Chronic stimulation of the semicircular canals using a multichannel vestibular prosthesis: effects on locomotion and angular vestibulo-ocular reflex in chinchillas

Abstract

Bilateral loss of vestibular sensation causes difficulty maintaining stable vision, posture and gait. An implantable prosthesis that partly restores vestibular sensation could significantly improve quality of life for individuals disabled by this disorder. We have developed a head-mounted multichannel vestibular prosthesis (MVP) that restores sufficient semicircular canal function to recreate a 3D angular vestibulo-ocular reflex (aVOR). In this study, we evaluated effects of chronic MVP stimulation on locomotion in chinchillas. Two of three animals examined exhibited significant improvements in both locomotion and aVOR.

Fig. 1

Movement analysis and aVOR gain for: A) Normal chinchilla, B) chinchilla with bilateral vestibular hypofunction (lesioned) without prosthetic stimulation, C) same chinchilla after chronic constant-rate stimulation, and D) same chinchilla after chronic stimulation with modulation to head motion. Normal chinchilla exhibited normal aVOR (data from [4]) and no high frequency circling. Lesioned chinchilla initially exhibited high frequency circling, which disappeared after chronic modulation but not after chronic constant-rate stimulation. Angular VOR was absent in the lesioned chinchilla with the prosthesis powered off or with constant-rate stimulation, but was partially restored with prosthetic modulation. Asymmetry in gain is due to inherent limitations in encoding inhibitory head motions using a unilaterally-implanted prosthesis. All sinusoidal eye responses were measured at 2Hz, 100°/s in the dark. Although movements were recorded for at least 15 minutes in the dark, only a representative 1 minute sample is shown for purpose of clarity.

Fig. 2

Effects of chronic adaptation on circling and aVOR. (A) Chinchillas with bilateral vestibular hypofunction (lesioned, n=6) demonstrated higher circling frequency than normal chinchillas (n=6). Three chinchillas underwent chronic prosthetic stimulation with and without modulation to head movement (B). In two (ch105 and ch207), circling frequency improved with chronic prosthetic modulation but not with chronic constant rate stimulation. Ch108 did not improve with prosthetic modulation. VOR disconjugacy (C), gain (D), and misalignment (E) for each chinchilla were analyzed at the start (day 0) and end (day 9 or 10) of chronic modulation. Disconjugacy improved in both chinchillas that also showed decrease in circling frequency but not for ch108. Gains for all chinchillas remained nearly constant, while misalignment changes were variable.

Fig. 3

Reversion to circling after cessation of motion-modulated prosthetic stimulation was not immediate. The two chinchillas that showed improvement in circling frequency with chronic modulation, reverted to rapid circling after the prosthesis was turned off. However, a significant increase in circling frequency was not observed until 4 days after the prosthesis was powered off.