Journal of Neurophysiology

Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement

D. L. Robinson, R. H. Wurtz

Abstract

1. In order to see whether cells in the superficial layers of the monkey superior colliculus can differentiate between real stimulus movement and self-induced stimulus movement we compared the discharge of these cells to stimulus movement in front of the stationary eye with stimulus movement generated by eye movements across a stationary stimulus. 2. Most of the cells recorded (65% of 231 cells) responded to stimulus velocities in front of the stationary eye as fast as those occurring during the peak velocity of a saccadic eye movement. Those cells that do respond usually have weak inhibitory regions and tend to have receptive fields further from fovea. 3. Move (61% of 105 cells) of the cells that did respond to rapid stimulus movement did not respond when an eye movement swept the receptive field over a stationary stimulus. 4. About half of these cells differentiated between these stimulus conditions when we used stimuli at least 1 log unit above background illumination; the remaining cells differentiated for stimuli 2 and 3 log units above background. Many cells differentiated between the two stimulus conditions over a wide range of directions of movement and the effect appears with about equal frequency in receptive fields at all distances from the fovea. 5. The differentiation is present for most cells even when the background illumination is reduced, indicating that visual factors are not the cause of the effect on these cells but may modify the response of other cells. 6. The suppression of background activity accompanying eye movements in the light is present following eye movements made in total darkness; the suppression, therefore, must result from an extraretinal signal. 4. The failure of these cells to respond to visual stimulation during eye movements is due to the same extraretinal signal that produces the suppression since a) the cells that show this suppression tend to be those that fail to respond to stimuli during eye movements, b) the time course of the suppression matches the time at which the effects of visual stimulation during an eye movement would reach the colliculus, and c) the cells which differentiate also show a decreased responsiveness to visual stimulation during the time of background suppression. While this extraretinal signal has the characteristics one would expect of a corollary discharge, proprioception as a source of the signal cannot be excluded. 8. Cells which differentiate between the two stimulus conditions usually also show an enhanced response to a visual stimulus in their receptive field when it is to be the target for a saccadic eye movement. These cells in the superior colliculus receive an extraretinal input which permits them to differentiate betweent real stimulus movements and stimulus movements resulting from the monkey's own eye movements. This differentiation would provide an uncontaminated visual movement signal and facilitate the detection of real movement in the environment...