Normalization Effects of Vision on the Compensatory VOR after Canal Plugging

The vestibulo-ocular reflex (VOR) combines with vision to compensate for head movement in light. Vision can also adapt the VOR during long-term visual-vestibular conflict. How vision might modify the VOR after inactivation of individual semicircular canal pairs is unknown and was studied by recording eye movements during sinusoidal rotation in light and in darkness before and after canal plugging.

Experiments were performed on six cynomolgus monkeys (Macaca fasciculuris) that had individual canals plugged. In two animals, the lateral canals were plugged (VC animals), and in four animals only one anterior and the contralateral posterior canals were intact (LARP-RALP animals). The techniques and methods of collection and analysis of data have been described in detail elsewhere.^1–3 Animals were sinusoidally rotated for 10 cycles at 0.2 Hz, peak velocity 60°/sec, about a spatial vertical axis while tilted in 10° increments forward or backward in pitch up to 90°. Horizontal, vertical, and torsional eye movements were recorded with search coils implanted on one eye. The gain was defined as the peak-to-peak eye velocity divided by peak-to-peak head velocity for the individual cycle of rotation (Fig. 1). Mean gains as a function of a tilt angle are shown in the graphs of Figure 2 (spatial curves).

FIGURE 1.

Horizontal (Ḣ), vertical ($\dot{\mathbf{\text{V}}}$) and roll (Ṙ) eye velocity of an animal before and after surgery duringsinusoidal rotation about avertical axis (St, stimulus) in darkness at a frequency of 0.2 Hz with a peak velocity ±60°/sec. (A) When the animal was upright before surgery, its eye velocity was predominantly horizontal. (B) After both lateral canals and the left anterior, right posterior, or right anterior and left posterior canals were plugged (RALP animal), rotation in dark while upright induced only small horizontal, vertical, and torsional velocities. (C) During the same rotation in light, however, the response was close to the preoperative response in darkness.

FIGURE 2.

Averaged gains as a function of head tilt of the yaw and roll components from normal (E, G) and from canal-plugged monkeys who were tested in darkness (A–D) and in light (F, H). (A, C) Two monkeys had both lateral canals plugged. (B, D) Four monkeys had both lateral canals and one anterior and the contralateral posterior canal plugged. The circles represent mean value of the horizontal eye velocities; triangles, mean value of the torsional velocities. Filled symbols are value obtained after surgery; unfilled before surgery. Solid lines are the model prediction for the data. Dashed fines are the best sinusoidal fits. The data were not fitted in F and H. In these graphs, the dashed line represents the best fit for the normal data in E and G. Negative values on the ordinate axis represent gains of eye velocities that were in phase with the stimulus. Arrows point to the tilt position with maximal gain response. The inserts below show head positions corresponding to the graphs above.

When normal animals were rotated in darkness in the upright position (Fig. 1A), the induced eye velocities were predominantly horizontal. When the animals were tilted forward or backward, the horizontal component decreased, and the torsional component increased (Fig. 2E, G). The maximal gains of the horizontal (0.87) and torsional (0.52) components were calculated from the best sinusoidal fit through the spatial curves (Fig. 2). For normal monkeys, the maximal horizontal gain occurred when the animals were tilted forward by 11° (spatial phase). Torsional gain was zero in the upright position (2° tilt backward).

In VC animals, spatial curves of the horizontal and torsional components had maxima when the animals were tilted backward 52° and 58°, respectively, with peak gains of 0.43 for horizontal and 0.44 for the torsional components (Fig. 2A, C). The horizontal gains of VC animals agreed with previous finding⁴. In LARP-RALP animals, the horizontal and torsional gain peaked at 0.29 when the animals were tilted backward 54° and 61°, respectively (Fig. 2B, D). In contrast to normal animals, the spatial phases of the horizontal and torsional components were 180° out of phase with each other in the plugged animals. Therefore, the horizontal⁵ and torsional components of the VOR recorded in darkness after surgery were anticompensatory at some tilt angles.

The data were compared (p < 0.05) to a model that projects the head velocity vector onto the normals of the canals according to the rotation of the canal plane within the head frame. It was assumed that each canal pair contributes independently to the eye movement response. The parameters of the model were taken from the normal data with the assumption that anterior, posterior, and lateral canals contribute equally to the roll and horizontal VOR, and that only the anterior and posterior canals contribute to the vertical VOR. The goodness of fit between the data and the model predictions were evaluated using an F statistic³. The model predicted the experimental data for the normal (Fig. 2E, G), the VC (Fig. 2A, C), and the LARP-RALP (Fig. 2B, D) animals without changes in parameters.

In each of the animals after canal plugging, vision caused the spatial phases to return to those recorded in the normal animals in darkness (Fig. 2F, H). The maximal horizontal gain for canal-plugged animals in light occurred at 10° forward and gains of 0.60 occurred for roll at 90° tilt forward. This can be compared to the data from the normal animals (p < 0.05).

These results indicate that both the vertical and lateral canals contribute a horizontal and torsional component to the VOR in the monkey according to the vector projection of head velocity onto the normals of the individual canals. The innate coordinate frame with regard to the head is not altered in adult animals by lesions of the individual canals. When the operated animals were tested in light, the gains, peak values, and spatial phases of eye velocity returned to the preoperative values, regardless of the type of surgery performed. Therefore, vision compensates for the lack of spatial adaptation of the response planes after peripheral lesions, converting a noncompensatory, direction-fixed response with regard to the head to an appropriate compensatory response.