Chronic Deafness Degrades Temporal Acuity in the Electrically Stimulated Auditory Pathway

John C Middlebrooks

doi:10.1007/s10162-018-0679-3

Abstract

Electrical stimulation of the auditory nerve with a penetrating intraneural (IN) electrode in acutely deafened cats produces much more restricted spread of excitation than is obtained in that preparation with a conventional cochlear implant (CI) as reported by Middlebrooks and Snyder (J Assoc Res Otolaryngol 8:258–279, 2007). That suggests that a future auditory prosthesis employing IN stimulation might offer human patients greater frequency selectivity than is available with a present-day CI. Nevertheless, it is a concern that the electrical field produced by an IN electrode might be too restricted to produce adequate stimulation of the partially depopulated auditory nerve of a deaf patient. We evaluated this by testing responses to IN and CI stimulation in adult-deafened cats. Activation of the auditory pathway was monitored by recording from the central nucleus of the inferior colliculus (ICC). Cats deaf for 153–277 days exhibited a ~ 30 % loss of auditory nerve fibers compared to cats deaf for < 18 h. Contrary to our concern, measures of thresholds and dynamic ranges showed no significant deafness-related impairment of excitation by IN or CN stimulation. Surprisingly, however, temporal acuity decreased dramatically in these adult-deafened cats, as demonstrated by a marked decrease in the maximum rate of electrical cochlear stimulation to which ICC neurons synchronized to IN or CI stimulation. For instance, half of ICC neurons synchronized to IN stimulation up to 203 pulses per second (pps) in acute deafness, whereas that number dropped to 79 pps for chronic deafness. Such a loss of temporal acuity might contribute to the poor sensitivity to temporal fine structure that has been reported in human CI users. Seemingly, the degraded temporal acuity that we observed in cats was even worse than the fine-structure sensitivity of human CI users, suggesting that most patients experience some improvement of temporal acuity resulting from restoration of patterned auditory nerve stimulation by a CI.

Highlights

The standard of care for bringing hearing sensitivity to severely-to-profoundly deaf people is a cochlear implant (CI) consisting of an array of electrodes inserted into the scala tympani of the cochlea
The chronically deaf data came from 13 nerves in 8 of the cats that were studied in terminal experiments, 8 nerves from the ear that was implanted with a CI and an IN array during the terminal experiment and 5 from the non-implanted ear
Across the 6 nerves that we examined from three acutely deafened cats, nerve areas ranged from 1.89 to 2.59 mm2, average fiber counts per high-magnification sample, averaged across each nerve, ranged from 341.1 to 480.5 fibers, and coefficients of variation for the counts in the 8-to-15 samples of each nerve (100 × standard deviation/ mean) ranged from 8.8 to 20.3

Summary

Introduction

The standard of care for bringing hearing sensitivity to severely-to-profoundly deaf people is a cochlear implant (CI) consisting of an array of electrodes inserted into the scala tympani of the cochlea. Success with CIs, varies widely among users (Gifford et al 2008; Holden et al 2013), and most CI users exhibit impaired sensitivity to temporal fine structure Several factors have been proposed to account for the variability in performance among post-lingually deaf CI users (reviewed by Moberly et al 2016). One widely held view is that the success with a CI declines with increasing duration of profound deafness prior to implantation (Gantz et al 1993; Blamey et al 1996; UK Cochlear Implant Study Group 2004; Holden et al 2013). Others have shown a marked influence of duration of deafness on CI performance only for durations of deafness 9 30 years (UK Cochlear Implant Study Group 2004; Moon et al 2014)

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Conclusion