Spatial orientation of caloric nystagmus in semicircular canal-plugged monkeys

Abstract

We studied caloric nystagmus before and after plugging all six semicircular canals to determine whether velocity storage contributed to the spatial orientation of caloric nystagmus. Monkeys were stimulated unilaterally with cold ( approximately 20 degrees C) water while upright, supine, prone, right-side down, and left-side down. The decline in the slow phase velocity vector was determined over the last 37% of the nystagmus, at a time when the response was largely due to activation of velocity storage. Before plugging, yaw components varied with the convective flow of endolymph in the lateral canals in all head orientations. Plugging blocked endolymph flow, eliminating convection currents. Despite this, caloric nystagmus was readily elicited, but the horizontal component was always toward the stimulated (ipsilateral) side, regardless of head position relative to gravity. When upright, the slow phase velocity vector was close to the yaw and spatial vertical axes. Roll components became stronger in supine and prone positions, and vertical components were enhanced in side down positions. In each case, this brought the velocity vectors toward alignment with the spatial vertical. Consistent with principles governing the orientation of velocity storage, when the yaw component of the velocity vector was positive, the cross-coupled pitch or roll components brought the vector upward in space. Conversely, when yaw eye velocity vector was downward in the head coordinate frame, i.e., negative, pitch and roll were downward in space. The data could not be modeled simply by a reduction in activity in the ipsilateral vestibular nerve, which would direct the velocity vector along the roll direction. Since there is no cross coupling from roll to yaw, velocity storage alone could not rotate the vector to fit the data. We postulated, therefore, that cooling had caused contraction of the endolymph in the plugged canals. This contraction would deflect the cupula toward the plug, simulating ampullofugal flow of endolymph. Inhibition and excitation induced by such cupula deflection fit the data well in the upright position but not in lateral or prone/supine conditions. Data fits in these positions required the addition of a spatially orientated, velocity storage component. We conclude, therefore, that three factors produce cold caloric nystagmus after canal plugging: inhibition of activity in ampullary nerves, contraction of endolymph in the stimulated canals, and orientation of eye velocity to gravity through velocity storage. Although the response to convection currents dominates the normal response to caloric stimulation, velocity storage probably also contributes to the orientation of eye velocity.

FIG. 1.

Histological sections from left labyrinth of M9308. A–C insets: each canal (A, anterior canal; B, lateral canal, and C, posterior canal) was completely occluded by a dense bone overgrowth after plugging. Arrowheads show the borders of the canals. The hair cells of the crista in each of the canals (A–C) and the utricular macula (D), saccular macula (E), and the cochlea (F) were intact.

FIG. 2.

Method for computing orientation vectors in 3 dimensions. A and B: sample roll, pitch, and yaw eye velocities as well as the eye velocity vector magnitude as a function of time induced by left ear (A) and right ear (B) stimulation in the prone position (insert). The horizontal arrows (<——>) show the last 37% of the decaying phase of the vector (heavy black line), which was used to calculate the orientation vectors eAvL and eAvR shown in A and B. This calculation was done by determining the optimal linear fit to the trajectory in 3-dimensional eye velocity space (Raphan and Sturm 1991). C: projections of the 3-dimensional representation of data in A and B and the computed orientation vectors, eAvL and eAvR. The g vector indicates the direction of gravitational force relative in the projected plane in the prone position. The circle with a dot indicates that the acceleration of gravity is coming out of the page toward the reader.

FIG. 3.

A: presentation of head coordinate frame. Curved arrows show the direction of the positive axes of rotation, which are consistent with the right-hand rule. Also shown are the 3 semicircular canals of the left labyrinth and their orientation relative to the head frame, as well as the relationship between the lateral canal plane and the stereotaxic horizontal. B–F: examples of caloric nystagmus induced by irrigation of the left ear in a normal monkey in the upright (B), supine (C), prone (D), left-side down (E), and right-side down (F) positions, shown in the insets. Irrigation was begun at time 0 with the animal upright, and it was continued for 15 s. At the end of stimulation, the animal was moved to the test position, and the lights were extinguished. Positive directions for each of the components of eye velocity were clockwise (CW) relative to the animal for roll, down for pitch, and left for yaw.

FIG. 4.

A: left labyrinth, looking slightly downward and forward from the left side. Approximate sites of plugging in the canals are stained in black. Arrows adjacent to the ampullae show the directions of cupula deflection that are postulated to occur from contraction of endolymph between canal plug and cupula due to cooling. B–F: examples of caloric nystagmus in the monkey of Fig. 3 after all 6 canals were plugged. The monkey was upright (B), supine (C), prone (D), left-side down (E), and right-side down (F) as shown in insets. Stimuli and scheme are the same as in Fig. 3. Note that the horizontal component was to the left, the side of stimulation, in every head position. Note also the prominent CCW roll component in prone (D) and the prominent vertical component in the left- (E) and right- (F) side down positions.

FIG. 5.

Two-dimensional projections in the yaw/roll (1) and the yaw/pitch (2) planes showing the orientation vectors of caloric nystagmus in the upright (A), supine (B), prone (C), left-side down (D), and right-side down position (E) in the 6-canal plugged animals. Trajectories of the decaying phases of the caloric vectors were plotted in gray for left ear stimulation and in black for right ear stimulation. Insets on the left show head positions and head coordinate axes in the spatial frame, and the g in each graph indicates the direction of gravitational force. The caloric vectors were normalized so that the length of the vector at the culmination of the caloric response was 1. The 3 × 1 matrices (3) of the averaged orientation vector for the left ear (ê_avL) and the right ear (ê_avR) for data shown in 1 and 2. Note that responses from the left and right ear stimulation were symmetrical, and yaw components were dominant in the upright position (A), roll components in the supine (B) and prone (C) positions, and pitch in the left-side down (D) and right-side down positions (E). A circle with a dot indicates that the acceleration of gravity is coming out of the page while a circle with an x indicates the acceleration of gravity is into the page.

FIG. 6.

1 and 2: 2-dimensional projections and the orientation vectors of caloric nystagmus in 5 normal animals in the upright (A), supine (B), prone (C), left-side down (D), and right-side down (E) positions. Scheme as in Fig. 5. The 3 × 1 matrices (3) of the averaged orientation vector for the left ear (ê_avL) and the right ear (ê_avR) for data shown in 1 and 2. Predominant velocity was along the z (head-vertical or yaw) axis and earth-vertical axis as in all canal-plugged animals.

FIG. 7.

Model predictions of eye velocity induced by cold caloric stimulation of the left ear in the upright (A and B), left-side down (C), right-side down (D), supine (E), and prone (F) positions. Vectors are shown in 3 dimensions in a head coordinate frame with the position of the animal’s head, and the coordinate axes shown by insets. The open arrows, x, y, z, show the positive directions of the spatial roll, pitch, and yaw axes, respectively, which are also shown on the heads of the animals in insets. Circles and dots show axes that project directly out of the picture, while axes that project into the page are shown by x’s enclosed in circles. In each case, an upward arrow shows the acceleration of gravity (a_g), which is also the direction of orientation of velocity storage. The orientation of the lateral (lat), anterior (ant), and posterior (post) canals are shown by their normals, and perpendicular dashes across the normals are the relative activations of each canal by the caloric stimulation. Viewed from the side, anterior and posterior canal normals overlay each other, but in A, B, E, and F, the anterior canals project 45° out of the page and the posterior canals 45° into the page. These normals have been offset slightly to show the anterior (gray) and posterior (black) normals. The basis for this is the model developed by Yakushin et al. (1998). “Actual Eye Velocity” is the average eye velocity vector obtained from the matrices for left ear stimulation shown in Fig. 5(3). “Eye Velocity 1” is the predicted eye velocity for canal nerve inhibition. “Eye Velocity 2” is the sum of “Eye Velocity 1” and contraction of the endolymph due to cooling. The vector “Eye Velocity 1” was only shown in A, since it would not be altered for any other position and was not used in the comparison with the “Actual Eye Velocity.” Only “Eye Velocity 2” was used for this comparison, and it was depicted in each of the figures parts (B–F). For the side down and supine/prone positions, the contribution of velocity storage was necessary to shift the vector from “Eye Velocity 2” to the “Actual Eye Velocity.” See text for details.