Collicular microstimulation during passive rotation does not generate fixed gaze shifts.

Abstract

We investigated whether saccades evoked by electrical stimulation (E-saccades) in the superior colliculus can compensate for passive sinusoidal head rotation in yaw so as to keep the rapid gaze shift constant. After accounting for variations in E-saccade onset position, we found significant horizontal metric changes, proportional to head velocity, in 31 of 37 experiments in 2 monkeys. Vertical effects were small. In a substantial fraction of the experiments (14/37), these metric changes represented significant but often insufficient compensatory adjustments in the horizontal component, opposite to the direction of head movement. However, very robust violations of gaze-shift constancy were remarkably common: significant anticompensatory changes in the horizontal component occurred in 17/37 experiments. In these cases, typically involving larger E-saccades, the horizontal component increased in size with rotation into the half field containing the E-saccade and became smaller during opposite rotation. Further analysis showed that, instead of showing a dichotomy, the metric effect actually varied along a continuum from compensatory to strongly anticompensatory. In addition to these metric changes, we found a robust kinematic effect of head rotation in metrically matched E-saccades. In all experiments where the effect was significant (34/37), horizontal peak velocity increased for rotation into the half field where the E-saccade was directed and decreased for opposite rotation. This kinematic effect was again proportional to head velocity and predominant in the horizontal component. Comparison of yaw and pitch rotation at the same stimulation site showed that both expressions of vestibular-saccade interaction (metric and kinematic) tended to align with the direction of rotation. The component-specific nature of the modulation suggests that the effects may have been caused by convergence of saccadic and vestibular signals at a component-coding stage downstream of the colliculus. We suggest that the quick-phase system got access to the common pulse generator as soon as the collicular stimulation had opened the pause-cell gate. Adding such an anticompensatory signal would act to increase the E-saccade horizontal component when the monkey was rotated in the same direction and bring about a decrease in size and peak velocity when it was opposite. In the large majority of experiments the metric changes failed to maintain gaze-shift constancy, either because they were in the wrong direction or because they were too small. Possible reasons for this major departure from the properties of natural gaze shifts are discussed.