Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes
Peter J. Boutros, … , Andreas Jaeger, Charles C. Della Santina
Peter J. Boutros, … , Andreas Jaeger, Charles C. Della Santina
Published November 14, 2019
Citation Information: JCI Insight. 2019;4(22):e128397. https://doi.org/10.1172/jci.insight.128397.
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Clinical Medicine Neuroscience Otology

Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes

Abstract

BACKGROUND Bilateral loss of vestibular (inner ear inertial) sensation causes chronically blurred vision during head movement, postural instability, and increased fall risk. Individuals who fail to compensate despite rehabilitation therapy have no adequate treatment options. Analogous to hearing restoration via cochlear implants, prosthetic electrical stimulation of vestibular nerve branches to encode head motion has garnered interest as a potential treatment, but prior studies in humans have not included continuous long-term stimulation or 3D binocular vestibulo-ocular reflex (VOR) oculography, without which one cannot determine whether an implant selectively stimulates the implanted ear’s 3 semicircular canals.METHODS We report binocular 3D VOR responses of 4 human subjects with ototoxic bilateral vestibular loss unilaterally implanted with a Labyrinth Devices Multichannel Vestibular Implant System vestibular implant, which provides continuous, long-term, motion-modulated prosthetic stimulation via electrodes in 3 semicircular canals.RESULTS Initiation of prosthetic stimulation evoked nystagmus that decayed within 30 minutes. Stimulation targeting 1 canal produced 3D VOR responses approximately aligned with that canal’s anatomic axis. Targeting multiple canals yielded responses aligned with a vector sum of individual responses. Over 350–812 days of continuous 24 h/d use, modulated electrical stimulation produced stable VOR responses that grew with stimulus intensity and aligned approximately with any specified 3D head rotation axis.CONCLUSION These results demonstrate that a vestibular implant can selectively, continuously, and chronically provide artificial sensory input to all 3 implanted semicircular canals in individuals disabled by bilateral vestibular loss, driving reflexive VOR eye movements that approximately align in 3D with the head motion axis encoded by the implant.TRIAL REGISTRATION ClinicalTrials.gov: NCT02725463.FUNDING NIH/National Institute on Deafness and Other Communication Disorders: R01DC013536 and 2T32DC000023; Labyrinth Devices, LLC; and Med-El GmbH.

Authors

Peter J. Boutros, Desi P. Schoo, Mehdi Rahman, Nicolas S. Valentin, Margaret R. Chow, Andrianna I. Ayiotis, Brian J. Morris, Andreas Hofner, Aitor Morillo Rascon, Andreas Marx, Ross Deas, Gene Y. Fridman, Natan S. Davidovics, Bryan K. Ward, Carolina Treviño, Stephen P. Bowditch, Dale C. Roberts, Kelly E. Lane, Yoav Gimmon, Michael C. Schubert, John P. Carey, Andreas Jaeger, Charles C. Della Santina

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Figure 1

Coplanar pairs of semicircular canals in the vestibular labyrinths encode 3D head rotational velocity in 3 mutually orthogonal components.

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Coplanar pairs of semicircular canals in the vestibular labyrinths encod...
Relative levels of activity within vestibular nerve branches innervating a labyrinth’s 3 semicircular canals encode 3 mutually orthogonal canal-aligned components of the head rotational velocity’s 3D axis. The vestibulo-ocular reflex (VOR) drives eye rotations that counteract head rotation to keep images stable on the retinae. (A) Pairs of coplanar canals normally encode 3 linearly independent components of head rotational velocity about axes perpendicular to the left horizontal (LH) and right horizontal canals (LHRH or +z axis), left anterior and right posterior canals (LARP), and right anterior and left posterior canals (RALP). By convention, positive rotations denote right-hand rule rotations as shown by black arrows. Each canal is most sensitive to rotation about an axis approximately perpendicular to its anatomic plane. (B–D) Head rotations about canal axes that excite the LA, LH, and LP canal, respectively, normally drive VOR responses that rotate both eyes in the opposite direction about the LARP, LHRH, and RALP axes. Physiologically excitatory directions (shown by gold arrows) are not always positive by the right-hand rule mathematical convention. (E) Head rotation about an arbitrary axis excites or inhibits each canal according to a cosine dependence on the angle between the axis of head rotation and the canal’s anatomic axis. (F) Relative activity on the 3 canals in each labyrinth (and their coplanar partners in the other ear) normally drives a VOR response that helps keep images of Earth-stationary objects stable on the retinae. Without the VOR, image slip on the retinae degrades vision during quick head rotations. Although most studies of the VOR measure and describe only yaw (z/LHRH in panel A, also called “horizontal”) and/or pitch (y/PITCH, also called “vertical”) components, all 3 components of the 3D VOR are required to maintain stable vision, and measurement of all 3 components is required to accurately estimate the relative levels of activity on each of a labyrinth’s 3 semicircular canals. Reproduced by permission from Labyrinth Devices, LLC, ©2019.