterson B A, Winer J A. Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI).  J Comp Neurol . 1994;  344 349-382
  • 23 Cox C L, Metherate R, Weinberger N M, Ashe J H. Synaptic potentials and effects of amino acid antagonists in the auditory cortex.  Brain Res Bull . 1992;  28 401-410
  • 24 Metherate R, Ashe J H. Synaptic interactions involving acetylcholine, glutamate, and GABA in rat auditory cortex.  Exp Brain Res . 1995;  107 59-72
  • 25 Wang J, Caspary D, Salvi R J. GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex.  Neuroreport . 2000;  11 1137-1140
  • 26 Salvi R J, Sun W, Wang J. Diminished GABA-A mediated inhibition in auditory cortex following carboplatin-induced inner hair cell loss.  Assoc Res Otolaryngol Abstr . 2000;  23 522
  • 27 Starr A, Picton T W, Sininger Y, Hood L J, Berlin C I. Auditory neuropathy.  Brain . 1996;  119 741-753
  • 28 Starr A, Sininger Y S, Pratt H. The varieties of auditory neuropathy.  J Basic Clin Physiol Pharmacol . 2000;  11 215-230
  • 29 Zeng F G, Oba S, Garde S, Sininger Y, Starr A. Temporal and speech processing deficits in auditory neuropathy.  Neuroreport . 1999;  10 3429-3435
  • 30 Butinar D, Zidar J, Leonardis L. Hereditary auditory, vestibular, motor, and sensory neuropathy in a Slovenian Roma (Gypsy) kindred.  Ann Neurol . 1999;  46 36-44
  • 31 Kraus N, Bradlow A R, Cheatham M A. Consequences of neural asynchrony: a case of auditory neuropathy.  J Assoc Res Otolaryngol . 2000;  1 33-45
  • 32 Burkard R, Trautwein P, Salvi R. The effects of click level, click rate, and level of background masking noise on the inferior colliculus potential (ICP) in the normal and carboplatin-treated chinchilla.  J Acoust Soc Am . 1997;  102 3620-3627
  • 33 Lockwood A H, Salvi R J, Coad M L. The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity.  Neurology . 1998;  50 114-120
    >