Vestibulo-ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment

Abstract

There is no effective treatment available for individuals unable to compensate for bilateral profound loss of vestibular sensation, which causes chronic disequilibrium and blurs vision by disrupting vestibulo-ocular reflexes that normally stabilize the eyes during head movement. Previous work suggests that a multichannel vestibular prosthesis can emulate normal semicircular canals by electrically stimulating vestibular nerve branches to encode head movements detected by mutually orthogonal gyroscopes affixed to the skull. Until now, that approach has been limited by current spread resulting in distortion of the vestibular nerve activation pattern and consequent inability to accurately encode head movements throughout the full 3-dimensional (3D) range normally transduced by the labyrinths. We report that the electrically evoked 3D angular vestibulo-ocular reflex exhibits vector superposition and linearity to a sufficient degree that a multichannel vestibular prosthesis incorporating a precompensatory 3D coordinate transformation to correct misalignment can accurately emulate semicircular canals for head rotations throughout the range of 3D axes normally transduced by a healthy labyrinth.

FIG. 1

A Precompensatory 3D remapping improves both axis and amplitude of prosthesis-encoded head velocity percept. Column 1 Mean head and eye velocity for a normal chinchilla during 50°/s peak 2-Hz whole body rotations in darkness about the axis of each coplanar pair of semicircular canals (SCC): horizontal (top row), left anterior/right posterior (LARP, middle row), and right anterior/left posterior (RALP, bottom row). For clarity, only mean responses are shown; the standard deviation for each trace was <6°/s. Eye traces are inverted to compare with head. Normal chinchillas exhibit good alignment with head rotation axis and symmetric gain (eye velocity/head velocity) of about 0.5 (data from Della Santina et al. 2007). Dashed curves indicate mean responses for all animals studied. Column 2 aVOR responses for chinchillas treated with intratympanic gentamicin (ITG) in one ear are attenuated during ipsilesional rotation. Column 3 Head rotation of a bilaterally vestibular-deficient animal (ch207) after ITG and canal plugging elicits no response for any axis when prosthesis is off. Column 4 Responses for the same animal when pulse rates on individual electrodes implanted in the left labyrinth SCCs are modulated without precompensatory 3D remapping. Misalignment due to current spread is evident for all three axes of rotation. Column 5 aVOR responses of the same animal to stimuli with precompensatory 3D remapping are like those of animals with a single working labyrinth (column 2). B 3D aVOR responses to prosthetic stimuli encoding head rotation about each of the three SCC axes without (B1) and with (B2) precompensatory 3D remapping for each of four implanted animals.

FIG. 2

Amplitude of best-fit whole cycle sinusoid velocity of aVOR response to stimuli delivered on an electrode near the horizontal (A), anterior (B), and posterior (C) semicircular canals of the left labyrinth in each of four chinchillas. Velocity varies almost linearly with stimulus intensity (pulse frequency depth of modulation as defined in text). R² > 0.93 for linear fit in each case.

FIG. 3

When precompensatory 3D remapping is employed, axis and speed of observed aVOR eye rotation responses align better with desired responses for virtual head rotations about any 3D axis as compared to the responses to uncompensated rotations. A Desired and actual eye velocity for 16 different directions tested prior to precompensation, each at 2 Hz and 50% stimulus intensity (SI, defined in text). Axis and speed are represented by orientation and length, respectively, of plotted vectors. Dashed lines define a head-based coordinate system comprising the horizontal, left anterior/right posterior (LARP) and right anterior/left posterior (RALP) axes; the length of each denotes 50°/s peak head velocity which would evoke an eye velocity of approximately 25°/s in a normal chinchilla. B Results for the same 16 desired rotations after precompensation (again 2 Hz, desired peak velocity 25°/s). Thick lines indicate error between response and stimulus. Errors are significantly smaller after precompensation. C Misalignment (angle between desired and actual eye rotation axis) for each of the 65 virtual head rotations tested without precompensation. Azimuth and elevation of each axis is as defined in B. D Misalignment is significantly smaller after precompensation. E, F Peak velocity for same cases as in C and D. Responses to precompensated stimuli are significantly closer to the desired velocity of 25°/s.

FIG. 4

A Misalignment angle for aVOR responses to prosthetic input is less with precompensation than without and smallest for high velocity head rotation. B The relationship between desired and observed aVOR responses with precompensation clusters around equality for all four implanted animals. C As for normal animals (Della Santina et al. 2007), a high-pass characteristic is noted for each animal’s aVOR response as a function of the modulation frequency encoding virtual 50°/s head rotations.