Effects of vestibular prosthesis electrode implantation and stimulation on hearing in rhesus monkeys

Abstract

To investigate the effects of vestibular prosthesis electrode implantation and activation on hearing in rhesus monkeys, we measured auditory brainstem responses (ABR) and distortion product otoacoustic emissions (DPOAE) in four rhesus monkeys before and after unilateral implantation of vestibular prosthesis electrodes in each of 3 left semicircular canals (SCC). Each of the 3 left SCCs were implanted with electrodes via a transmastoid approach. Right ears, which served as controls, were not surgically manipulated. Hearing tests were conducted before implantation (BI) and then 4 weeks post-implantation both without electrical stimulation (NS) and with electrical stimulation (S). During the latter condition, prosthetic electrical stimuli encoding 3 dimensions of head angular velocity were delivered to the 3 ampullary branches of the left vestibular nerve via each of 3 electrode pairs of a multichannel vestibular prosthesis. Electrical stimuli comprised charge-balanced biphasic pulses at a baseline rate of 94 pulses/s, with pulse frequency modulated from 48 to 222 pulses/s by head angular velocity. ABR hearing thresholds to clicks and tone pips at 1, 2, and 4 kHz increased by 5-10 dB from BI to NS and increased another ∼5 dB from NS to S in implanted ears. No significant change was seen in right ears. DPOAE amplitudes decreased by 2-14 dB from BI to NS in implanted ears. There was a slight but insignificant decrease of DPOAE amplitude and a corresponding increase of DPOAE/Noise floor ratio between NS and S in implanted ears. Vestibular prosthesis electrode implantation and activation have small but measurable effects on hearing in rhesus monkeys. Coupled with the clinical observation that patients with cochlear implants only rarely exhibit signs of vestibular injury or spurious vestibular nerve stimulation, these results suggest that although implantation and activation of multichannel vestibular prosthesis electrodes in human will carry a risk of hearing loss, that loss is not likely to be severe.

Copyright © 2010 Elsevier B.V. All rights reserved.

Figures

Figure 1. 3D computed tomography [CT] reconstructions of electrode array placement

(A) Posterolateral view of 3D CT surface reconstruction showing electrode array leads implanted in the left labyrinth of a rhesus monkey via the mastoid cavity. a: lead to anterior and horizontal ampullae; b: lead to posterior ampulla; c: common crus reference electrode; d: neck reference electrode; M: mandibular ramus; Z: zygomatic arch; ANT, POST, SUP, INF: anterior, posterior, superior, inferior. (B) Oblique CT cut through the plane of the basal turn of the cochlea [Co], showing bifurcated electrode array [a] entering the ampullae of the superior [s-scc] and horizontal [h-scc] semicircular canals. Part of the neck reference electrode [d] is also visible, but the posterior scc electrode array is not included in this section. AM, PL: anteriomedial, posterolateral.

Figure 2. Eye movement responses

to pulse rate modulated, biphasic constant current pulses delivered via bipolar prosthesis electrodes implanted in the left labyrinth of a stationary alert rhesus monkey tested in darkness. Upper traces show stimulus waveforms modulating pulse rates on electrodes in the left horizontal (LH), left anterior (LA) and left posterior (LP) semicircular canal ampullary nerves. In each case, modulation frequency is 2 Hz, baseline pulse rate is 94 pulses/sec, modulation range is 48–222 pulses/sec, and the modulating waveforms shown were passed to the microprocessor of the prosthesis in place of actual gyro signals to emulate sinusoidally varying head velocity about each semicircular canal axis in an animal whose head remained still. Lower traces show eye movements about the mean horizontal (HORIZ), left-anterior/right-posterior (LARP), and right-anterior/left-posterior (RALP) axes of the head, which approximately align with the corresponding semicircular canals. Blinks and/or voluntary saccades are also evident as departures from the generally sinusoidal responses to prosthetic stimuli.

Figure 3. ABR thresholds in response to clicks and tone pips

(A) ABR thresholds [mean±SD] in response to clicks and pure tone pips at 1, 2 and 4 Hz, measured from eight normal ears in four rhesus monkeys. (B) ABR thresholds measured from implanted left ears (triangles) and nonimplanted right ears (squares) 4 weeks after surgery in four monkeys, prior to prosthesis activation. (C) ABR thresholds measured during prosthetic vestibular stimulation of the implanted ear (modulating over the range 48–222 pulses/sec).

Figure 4. Absolute distortion product otoacoustic emission [DPOAE] response amplitudes

(A) DPOAE levels [mean±SD] in response to clicks and pure tone pips at 1, 2 and 4 Hz, measured from eight normal ears in four rhesus monkeys. (B) DPOAE levels measured from implanted ears (triangles) and contralateral ears (squares) 4 weeks after surgery in four monkeys, prior to prosthesis activation. (C) DPOAE levels measured during prosthetic vestibular stimulation of the implanted ear (modulating over the range 48–222 pps). In panels B and C, triangles represent left (implanted) ear and squares represent right (control) ear.

Figure 5. Distortion product vs. noise floor [DP/NF] ratios

(A) DP/NF ratio [mean±SD] in response to clicks and pure tone pips at 1, 2 and 4 Hz, measured from eight normal ears in four rhesus monkeys. (B) DP/NF ratio measured from implanted ears (triangles) and contralateral ears (squares) 4 weeks after surgery in four monkeys, prior to prosthesis activation. (C) DP/NF ratio measured during prosthetic vestibular stimulation of the implanted ear (modulating over the range 48–222 pps). In panels B and C, triangles represent left (implanted) ear and squares represent right (control) ear.