SEMICIRCULAR CANAL CONTRIBUTIONS TO THE 3-DIMENSIONAL VESTIBULOOCULARREFLEX - A MODEL-BASED APPROACH

1. We studied the contribution of the individual semicircular canals t o the generation of horizontal and torsional eye movements in cynomolg us monkeys. Eye movements were elicited by sinusoidal rotation about a vertical (gravitational) axis at 0.2 Hz with the animals tilted in va rious attitudes of static forward or backward pitch. The gains of the horizontal and torsional components of the vestibuloocular reflex (VOR ) were measured for each tilt position. The gains as a function of til t position were fit with sinusoidal functions, and spatial gains and p hases were determined. After control responses were recorded, the semi circular canals were plugged, animals were allowed to adapt, and the t est procedure was repeated. Animals were prepared with only the anteri or and posterior canals intact [vertical canal (VC) animals], with onl y the lateral canals intact [lateral canal(LC) animal], and with only one anterior and the contralateral posterior canals intact [right ante rior and left posterior canal (RALP) animals; left anterior and right posterior canal (LARP) animals]. 2. In normal animals, the gain of the horizontal (yaw axis) velocity of the compensatory eye movements decr eased as they were pitched forward or backward, and a torsional veloci ty appeared, reversing phase at the peak of the horizontal gain. After the anterior and posterior canals were plugged (LC animal), the horiz ontal component was reduced when the animal was tilted backward; the g ain was zero with about -60 degrees of backward tilt. The spatial phas e of the torsional component had the same characteristics. This is con sistent with the fact that both responses were produced by the lateral canals, which from our results are tilted between 28 and 39 degrees a bove the horizontal stereotaxic plane. 3. After both lateral canals we re plugged (VC animals), horizontal velocity was reduced in the uprigh t position but increased as the animals were pitched backward relative to the axis of rotation. Torsional velocities, which were zero in the upright position in the normal animal, were now 180 degrees out of ph ase with the horizontal velocity. The peak values of the horizontal an d torsional components were significantly shifted from the normal data and were closely aligned with each other, reaching peak values at app roximately -56 degrees pitched back (-53 degrees horizontal, -58 degre es torsional). The same was true for the LARP and RALP animals; the pe ak values were at -59 degrees pitched back (-55 degrees horizontal, -6 2 degrees torsional). Likewise, in the LC animal the peak yaw and roll gains occurred at about the same angle of forward tilt, 35 degrees (3 0 degrees horizontal, 39 degrees torsional). Thus, in each case, the c anal plugging had transformed the VOR from a compensatory to a directi on-fixed response with regard to the head. Therefore there was no adap tation of the response planes of the individual canals after plugging. 4. The data were compared with eye velocity predictions of a model ba sed on the geometric organization of the canals and their relation to a head coordinate frame. The model used the normal to the canal planes to form a nonorthogonal coordinate basis for representing eye velocit y. An analysis of variance was used to define the goodness of fit of m odel predictions to the data. Model predictions and experimental data agreed closely for both normal animals and for the animals with canal lesions. Moreover, if horizontal and roll components from the LC and V C animals were combined, the summation overlay the response of the nor mal monkeys and the predictions of the model. In addition, a combinati on of the RALP and LARP animals predicted the response of the lateral- canal-plugged (VC) animals. 5. When operated animals were tested in li ght, the gains, peak values, and spatial phases of horizontal and roll eye velocity returned to the preoperative values, regardless of the t ype of surgery performed. This indicates that vision compensated for t he lack of spatial adaptation of the response planes after plugging. I t converted a noncompensatory, direction-fixed response with regard to the head to an appropriate compensatory response. 6. These results in dicate that both the vertical and lateral canals contribute a horizont al and torsional component to the VOR in the monkey according to the v ector projection of head velocity onto the normals of the individual c anals. The individual components can be predicted according to the pos ition of the canals in the head with regard to the plane of rotation. The nonorthogonality of the canal planes must be considered when predi cting canal activation of eye movements in response to rotation around any axis.