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

Abstract

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 degrees/s) to 4.0 Hz ( approximately 6 degrees/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 approximately 0.8 and 0.6 in upright and 90 degrees pitch, respectively. NC animals had small aVOR gains at 0.2 Hz, and the temporal phases were shifted approximately 90 degrees 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 x 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.

Spatial Properties of Central Vestibular Neurons of Monkeys After Bilateral Lateral Canal Nerve Section

“…Movements of the left eye were recorded in three dimensions with the implanted scleral search coils. The techniques of eye movement recording have been described in detail in previous publications (Yakushin et al 1995(Yakushin et al , 1998. Yaw and pitch velocities were calibrated by rotating animals in light with a step of velocity at 30°/s about a spatial vertical axis for 30 s in each direction with the animal upright or side down.…”

“…Once the associated vertical canal was identified, animals were oscillated at 0.2 Hz around a spatial vertical axis at 60°/s either upright or tilted at 15°increments in the fore-aft direction up to 90°. The purpose of this test (test 2) was to determine whether maximal canal-related activity was significantly different from the tilt of the vertical canal plane, which is ϳ50°tilt backward (Yakushin et al 1995(Yakushin et al , 1998. We assumed that the temporal sensitivity of the recorded unit was positive when the activity increased with rotation toward the ipsilateral side and negative if activity increased during rotation toward the contralateral side.…”

“…Before operation, the spatial properties of the yaw axis aVOR were normal in these animals, with peak gains of Ϸ0.9. Yaw eye velocity was maximal close to the upright position and the yaw gains declined when the animals were tilted forward or back (Angelaki and Hess 1996;Böhmer et al 1985;Yakushin et al 1995Yakushin et al , 1998. After lateral canal nerve section, the evoked yaw eye velocities were considerably smaller than in the normal animal, with maximal gains of Ϸ0.2.…”

Tuning of gravity-dependent and gravity-independent vertical angular VOR gain changes by frequency of adaptation

“…Therefore, the spatial phase ␤ was assumed to be 90°for adaptation RSD and Ϫ90°for adaptation LSD. The significance of the fit was verified by F statistic, a reduced case of ANOVA at P Ͻ 0.05 (Yakushin et al 1998. It should be noted that gravity-dependent changes are determined as the amplitude of the fit and according to such convention are always positive regardless of whether the aVOR gain was increased or decreased.…”

Squirrel Monkeys and Space Motion Sickness

“…Otolith neurons did not respond to even intense angular accelerations [78]. In this connection, the readers should consult the elaborate experiments of canal plugging in rhesus monkeys conducted by Cohen, Suzuki and their colleagues or Highstein and his colleagues [160][161][162].…”