Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position.

Abstract

Monkeys [Macaca mulatta and M. nemestrina] were trained to look to brief visual targets presented in a completey darkened room. On some trials, after the visual target disappeared but before a saccade to the target could be initiated, the eyes were driven to another position in the orbit by electrical stimulation of the superior colliculus. Retinocentric models of the saccadic system predict that a saccade with a predetermined distance and direction based entirely on retinal error will occur. If this were the case, gaze would miss the target location by a distance and direction equal to the vector of the stimulation-induced movement. Spatial models assume that the retinal error signal will be combined with information about the change in eye position produced by stimulation and predict that the animal will look to the position of the target in space. Results confirm the predictions of spatial models. Animals compensated for the stimulation-induced perturbation by looking to the position of the target in space. The result predicted by retinocentric models (a saccade with a direction and amplitude based on retinal error alone) was never observed. The eye movement that compensated for the change in eye position produced by stimulation was a saccade, not a passive, low velocity movement to an orbital position of mechanical equilibrium established by a tonic pattern of motoneuron activation specified by the visual target. This indicates that a new saccade command, based on stored information about the location of the retinal image and information about the new position of the eyes, had been issued. Computation of the vector of the compensatory saccade does not necessarily increase the latency of target acquisition. The interval between the end of a stimulation-induced saccade and the beginning of the compensatory saccade was frequently 20 ms or less, permitting the animal to acquire the target with a normal latency. Compensatory movements to the remembered location of the target were less accurate than movements to a continuously illuminated target. The reduction in accuracy is attributed to nonveridical spatial memory and eye-position signals, but precise estimates of the magnitude of the error attributable to each of these sources were not obtained. Fixation of a visual target significantly increased the threshold for producing saccades by collicular stimulation. The amplitude of saccades evoked by suprathreshold currents was reduced if stimulation occurred during fixation. Evidently, fixation is more than the mere absence of saccade commands and that an active process prevents saccades during fixation. If stimulation occurred prior to a saccade to a visual target, the vector of the stimulation-induced saccade was affected by the position of the visual target. Changes in the horizontal position of the target affected the horizontal component of the stimulation-induced saccade, and changes in the vertical position of the target affected the vertical component. The magnitude of the interaction affect was a function of the interval between target onset and stimulation onset. Results are consistent with existing models of the saccadic system that assume that saccades are controlled by a local feedback circuit in the pontine reticular formation.