Neuronal mechanisms of two-dimensional orienting movements in the cat. I. A quantitative study of saccades and slow drifts produced in response to the electrical stimulation of the superior colliculus.

To evaluate the metrics of rapid eye movements caused by the activation of distinct collicular microzones, the superior colliculus (SC) was electrically stimulated in alert behaving cats while their heads were restrained. A quantitative study of electrically induced rapid eye movements demonstrated that their amplitude and direction depended on the intensity of stimulation, the electrode location, and the initial position of the eyes, while their duration depended on the intensity of stimulation. When detailed quantitative procedures are employed, properties of saccades produced in response to the electrical stimulation of the feline SC resemble those of saccades elicited in response to the electrical stimulation of a variety of primate brain areas. Besides saccades, electrical stimulation of the feline SC gave rise to slow drifts whose amplitude and direction was also influenced by the initial position of the eyes. Because their size depended on the frequency of stimulation and their time course reflected mechanical properties of the oculomotor plant, induced slow drifts could be due to a more or less direct projection of the SC onto extraocular motoneurons. A model that includes such a variety of connections between the SC and extraocular motoneurons is presented and is shown to produce realistic combinations of fast and slow eye movements when its input is a step function of time. The present findings support the notion that an orbital mechanical factor underlies the eye position sensitivity of slow drifts and saccades evoked in response to the electrical stimulation of the SC.