Effects of Biphasic Current Pulse Frequency, Amplitude, Duration, and Interphase Gap on Eye Movement Responses to Prosthetic Electrical Stimulation of the Vestibular Nerve

Abstract

An implantable prosthesis that stimulates vestibular nerve branches to restore sensation of head rotation and vision-stabilizing reflexes could benefit individuals disabled by bilateral loss of vestibular (inner ear balance) function. We developed a prosthesis that partly restores normal function in animals by delivering pulse frequency modulated (PFM) biphasic current pulses via electrodes implanted in semicircular canals. Because the optimal stimulus encoding strategy is not yet known, we investigated effects of varying biphasic current pulse frequency, amplitude, duration and interphase gap on vestibulo-ocular reflex (VOR) eye movements in chinchillas. Increasing pulse frequency increased response amplitude while maintaining a relatively constant axis of rotation. Increasing pulse amplitude (range 0-325 μA) also increased response amplitude but spuriously shifted eye movement axis, probably due to current spread beyond the target nerve. Shorter pulse durations (range 28-340 μs) required less charge to elicit a given response amplitude and caused less axis shift than longer durations. Varying interphase gap (range 25-175 μs) had no significant effect. While specific values reported herein depend on microanatomy and electrode location in each case, we conclude that PFM with short duration biphasic pulses should form the foundation for further optimization of stimulus encoding strategies for vestibular prostheses intended to restore sensation of head rotation.

Directional Plasticity Rapidly Improves 3D Vestibulo-Ocular Reflex Alignment in Monkeys Using a Multichannel Vestibular Prosthesis

“…This should achieve more symmetric responses for both excitatory and inhibitory head rotations, respectively, in an animal using a single, unilaterally implanted prosthesis, than could be achieved without a baseline rate above the afferents' spontaneous discharge. By adapting central vestibular neurons to an increased baseline rate when the head is stationary, one can down-modulate stimulus pulse rates further below baseline to encode inhibitory head rotations (e.g., see Lewis et al 2010;Della Santina et al 2007;Davidovics et al 2011). In this study, we used approximately normal baseline rates in the MVP, accepting a greater degree of VOR asymmetry (because spontaneous afferent activity maintains a floor beneath which reductions in prosthesis pulse rate cannot reduce afferent activity; in exchange for a larger dynamic range of eye rotations in response to excitatory head rotations.…”

“…When this reflex fails due to labyrinthine injuries that spare the vestibular nerve, a multichannel vestibular prosthesis (MVP) can help stabilize images on the retinae and normalize perception of head movement by measuring 3D head movement and encoding that movement via electrical stimuli delivered to the ampullary nerves. We previously developed and described such a device, demonstrating its ability to partially restore a normal 3D VOR (Della Santina et al 2005bFridman et al 2010;Davidovics et al 2011;Dai et al 2011).…”

“…Despite promising results using this approach, current spread or imprecise electrode placement can reduce MVP efficacy through spurious activation of nontarget axons, which manifests as misalignment between the actual and perceived axis of head motion (Della Santina et al 2007;Fridman et al 2010;Davidovics et al 2011;Dai et al 2011). Reducing this misalignment is a key goal of efforts to translate this technology to clinical application.…”

Multichannel Vestibular Prosthesis Employing Modulation of Pulse Rate and Current with Alignment Precompensation Elicits Improved VOR Performance in Monkeys

“…We extended this approach to a multichannel vestibular prosthesis (MVP) that senses 3D head rotation and encodes it via stimulation of all three ampullary nerves in the labyrinth, and we demonstrated its ability to partly restore the 3D VOR in both rodents and rhesus monkeys rendered vestibular deficient via bilateral intratympanic injection of gentamicin (Della Santina et al 2005aFridman et al 2010a;Dai et al 2011b, c;Davidovics et al 2011Davidovics et al , 2012Sun et al 2011).…”

Histopathologic Changes of the Inner ear in Rhesus Monkeys After Intratympanic Gentamicin Injection and Vestibular Prosthesis Electrode Array Implantation

“…Apart from the proximity of an electrode to its target nerve branch, the relative distance from an electrode to target vs nontarget ampullary nerves is a key determinant of 3D eVOR performance because restoration of a directionally appropriate 3D VOR requires selective stimulation of the target ampullary nerve and minimization of current spread to nontarget neurons. The anatomic proximity of HSCC and SSCC ampullary nerves is such that achieving selective stimulation of one without inadvertently exciting the other has been a central challenge in designing electrode arrays, implantation techniques and stimulation protocols (Fridman et al 2010;Della Santina et al 2005;Della Santina et al 2007b;Davidovics et al 2011). In one specimen (F32RhD/right), the HSCC electrode capsule was situated 452 and 928 μm from the targeted HSCC and SSCC ampullary nerves, respectively, representing a difference in distance of only 476 μm (Fig.…”