Does cochlear implantation and electrical stimulation affect residual hair cells and spiral ganglion neurons?

Abstract

Increasing numbers of cochlear implant subjects have some level of residual hearing at the time of implantation. The present study examined whether (i) hair cells that have survived one pathological insult (aminoglycoside deafening), can survive and function following long-term cochlear implantation and electrical stimulation (ES); and (ii) chronic ES in these cochleae results in greater trophic support of spiral ganglion neurons (SGNs) compared with cochleae devoid of hair cells. Eight cats, with either partial (n=4) or severe (n=4) sensorineural hearing loss, were bilaterally implanted with scala tympani electrode arrays 2 months after deafening, and received unilateral ES using charge balanced biphasic current pulses for periods of up to 235 days. Frequency-specific compound action potentials and click-evoked auditory brainstem responses (ABRs) were recorded periodically to monitor the residual acoustic hearing. Electrically-evoked ABRs (EABRs) were recorded to confirm the stimulus levels were 3-6 dB above the EABR threshold. On completion of the ES program the cochleae were examined histologically. Partially deafened animals showed no significant increase in acoustic thresholds over the implantation period. Moreover, chronic ES of an electrode array located in the base of the cochlea did not adversely affect hair cells in the middle or apical turns. There was evidence of a small but statistically significant rescue of SGNs in the middle and apical turns of stimulated cochleae in animals with partial hearing. Chronic ES did not, however, prevent a reduction in SGN density for the severely deaf cohort, although SGNs adjacent to the stimulating electrodes did exhibit a significant increase in soma area (p<0.01). In sum, chronic ES in partial hearing animals does not adversely affect functioning residual hair cells apical to the electrode array. Moreover, while there is an increase in the soma area of SGNs close to the stimulating electrodes in severely deaf cochleae, this trophic effect does not result in increased SGN survival.

Factors influencing neurotrophic effects of electrical stimulation in the deafened developing auditory system

“…Lousteau (1987), Hartshorn et al (1991), and Miller and Altschuler et al (1995; demonstrated increased SG cell survival after chronic ICES in guinea pigs deafened by ototoxic drugs and implanted as young adults. In contrast, other studies have failed to find trophic effects in vivo in guinea pigs , and Shepherd and coworkers (Araki et al, 1998;Shepherd et al, 1994) found no overall difference in SG cell survival after chronic ICES in cats deafened at an early age by ototoxic drugs, although recently they reported a significant regional increase in SG survival in partially deafened cats and a consistent increase in the size of stimulated SG cells (Coco et al, 2007).…”

Effects of Hearing Preservation on Psychophysical Responses to Cochlear Implant Stimulation

“…However, since the stimulation was not continuous, the total duration of electrical stimulation was limited to a small fraction of the time that was spent in the testing booth. As a result, the subjects in this study received much less electrical stimulation as compared to other studies that employed chronic electrical stimulation to test safe limits or protective effects of electrical stimulation (Walsh et al 1981;Duckert and Miller 1982;Duckert 1983;Ni et al 1992;Xu et al 1997;Coco et al 2007). …”

“…One animal study suggests that cochlear implantation surgery causes hearing loss due to the direct acute trauma of electrode insertion combined with subsequent apoptotic cell death of hair cells (Eshraghi et al 2005). The effects of electrical stimulation on hair cells have also been studied in the past in several animal species, with mixed results that depend partly on charge density (Walsh et al 1981;Duckert and Miller 1982;Duckert 1983;Ni et al 1992;Xu et al 1997;Coco et al 2007). Thus, cochlear pathology may be a result of the implantation surgery or the electrical stimulation itself.…”

Effects of Brain-Derived Neurotrophic Factor (BDNF) and Electrical Stimulation on Survival and Function of Cochlear Spiral Ganglion Neurons in Deafened, Developing Cats

“…Presumably, reduction in somatic size reflects reduced metabolic requirements of these neurons due to reduced spike activity after deafness (Hartmann et al 1984;Liberman and Kiang 1978;Shepherd and Javel 1997). When electrical stimulation from a CI is applied to reactivate these neurons, modest but significant increases in SG soma area in the stimulated cochleae have been reported (Araki et al 1998;Coco et al 2007;Leake et al 1999Leake et al , 2007. However, the effects on soma area associated with neurotrophin administration are much greater than the cell size changes elicited with electrical stimulation.…”

“…In our laboratory, studies of cats deafened prior to hearing onset have shown that multichannel CI electrical stimulation applied over several months results in substantial improvement in SG neural survival (Leake et al 1999(Leake et al , 2007(Leake et al , 2008a above that seen in the contralateral deafened cochleae. Other studies, however, have not found evidence of trophic effects of electrical stimulation (Araki et al 1998;Coco et al 2007;Li et al 1999;Shepherd et al 1994). These disparities in findings suggest that differences among animal models, methods of stimulation (e.g., the position of stimulating electrodes, applied signals, and efficacy in exciting neurons across a broad sector of the spiral ganglion), and/or methods of analysis of SG density are critically important.…”