Dynamics and Kinematics of the Angular Vestibulo-Ocular Reflex in Monkey: Effects of Canal Plugging

Abstract

Yakushin, Sergei B., Theodore Raphan, Jun-Ichi Suzuki, Yasuko Arai, and Bernard Cohen. Dynamics and kinematics of the angular vestibulo-ocular reflex in monkey: effects of canal plugging. J. Neurophysiol. 80: 3077–3099, 1998. Horizontal and roll components of the angular vestibulo-ocular reflex (aVOR) were elicited by sinusoidal rotation at frequencies from 0.2 Hz (60°/s) to 4.0 Hz (≈6°/s) in cynomolgus monkeys. Animals had both lateral canals plugged (VC, vertical canals intact), both lateral canals and one pair of the vertical canals plugged (RALP, right anterior and left posterior canals intact; LARP, left anterior and right posterior canal intact), or all six semicircular canal plugged (NC, no canals). In normal animals, horizontal and roll eye velocity was in phase with head velocity and peak horizontal and roll gains were ≈0.8 and 0.6 in upright and 90° pitch, respectively. NC animals had small aVOR gains at 0.2 Hz, and the temporal phases were shifted ≈90° toward acceleration. As the frequency increased to 4 Hz, aVOR temporal gains and phases tended to normalize. Findings were similar for the LARP, RALP, and VC animals when they were rotated in the planes of the plugged canals. That is, they tended to normalize at higher frequencies. A model was developed incorporating the geometric organization of the canals and first order canal-endolymph dynamics. Canal plugging was modeled as an alteration in the low frequency 3-db roll-off and corresponding dominant time constant. The shift in the low-frequency 3-dB roll-off was seen in the temporal responses as a phase lead of the aVOR toward acceleration at higher frequencies. The phase shifted toward stimulus velocity as the frequency increased toward 4.0 Hz. By incorporating a dynamic model of the canals into the three-dimensional canal system, the spatial responses were predicted at all frequencies. Animals were also stimulated with steps of velocity in planes parallel to the plugged lateral canals. This induced a response with a short time constant and low peak velocity in each monkey. Gains were normalized for step rotation with respect to time constant as (steady state eye velocity)/(stimulus acceleration × time constant). Using this procedure, the gains were the same in canal plugged as in normal animals and corresponded to gains obtained in the frequency analysis. The study suggests that canal plugging does not block the afferent response to rotation, it merely shifts the dynamic response to higher frequencies.