Vestibulo-Ocular Reflex Responses to a Multichannel Vestibular Prosthesis Incorporating a 3D Coordinate Transformation for Correction of Misalignment

Abstract

There is no effective treatment available for individuals unable to compensate for bilateral profound loss of vestibular sensation, which causes chronic disequilibrium and blurs vision by disrupting vestibulo-ocular reflexes that normally stabilize the eyes during head movement. Previous work suggests that a multichannel vestibular prosthesis can emulate normal semicircular canals by electrically stimulating vestibular nerve branches to encode head movements detected by mutually orthogonal gyroscopes affixed to the skull. Until now, that approach has been limited by current spread resulting in distortion of the vestibular nerve activation pattern and consequent inability to accurately encode head movements throughout the full 3-dimensional (3D) range normally transduced by the labyrinths. We report that the electrically evoked 3D angular vestibulo-ocular reflex exhibits vector superposition and linearity to a sufficient degree that a multichannel vestibular prosthesis incorporating a precompensatory 3D coordinate transformation to correct misalignment can accurately emulate semicircular canals for head rotations throughout the range of 3D axes normally transduced by a healthy labyrinth.

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

“…Previous experiments have shown that misalignment between the actual axis of head motion and the perceived axis (as indicated by the VOR axis) occurs during prosthetic electrical stimulation of ampullary nerves, probably due to current spread (Della Santina et al 2007;Lewis et al 2010;Fridman et al 2010;Hayden et al 2011). Here, we examined whether misalignment can be reduced through central adaptation via a directional plasticity mechanism similar to that which arises when normal animals are exposed to directionally altered visual scene movement coupled to head rotation.…”

“…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.…”

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.…”

“…The multichannel vestibular prosthesis (MVP) developed in our laboratory encodes 3D head rotation and elicits VOR responses approximately aligned to ideal response directions when assayed using 3D oculographic techniques (Della Santina et al 2007a;Fridman et al 2010;Davidovics et al 2013;Dai et al 2013 Despite physiologic data (Rubinstein et al 2012;Fridman et al 2010;Davidovics et al 2013;Perez Fornos et al 2014;Stokroos et al 2014;Dai et al 2011a) demonstrating well-aligned electrically evoked vestibulo-ocular reflex (eVOR) responses, and intact hearing in rhesus monkeys treated with intratympanic gentamicin (ITG) to ablate the natural VOR and then implanted with MVP electrode arrays (Dai et al 2011b), uncertainty remains regarding the status of the neuroepithelium after ITG injection and the extent of trauma caused by MVP electrode implantation. In contrast to the large body of evidence (Nadol and Eddington 2006;Nadol et al 2008;O'Leary et al 2013;Shepherd et al 1984) on the biocompatibility and tolerability of cochlear implant electrodes and the incidence of unfavorable tissue responses to implantation trauma that could hinder implant performance, there is a paucity of published data on the occurrence and extent of adverse reactions to implantation of vestibular prosthesis electrodes.…”