A Multichannel Semicircular Canal Neural Prosthesis Using Electrical Stimulation to Restore 3-D Vestibular Sensation

Abstract

Bilateral loss of vestibular sensation can be disabling. Those afflicted suffer illusory visual field movement during head movements, chronic disequilibrium and postural instability due to failure of vestibulo-ocular and vestibulo-spinal reflexes. A neural prosthesis that emulates the normal transduction of head rotation by semicircular canals could significantly improve quality of life for these patients. Like the 3 semicircular canals in a normal ear, such a device should at least transduce 3 orthogonal (or linearly separable) components of head rotation into activity on corresponding ampullary branches of the vestibular nerve. We describe the design, circuit performance and in vivo application of a head-mounted, semi-implantable multi-channel vestibular prosthesis that encodes head movement in 3 dimensions as pulse-frequency-modulated electrical stimulation of 3 or more ampullary nerves. In chinchillas treated with intratympanic gentamicin to ablate vestibular sensation bilaterally, prosthetic stimuli elicited a partly compensatory angular vestibulo-ocular reflex in multiple planes. Minimizing misalignment between the axis of eye and head rotation, apparently caused by current spread beyond each electrode's targeted nerve branch, emerged as a key challenge. Increasing stimulation selectivity via improvements in electrode design, surgical technique and stimulus protocol will likely be required to restore AVOR function over the full range of normal behavior.

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

“…As described in detail in previous publications Chiang et al 2011;Della Santina et al 2007;Davidovics et al 2013), the mapping function was sigmoidal, smooth, and approximately linear for small deviations about the baseline pulse rate of 94 pps. The maximum pulse rate (e.g., during excitatory head rotations at 9300°/s) was 400 pps, and the minimum pulse rate (e.g., during inhibitory head rotations at 9300°/s) was 0 pps.…”

“…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.…”

“…We used 94 pps baseline stimulation rate, peak rate of 300 pps, and a sigmoid curvature of C=2 (Della Santina et al 2007) to mimic the mean resting rate of normal rhesus monkey vestibular afferent fibers (Sadeghi et al 2007). In chinchillas, the mean resting rate after intratympanic gentamicin treatment is typically about 60 % of normal (Hirvonen et al 2005;Della Santina et al 2005b), so the 94-pps baseline rate is probably above the spontaneous rate in rhesus monkeys after gentamicin ototoxic injury.…”

“…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.…”

“…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.…”