Chronic electrical stimulation by a cochlear implant promotes survival of spiral ganglion neurons after neonatal deafness

TLDR

Neonatal deafness leads to spiral ganglion neuron loss, and previous studies suggest that stimulation duration may affect survival, though the relative impact of stimulation type versus duration remains unclear. This investigation examined the consequences of neonatal deafness and chronic intracochlear electrical stimulation delivered by a cochlear implant during maturation. Kittens were bilaterally deafened with an ototoxic drug, then received unilateral electrical stimulation beginning at 7–10 weeks for 22–47 weeks, using bipolar intracochlear electrodes that delivered temporally challenging signals. Chronic stimulation preserved about 50 % of normal spiral ganglion cell density versus 30 % in controls—a 20 % significant improvement over prior 30 pps protocols—and also increased soma size, contributing to higher neural density.

Abstract

This investigation examined the consequences of neonatal deafness and chronic intracochlear electrical stimulation delivered by a cochlear implant during maturation. Kittens were bilaterally deafened by an ototoxic drug administered daily for 2 weeks immediately after birth. Unilateral electrical stimulation was initiated at 7-10 weeks of age and continued over periods of 22-47 weeks (4 hours/day; 5 days/week). Bipolar intracochlear electrodes delivered one of several different electrical signals designed to be temporally challenging to the central auditory system. Morphometric evaluation of spiral ganglion (SG) cell somata within Rosenthal's canal demonstrated a mean of approximately 50% of normal cell density maintained in the chronically stimulated ears, compared with approximately 30% on the control deafened side. This 20% difference in density was highly significant and was greater than differences reported in earlier studies using 30 pps stimulation delivered by either intracochlear bipolar or round window monopolar electrodes. However, the duration of stimulation was also longer in the present study, so it is unclear to what extent the nature of the temporally challenging stimulation vs. its duration contributed to the marked increase in survival. Measurements of the SG cell somata revealed a pronounced decrease in cell diameter in neonatally deafened cats studied about 1 year after deafening, and an additional decrease after long-term deafness (2.5-6.5 years). Furthermore, in the cochlear regions with the greatest stimulation-induced differences in SG cell density, direct measurements of cross-sectional soma area of the largest cells revealed that cells were significantly larger in the stimulated ears. Thus, in addition to the marked increase in the number of surviving SG cells, larger soma area contributed modestly to the pronounced increase in neural density following chronic electrical stimulation.