Virtual labyrinth model of vestibular afferent excitation via implanted electrodes: validation and application to design of a multichannel vestibular prosthesis

Abstract

To facilitate design of a multichannel vestibular prosthesis that can restore sensation to individuals with bilateral loss of vestibular hair cell function, we created a virtual labyrinth model. Model geometry was generated through 3-dimensional (3D) reconstruction of microMRI and microCT scans of normal chinchillas (Chinchilla lanigera) acquired with 30–48 μm and 12 μm voxels, respectively. Virtual electrodes were positioned based on anatomic landmarks, and the extracellular potential field during a current pulse was computed using finite element methods. Potential fields then served as inputs to stochastic, nonlinear dynamic models for each of 2415 vestibular afferent axons with spiking dynamics based on a modified Smith and Goldberg model incorporating parameters that varied with fiber location in the neuroepithelium. Action potential propagation was implemented by a well validated model of myelinated fibers. We tested the model by comparing predicted and actual 3D angular vestibulo-ocular reflex (aVOR) axes of eye rotation elicited by prosthetic stimuli. Actual responses were measured using 3D video-oculography. The model was individualized for each animal by placing virtual electrodes based on microCT localization of real electrodes. 3D eye rotation axes were predicted from the relative proportion of model axons excited within each of the three ampullary nerves. Multiple features observed empirically were observed as emergent properties of the model, including effects of active and return electrode position, stimulus amplitude and pulse waveform shape on target fiber recruitment and stimulation selectivity. The modeling procedure is partially automated and can be readily adapted to other species, including humans.

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.…”

“…Reducing this misalignment is a key goal of efforts to translate this technology to clinical application. Improvements in the design of electrode arrays (Hayden et al 2011), stimulus waveforms (Davidovics et al 2011, multichannel coding strategies , and current steering via multipolar stimulation ) have all improved misalignment, but some residual current spread and misalignment are unavoidable, so performance will ultimately depend on an implant user's ability to adjust over time to artificial sensory input.…”

Restoring the 3D vestibulo-ocular reflex via electrical stimulation: The Johns Hopkins multichannel vestibular prosthesis project

“…Definitively comparing the selectivity of different electrode array designs via in vivo experiments has been challenging, due to the large number of uncontrolled factors specific to each given animal (e.g., microanatomy, exact location of implanted electrodes, health of neural tissues in the implanted ear, etc.). To overcome this bottleneck and to achieve a more intuitive understanding of the biophysics of prosthetic vestibular nerve stimulation, we constructed an anatomically precise finite element/neuromorphic model of current flow in the implanted labyrinth [3]. …”

Progress Toward Development of a Multichannel Vestibular Prosthesis for Treatment of Bilateral Vestibular Deficiency

“…The anodic phase is only included to maintain charge balance over a millisecond time scale. Some MVP stimulus paradigm implementations also allow pulses to be asymmetric, typically using a “cathodic pseudomonophasic” approach in which a relatively brief and high‐amplitude cathodic phase is charge‐balanced by a relatively long and low‐current anodic phase (Hayden et al, 2011; Macherey et al, 2011).…”

“…Accurately targeting each SCC nerve branch via precise surgical placement of electrodes in the vestibular labyrinth can maximize electrode‐nerve coupling with the target ampullary nerve branch while minimizing misalignment owing to spurious stimulation of nontarget branches. Hayden et al extensively modeled current flow within the implanted chinchilla labyrinth, developing a finite element model based on precise anatomy, coupling that model's potential field predictions with a stochastic neuromorphic model incorporating 2415 model vestibular afferent fibers and realistic temporal dynamics, and then comparing model predictions of population activity in each nerve branch to quantitative measurements of 3D VOR responses (Hayden et al, 2011). This model has recently been extended to the rhesus monkey labyrinth (Hedjoudje et al, 2012).…”