NEURONS IN THE MONKEY SUPERIOR COLLICULUS PREDICT THE VISUAL RESULT OF IMPENDING SACCADIC EYE-MOVEMENTS

1. Previous experiments have shown that visual neurons in the lateral intraparietal area (LIP) respond predictively to stimuli outside their classical receptive fields when an impending saccade will bring those stimuli into their receptive fields. Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demo nstrate similar predictive responses in the monkey colliculus. 2. We s tudied the behavior of 90 visually responsive neurons in the superfici al and intermediate layers of the superior colliculus of two rhesus mo nkeys (Macaca mulatta) when visual stimuli or the locations of remembe red stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells respo nded predictively before a saccade outside the movement field of the n euron when that saccade would bring the location of a stimulus into th e receptive field. Each of these neurons did not respond to the stimul us unless an eye movement brought it into its receptive field, nor did it discharge in association with the eye movement unless it brought a stimulus into its receptive field. 4. These neurons were located in t he deeper parts of the intermediate layers and had relatively larger r eceptive fields and movement fields than the cells at the top of the i ntermediate layers. 5. The predictive responses of most of these neuro ns (16/18, 89%) did not require that the stimulus be relevant to the m onkey's rewarded behavior. However, for some neurons the predictive re sponse was enhanced when the stimulus was the target of a subsequent s accade into the neuron's movement field. 6. Most neurons with predicti ve responses responded with a similar magnitude and latency to a conti nuous stimulus that remained on after the saccade, and to the same sti mulus when it was only flashed for 50 ms coincident with the onset of the saccade target and thus never appeared within the cell's classical receptive field. 7. The visual response of neurons in the intermediat e layers of the colliculus is suppressed during the saccade itself. Ne urons that showed predictive responses began to discharge before the s accade, were suppressed during the saccade, and usually resumed discha rging after the saccade. 8. Three neurons in the intermediate layers r esponded tonically from stimulus appearance to saccade without a presa ccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelev ant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would be brought into their receptive fie lds by a saccade. This suggests that such responses will also not be f ound in the retina and striate and early prestriate visual cortex, whi ch are the major sources of visual input to these layers. 10. For both superficial and intermediate layer neurons, the response to a stimulu s flashed in the receptive field was stronger than the response of the neuron to the same stimulus brought into the receptive held by an eye movement (the reafferent response). 11. We suggest that the predictiv e response is caused by a transient shift in the retinal receptive fie ld of the neuron, effected by a neural discharge corollary to the impe nding saccade. This mechanism enables the visual input to the saccadic system to compensate for eye movements and maintain a spatially accur ate retinotopic representation of the visual world.