Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis

Abstract

By sensing three-dimensional (3D) head rotation and electrically stimulating the three ampullary branches of a vestibular nerve to encode head angular velocity, a multichannel vestibular prosthesis (MVP) can restore vestibular sensation to individuals disabled by loss of vestibular hair cell function. However, current spread to afferent fibers innervating non-targeted canals and otolith endorgans can distort the vestibular nerve activation pattern, causing misalignment between the perceived and actual axis of head rotation. We hypothesized that over time, central neural mechanisms can adapt to correct this misalignment. To test this, we rendered five chinchillas vestibular-deficient via bilateral gentamicin treatment and unilaterally implanted them with a head mounted MVP. Comparison of 3D angular vestibulo-ocular reflex (aVOR) responses during 2 Hz, 50°/s peak horizontal sinusoidal head rotations in darkness on the first, third and seventh days of continual MVP use revealed that eye responses about the intended axis remained stable (at about 70% of the normal gain) while misalignment improved significantly by the end of one week of prosthetic stimulation. A comparable time course of improvement was also observed for head rotations about the other two semicircular canal axes and at every stimulus frequency examined (0.2–5 Hz). In addition, the extent of disconjugacy between the two eyes progressively improved during the same time window. These results indicate that the central nervous system rapidly adapts to multichannel prosthetic vestibular stimulation to markedly improve 3D aVOR alignment within the first week after activation. Similar adaptive improvements are likely to occur in other species, including humans.

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

“…We would then be able to characterize the uncompensated eye responses and program the prosthesis with appropriately calculated transformation matrices necessary to elicit well-aligned responses. As the subject adapts to prosthetic stimulation, it is likely that VOR alignment and magnitude will improve further as it did in chinchillas over a period of 7 days (Dai et al 2011c). The stimulation strategies described in this paper, which were utilized to elicit large VOR responses in any desired direction in primates, provide a solid foundation for successful restoration of VOR in patients suffering from bilateral vestibular disorder.…”

“…Our methods for surgical implantation of a head-fixation mechanism and scleral coils for magnetic search coil recording of 3D eye movements in primates have been described previously (Minor et al 1999;Dai et al 2011c). With the animal under general inhalational anesthesia (1.5-5 % isoflurane), a light poly-ether-ether-ketone head cap was affixed to the skull under sterile conditions using titanium bone screws and poly-methyl methacrylate.…”

“…Prior to any intervention of either labyrinth, normal VOR performance was characterized during whole-body rotations in darkness for 50°/s peak velocity sinusoids at 0.05, 0.1, 0.2, 0.5, 1, 2, and 5 Hz and for acceleration steps of 1,000°/s 2 to a plateau velocity of 150°/s using the eye movement measurement methods described below (Dai et al 2011c). Gains for rotational frequencies 0.5-5 Hz were close to one for all three SCC axes tested.…”

“…After characterization of an animal's normal VOR performance, a separate surgery was performed to implant an electrode array in the left labyrinth via a transmastoid approach similar to that used for cochlear implantation or labyrinthectomy (Dai et al 2011c). Under sterile conditions, a cortical mastoidectomy was performed.…”

Vestibular Implants: 8 Years of Experience with Electrical Stimulation of the Vestibular Nerve in 11 Patients with Bilateral Vestibular Loss

“…Electrical stimulation was identified as an effective means for activating the vestibular system in animals already in the 1960s [19,20]. Most recent animal research efforts have concentrated on meticulously investigating the effects of electrical stimulation parameters on vestibular responses [21], focusing mainly on vestibulo-ocular responses [22,23,24,25,26,27,28,29,30,31,32,33,34], but also on orientation percepts and postural responses [35,36,37]. In humans, extralabyrinthine and intralabyrinthine surgical routes to the lateral (LAN), posterior (PAN) and superior (SAN) ampullary branches of the vestibular nerve have been described and validated in peroperative stimulation trials [38,39,40,41,42,43].…”