Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model

Front Neurosci. 2022 Jul 6:16:914876. doi: 10.3389/fnins.2022.914876. eCollection 2022.

Abstract

After hearing loss retrograde degeneration of spiral ganglion neurons (SGNs) has been described. Studies modeling the effects of degeneration mostly omitted peripheral processes (dendrites). Recent experimental observations indicated that degenerating SGNs manifested also a reduced diameter of their dendrites. We simulated populations of 400 SGNs inside a high resolution cochlear model with a cochlear implant, based on μCT scans of a human temporal bone. Cochlear implant stimuli were delivered as biphasic pulses in a monopolar configuration. Three SGN situations were simulated, based on our previous measurements of human SGN dendrites: (A) SGNs with intact dendrites (before degeneration), (B) degenerating SGNs, dendrites with a smaller diameter but original length, (C) degenerating SGNs, dendrites omitted. SGN fibers were mapped to characteristic frequency, and place pitch was estimated from excitation profiles. Results from degenerating SGNs (B, C) were similar. Most action potentials were initiated in the somatic area for all cases (A, B, C), except for areas near stimulating electrodes in the apex with intact SGNs (A), where action potentials were initiated in the distal dendrite. In most cases, degenerating SGNs had lower thresholds than intact SGNs (A) (down to -2 dB). Excitation profiles showed increased ectopic activation, i.e., activation of unintended neuronal regions, as well as similar neuronal regions excited by different apical electrodes, for degenerating SGNs (B, C). The estimated pitch showed cases of pitch reversals in apical electrodes for intact SGNs (A), as well as mostly identical pitches evoked by the four most apical electrodes for degenerating SGNs (B, C). In conclusion, neuronal excitation profiles to electrical stimulation exhibited similar traits in both ways of modeling SGN degeneration. Models showed degeneration of dendrites caused increased ectopic activation, as well as similar excitation profiles and pitch evoked by different apical electrodes. Therefore, insertion of electrodes beyond approximately 450° may not provide any benefit if SGN dendrites are degenerated.

Keywords: cochlear implant; computational model; deep insertion; ectopic activation; human; neural degeneration; personalized model; spiral ganglion neurons.