Oculomotor Target Selection is Cortically Mediated by Complex Objects

Abstract

Successful oculomotor target selection often requires discriminating visual features but it remains contentious whether oculomotor substrates encoding saccade vectors functionally contribute to this process. One possibility is that visual features are discriminated cortically and oculomotor modules select the object with the highest activation in the set of all preprocessed cortical object representations, while an alternative possibility is that oculomotor modules actively discriminate potential targets based on visual features. If the latter view is correct, these modules should not require input from specialized visual cortices encoding the task relevant features. We therefore examined whether the latency of visual onset responses elicited by abrupt distractor onsets is consistent with input from specialized visual cortices by non-invasively measuring human saccade metrics (saccade curvature, endpoint deviations, saccade frequency, error proportion) as a function of distractor processing time for novel, visually complex distractors that had to be discriminated from a target to guide saccades. Visual onset response latencies were ~110 ms, consistent with projections from anterior cortical sites specialized for object processing. Surprisingly, oculomotor visual onset responses encoded features, as we manipulated the visual similarity between targets and distractors and observed an increased visual onset response magnitude and duration when the distractor was highly similar to the target, which was not attributable to an inhibitory processing delay. Visual onset responses were dynamically modulated by executive function, as these responses were anticipatorily extinguished over the time course of the experiment. As expected, the latency of distractor-related inhibition was modulated by the behavioral relevance of the distractor. Significance StatementWe provide novel insights into the role of the oculomotor system in saccadic target selection by challenging the convention that neural substrates that encode oculomotor vectors functionally contribute to target discrimination. Our data show that the oculomotor system selects a winner from amongst the preprocessed object representations output from specialized visual cortices as supposed to discriminating visual features locally. We also challenge the convention that oculomotor visual onset responses are feature-invariant, as they encoded task-relevance.