Chronic intracochlear electrical stimulation induces selective survival of spiral ganglion neurons in neonatally deafened cats

Ten newborn kittens were deafened by systemic administration of neomycin sulfate. Profound hearing losses were documented by ABR and FFR (500 Hz) testing. At 9-17 weeks of age, the young deafened cats were unilaterally implanted with a multichannel scala tympani electrode. Six of the animals were chronically stimulated at 6 dB above electrically evoked ABR thresholds for 1 h/day for periods of 1 month or 3 months. Stimuli were charge-balanced biphasic pulses (200 microseconds/phase, 30 pps.) The remaining 4 cats underwent identical deafening and implantation schedules but were not stimulated. Results indicate that administration of neomycin in neonatal cats induced degeneration of hair cells and spiral ganglion cell loss that was bilaterally symmetrical between the two cochleas of each individual animal, although there was variation between animals in the severity of the ototoxic drug effect. In animals receiving passive (unstimulated) implants, morphometric analysis of spiral ganglion cell density showed no significant difference in ganglion cell survival between the implanted cochleas and the contralateral control ears. In contrast, animals that were chronically stimulated for 3 months showed significantly better neuronal survival in implanted and stimulated cochleas as compared to contralateral deafened control ears. The induced conservation of spiral ganglion neurons was observed consistently within the basal cochlear region near the stimulating electrodes. In more apical regions there was no significant difference between the stimulated and control cochleas. The mechanisms underlying this selective conservation of spiral ganglion neurons induced by chronic intracochlear electrical stimulation are uncertain. Since no comparable chronic stimulation studies have been conducted in adults, it is not known whether similar conservation effects could be induced in mature animals.

[1]  E. Weibel Stereological Methods. Practical methods for biological morphometry , 1979 .

[2]  Douglas B. Webster,et al.  Late onset of auditory deprivation does not affect brainstem auditory neuron soma size , 1983, Hearing Research.

[3]  D. Moore,et al.  Projections from the cochlear nucleus to the inferior colliculus in normal and neonatally cochlea‐ablated gerbils , 1985, The Journal of comparative neurology.

[4]  M. Silverman,et al.  Plasticity of binaural interaction. I. Effect of early auditory deprivation. , 1977, Journal of neurophysiology.

[5]  J. Coleman,et al.  Age-dependent effects of acoustic deprivation on spherical cells of the rat anteroventral cochlear nucleus , 1983, Experimental Neurology.

[6]  J. Coleman,et al.  Effects of monaural and binaural sound deprivation on cell development in the anteroventral cochlear nucleus of rats , 1979, Experimental Neurology.

[7]  R. Lousteau,et al.  Increased spiral ganglion cell survival in electrically stimulated, deafened guinea pig cochleae , 1987, The Laryngoscope.

[8]  D. Webster,et al.  Auditory brainstem responses in neonatally sound deprived CBA/J mice , 1983, Hearing Research.

[9]  D B Moody,et al.  The patas monkey as a model for dihydrostreptomycin ototoxicity. , 1977, Acta oto-laryngologica.

[10]  R A Levine,et al.  Auditory-Nerve Activity in Cats Exposed to Ototoxic Drugs and High-Intensity Sounds , 1976, The Annals of otology, rhinology, and laryngology.

[11]  H. Spoendlin,et al.  Retrograde degeneration of the cochlear nerve. , 1975, Acta oto-laryngologica.

[12]  P. A. Leake-Jones,et al.  Neomycin ototoxicity: ultrastructural surface pathology of the organ of Corti. , 1980, Scanning electron microscopy.

[13]  Stephen J. Rebscher,et al.  Chronic intracochlear electrical stimulation in the neonatally deafened cat. II: Temporal properties of neurons in the inferior colliculus , 1991, Hearing Research.

[14]  D. Webster,et al.  Neonatal sound deprivation affects brain stem auditory nuclei. , 1977, Archives of otolaryngology.

[15]  D R Moore,et al.  Auditory brainstem of the ferret: Effects of unilateral cochlear lesions on cochlear nucleus volume and projections to the inferior colliculus , 1988, The Journal of comparative neurology.

[16]  R. Ruben,et al.  Plasticity of the Developing Auditory System , 1980, The Annals of otology, rhinology, and laryngology.

[17]  S D Esterly,et al.  A critical period for the recovery of sound localization accuracy following monaural occlusion in the barn owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  D. Webster Conductive hearing loss affects the growth of the cochlear nuclei over an extended period of time , 1988, Hearing Research.

[19]  Michael C. Vivion,et al.  Deaf animal models for studies of a multichannel cochlear prosthesis , 1982, Hearing Research.

[20]  G Hung,et al.  Stereological methods. Vol. 1: Practical methods for biological morphometry By . Academic Press, New York/London, 1979. xvi + 415 pp., $57.50 , 1984 .

[21]  Patricia A. Leake,et al.  Cochlear pathology of long term neomycin induced deafness in cats , 1988, Hearing Research.

[22]  R. Ruben Unsolved issues around critical periods with emphasis on clinical application. , 1986, Acta oto-laryngologica. Supplementum.

[23]  Leake-Jones Pa,et al.  Cochlear pathology in cats following administration of neomycin sulfate. , 1979 .

[24]  A Kohonen,et al.  Effect of some ototoxic drugs upon the pattern and innervation of cochlear sensory cells in the guinea pig. , 1965, Acta oto-laryngologica. Supplementum.

[25]  J. E. Williams,et al.  Development of the dorsal and ventral cochlear nuclei in rat and effects of acoustic deprivation. , 1982, Brain research.

[26]  H. Killackey,et al.  Ascending projections to the inferior colliculus following unilateral cochlear ablation in the neonatal gerbil, Meriones unguiculatus , 1983, The Journal of comparative neurology.

[27]  H. Schuknecht,et al.  Ganglion cell populations in normal and pathological human cochleae. Implications for cochlear implantation. , 1978, The Laryngoscope.

[28]  L. Johnsson,et al.  Sequence of Degeneration of Corti's Organ and its First-Order Neurons , 1974, The Annals of otology, rhinology, and laryngology.

[29]  Molly Webster,et al.  Effects of Neonatal Conductive Hearing Loss on Brain Stem Auditory Nuclei , 1979, The Annals of otology, rhinology, and laryngology.

[30]  M. Stroud,et al.  Clinical differentiation of conductive hearing loss , 1978, The Laryngoscope.