Abstract

Oculomotor target selection often requires discriminating visual features, but it remains unclear how oculomotor substrates encoding saccade vectors functionally contribute to this process. One possibility is that oculomotor vector representations (observed directly as physiological activation or inferred from behavioral interference) of potential targets are continuously reweighted by task relevance computed elsewhere in specialized visual modules, whereas an alternative possibility is that oculomotor modules use local featural analyses to actively discriminate potential targets. Strengthening the former account, oculomotor vector representations have longer onset latencies for ventral- (i.e., color) than dorsal-stream features (i.e., luminance), suggesting that oculomotor vector representations originate from featurally relevant specialized visual modules. Here, we extended this reasoning by behaviorally examining whether the onset latency of saccadic interference elicited by visually complex stimuli is greater than is commonly observed for simple stimuli. We measured human saccade metrics (saccade curvature, endpoint deviations, saccade frequency, and error proportion) as a function of time after abrupt distractor onset. Distractors were novel, visually complex, and had to be discriminated from targets to guide saccades. The earliest saccadic interference latency was ∼110 ms, considerably longer than previous experiments, suggesting that sensory representations projected into the oculomotor system are gated to allow for sufficient featural processing to satisfy task demands. Surprisingly, initial oculomotor vector representations encoded features, as we manipulated the visual similarity between targets and distractors and observed increased vector modulation response magnitude and duration when the distractor was highly similar to the target. Oculomotor vector modulation was gradually extinguished over the time course of the experiment.NEW & NOTEWORTHY We challenge the role of the oculomotor system in discriminating features during saccadic target selection. Our data suggest that the onset latency of oculomotor vector representations is scaled by task difficulty and featural complexity, suggesting that featural computations are performed outside of the oculomotor system, which receives the output of these computations only after sufficient visual and cognitive processing. We also challenge the convention that initial oculomotor vector representations are feature invariant, as they encoded task relevance.

Highlights

  • The oculomotor system encodes visual stimuli [1, 2] and saccades [3, 4] as vectors on orderly spatial maps

  • We examined saccade endpoint deviations, saccade frequencies, and error proportions, as they are indicative of oculomotor excitatory and suppressive processing: 1) subthreshold microstimulation of a secondary saccade vector in superior colliculus (SCi) or frontal eye fields (FEF) concurrent with saccade initiation causes saccade endpoints to shift toward the stimulated vector and the magnitude of these deviations is proportional to the intensity of the microstimulation [3, 4, 32] (Fig. 1). 2) The abrupt onset of a visual stimulus transiently lowers the behavioral likelihood of saccade initiation $60 ms after stimulus onset [31]

  • As distractor identity could be decoded from the magnitude and duration of excitatory processing related to the distractor onset, this suggests that the oculomotor system dynamically receives preprocessed object representations from relevant visual modules and encodes these objects as dynamically reweighted oculomotor vectors, as we have argued previously [17, 18, 22]

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Summary

Introduction

The oculomotor system encodes visual stimuli [1, 2] and saccades [3, 4] as vectors on orderly spatial maps. If multiple potential saccade targets are present, the oculomotor system must select a winner from among the available oculomotor vector representations, a process called target selection. Competition between oculomotor vector representations during target selection can be inferred behaviorally from the spatial biasing of a target-directed saccade by some secondary stimulus, such as in the remote distractor [5,6,7,8,9] or double-stepping target [10, 11] paradigms. The modulation of saccade trajectories by competing distractors during target selection is sensitive to the time course of oculomotor planning. Saccade trajectories are typically biased toward distractors at short saccade latencies [12,13,14,15,16], whereas at longer saccade latencies, saccades curve away from distractors [14] and endpoint averaging ceases [12, 13, 15].

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