We examined the activity of neurons in the deep layers of the superior colliculus of awake behaving rhesus monkeys during the performance of standard oculomotor tasks as well as during self-guided eye movements made while viewing natural images. The standard tasks were used to characterize the activity of neurons based on established criteria. The natural viewing paradigm enabled the sampling of neuronal activity during saccades and fixations distributed over a wide range of eye positions. Two distinct aspects of eye-movement behavior contributed to the modulation of firing activity in these neurons. The well-established influence of saccade amplitude and direction was strongest and most prevalent surrounding the time of the start of the saccade. However, the activity of these neurons was also affected by the orbital position of the eyes, and this effect was best observed during intervals of fixation. Many neurons were sensitive to both parameters, and the directions of their saccade vector and eye position response fields tended to be aligned. The sample of neurons included visual, build-up, and burst activities, alone or in combination. All of these activity types were included in the subpopulation of neurons with significant eye-position tuning, although position tuning was more common in neurons with build-up or burst activity and less common in neurons with visual activity. The presence of both eye-position as well as saccade-vector signals in the superior colliculus is likely important for its role in the planning and guidance of combined movements of the eyes and head.
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