Spatial and temporal properties of eye movements produced by electrical stimulation of semicircular canal afferents

Abstract

To investigate the characteristics of eye movements produced by electrical stimulation of semicircular canal afferents, we studied the spatial and temporal features of eye movements elicited by short-term lateral canal stimulation in two squirrel monkeys with plugged lateral canals, with the head upright or statically tilted in the roll plane. The electrically induced vestibuloocular reflex (eVOR) evoked with the head upright decayed more quickly than the stimulation signal provided by the electrode, demonstrating an absence of the classic velocity storage effect that improves the dynamics of the low-frequency VOR. When stimulation was provided with the head tilted in roll, however, the eVOR decayed more rapidly than when the head was upright, and a cross-coupled vertical response developed that shifted the eye's rotational axis toward alignment with gravity. These results demonstrate that rotational information provided by electrical stimulation of canal afferents interacts with otolith inputs (or other graviceptive cues) in a qualitatively normal manner, a process that is thought to be mediated by the velocity storage network. The observed interaction between the eVOR and graviceptive cues is of critical importance for the development of a functionally useful vestibular prosthesis. Furthermore, the presence of gravity-dependent effects (dumping, spatial orientation) despite an absence of low-frequency augmentation of the eVOR has not been previously described in any experimental preparation.

Fig. 1.

Normal and prosthesis-mediated vestibuloocular reflexes (VORs) measured in the dark and with the head upright. Head motion stimuli (bottom, solid lines) were velocity steps from 0 to 80°/s. Top: the VOR response in the normal monkeys. Middle: the prosthesis-driven VOR response, which was measured after 30 min of tonic electrical stimulation of 1 lateral canal ampullary nerve with the animal stationary. Although the motion-modulated prosthesis stimulation was filtered with a time constant of 5 s to approximate normal cupular dynamics (bottom, dashed lines), the prosthesis-mediated VOR decayed more rapidly than the input signal in both monkeys while the normal VOR decayed more slowly than the input signal. All eye movement traces in this and subsequent figures follow the right-hand rule, with positive values representing leftward or downward eye movements.

Fig. 2.

Electrically induced VOR (eVOR) responses produced by electrical stimulation of 1 lateral canal ampullary nerve with the monkeys stationary and in the dark. The animals were either upright or tilted in the roll plane toward the right-ear-down position by 30° (monkey R) or 45° (monkey S). The electrical stimulation consisted of a step increase (200 → 367 Hz, monkey R) or decrease (250 → 26 Hz, monkey S) from the tonic level of stimulation provided by the prosthesis, which decayed with a time constant of 80 s. H, horizontal; V, vertical.

Fig. 3.

Spatial characteristics of representative eVOR responses (monkeys R and S) and the postrotational tilt responses in a normal monkey. Quick phases have been removed from all data, and eye velocity is plotted in head-centered coordinates, with horizontal velocity on the y-axis and vertical velocity on the x-axis. The orientation of the Earth-vertical relative to the head is indicated by the arrows, and the peak axis shift is indicated by the lines. Head tilt angles were 30° (monkey R), 45° (monkey S), and 32° (normal monkey).

Fig. 4.

Slow-phase eye movement responses produced by electrical stimulation (left and center) and a standard postrotational tilt paradigm in a normal monkey (right). Each plot includes responses with the head upright (solid lines) and tilted (dashed lines) and the [upright − tilted] difference (dotted lines). Total eye velocity in the frontal plane is calculated with the approach described in methods. Bottom: the electrical stimulation provided by the prosthesis in monkeys R and S (step change followed by a decay to baseline with an 80-s time constant) and the approximate change in lateral canal afferent firing in a normal squirrel monkey subjected to a 160°/s velocity step (estimated from Goldberg and Fernandez 1971).

Fig. 5.

Slow-phase eVOR responses, [upright − tilted] difference, for both stimulated monkeys. Traces represent the mean (dark lines) ± SE and are calculated from 6 upright and tilted trials for each monkey.