Goal representations dominate superior colliculus activity during extrafoveal tracking

The primate superior colliculus (SC) has long been known to be involved in saccade generation. However, SC neurons also exhibit fixation-related and smooth-pursuit-related activity. A parsimonious explanation for these seemingly disparate findings is that the SC contains a map of behaviorally relevant goal locations, rather than just a motor map for saccades and fixation. This explanation predicts that SC activity should reflect the behavioral goal, even when the behavioral response is not fixation or saccades, and even if the goal does not correspond to a visual stimulus. We tested this prediction by using a tracking task that dissociates the stimulus and goal locations. In this task, monkeys tracked the invisible midpoint between two peripheral bars, such that the visual stimuli were peripheral but the goal was foveal/parafoveal. We recorded from SC neurons representing peripheral locations associated with the stimulus or central locations associated with the goal. Most neurons with peripheral response fields did not respond differently during tracking than during passive viewing of the stimulus under fixation; most neurons with central response fields responded more during tracking than during fixation, despite the lack of a visual stimulus. Moreover, the spatial distribution of activity during tracking was larger than that during fixation or tracking of a foveal stimulus, suggesting that the greater spatial uncertainty about the invisible goal corresponded to more widespread SC activity. These results demonstrate the flexibility with which activity across the SC represents the location, as well as the spatial precision, of behaviorally relevant goals for multiple eye movements.