Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements

Abstract

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 demonstrate similar predictive responses in the monkey colliculus. 2. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. Each of these neurons did not respond to the stimulus 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 the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. 5. The predictive responses of most of these neurons (16/18, 89%) did not require that the stimulus be relevant to the monkey's rewarded behavior. However, for some neurons the predictive response was enhanced when the stimulus was the target of a subsequent saccade into the neuron's movement field. 6. Most neurons with predictive responses responded with a similar magnitude and latency to a continuous stimulus that remained on after the saccade, and to the same stimulus 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 intermediate layers of the colliculus is suppressed during the saccade itself. Neurons that showed predictive responses began to discharge before the saccade, were suppressed during the saccade, and usually resumed discharging after the saccade. 8. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelevant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would not be brought into their receptive fields by a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

Transsaccadic memory of position and form

“…The receptive fields are large, however, and would not be able to hold details of the features of a reference objects. Similar properties have been reported from neurons in the superior colliculus (Walker et al, 1995).…”

Computational models of spatial updating in peri-saccadic perception

“…Such predictive responses have been reported in the LIP area [36][37][38], the SC [39], the FEF [40,41] and even earlier areas like V3 and V3A [42]. Neurons in some of these areas show an increase in responsiveness at the future receptive field accompanied by a decrease in sensitivity at the present receptive field [38,42].…”

Modeling functions of striatal dopamine modulation in learning and planning

“…Neural recording studies during saccadic eye movement tasks report direct evidence for this postulated phenomenon. Sensory and sensorimotor neural activity in frontal eye fields (Goldberg & Bruce 1990;Umeno & Goldberg 1997), superior colliculus (Walker et al 1995), and lateral intraparietal area (Duhamel et al 1992), striate and extrastriate cortex (Nakamura and Colby, 1999) anticipates the retinal consequences of saccades about 100 msec before these saccades are elicited. The saccade preparationdependent transformation of these receptive fields has been proposed to occur in frontal eye fields (Goldberg and Bruce, 1990) or in lateral intraparietal area (Dominey and Arbib, 1992).…”

“…Planning was simulated with Actor-Critic models for which the action selection of the Actor is guided by transient influences of the Critic (Sutton and Barto, 1981). Since dopamine bursts transiently influence striatal activity (Gonon, 1997) and dopamine is involved in planning tasks (Wallesch et al, 1990;Salamone, 1992;Lange et al, 1992;Talor and Saint-Cyr, 1995), dopamine may guide action selection in such planning tasks. To test this hypothesis, we simulate interactions between the anatomical structures shown in Fig.…”