Oculomotor feature discrimination is cortically mediated.

Eye movements are often directed toward stimuli with specific features. Decades of neurophysiological research has determined that this behavior is subserved by a feature-reweighting of the neural activation encoding potential eye movements. Despite the considerable body of research examining feature-based target selection, no comprehensive theoretical account of the feature-reweighting mechanism has yet been proposed. Given that such a theory is fundamental to our understanding of the nature of oculomotor processing, we propose an oculomotor feature-reweighting mechanism here. We first summarize the considerable anatomical and functional evidence suggesting that oculomotor substrates that encode potential eye movements rely on the visual cortices for feature information. Next, we highlight the results from our recent behavioral experiments demonstrating that feature information manifests in the oculomotor system in order of featural complexity, regardless of whether the feature information is task-relevant. Based on the available evidence, we propose an oculomotor feature-reweighting mechanism whereby (1) visual information is projected into the oculomotor system only after a visual representation manifests in the highest stage of the cortical visual processing hierarchy necessary to represent the relevant features and (2) these dynamically recruited cortical module(s) then perform feature discrimination via shifting neural feature representations, while also maintaining parity between the feature representations in cortical and oculomotor substrates by dynamically reweighting oculomotor vectors. Finally, we discuss how our behavioral experiments may extend to other areas in vision science and its possible clinical applications.

Motion distractors perturb saccade programming later in time than static distractors.

The mechanism that reweights oculomotor vectors based on visual features is unclear. However, the latency of oculomotor visual activations gives insight into their antecedent featural processing. We compared the oculomotor processing time course of grayscale, task-irrelevant static and motion distractors during target selection by continuously measuring a battery of human saccadic behavioral metrics as a function of time after distractor onset. The motion direction was towards or away from the target and the motion speed was fast or slow. We compared static and motion distractors and observed that both distractors elicited curved saccades and shifted endpoints at short latencies (∼25 ms). After 50 ms, saccade trajectory biasing elicited by motion distractors lagged static distractor trajectory biasing by 10 ms. There were no such latency differences between distractor motion directions or motion speeds. This pattern suggests that additional processing of motion stimuli occurred prior to the propagation of visual information into the oculomotor system. We examined the interaction of distractor processing time (DPT) with two additional factors: saccadic reaction time (SRT) and saccadic amplitude. Shorter SRTs were associated with shorter DPT latencies of biased saccade trajectories. Both SRT and saccadic amplitude were associated with the magnitude of saccade trajectory biases.

Oculomotor target selection is mediated by complex objects.

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.

Higher order, multifeatural object encoding by the oculomotor system.

Previous behavioral and physiological research has demonstrated that as the behavioral relevance of potential saccade goals increases, they elicit more competition during target selection processing as evidenced by increased saccade curvature and neural activity. However, these effects have only been demonstrated for lower order feature singletons, and it remains unclear whether more complicated featural differences between higher order objects also elicit vector modulation. Therefore, we measured human saccades curvature elicited by distractors bilaterally flanking a target during a visual search saccade task and systematically varied subsets of features shared between the two distractors and the target, referred to as objective similarity (OS). Our results demonstrate that saccades deviated away from the distractor highest in OS to the target and that there was a linear relationship between the magnitude of saccade deviation and the number of feature differences between the most similar distractor and the target. Furthermore, an analysis of curvature over the time course of the saccade demonstrated that curvature only occurred in the first 20-30 ms of the movement. Given the multifeatural complexity of the novel stimuli, these results suggest that saccadic target selection processing involves dynamically reweighting vector representations for movement planning to several possible targets based on their behavioral relevance. NEW & NOTEWORTHY We demonstrate that small featural differences between unfamiliar, higher order object representations modulate vector weights during saccadic target selection processing. Such effects have previously only been demonstrated for familiar, simple feature singletons (e.g., color) in which features characterize entire objects. The complexity and novelty of our stimuli suggest that the oculomotor system dynamically receives visual/cognitive information processed in the higher order representational networks of the cortical visual processing hierarchy and integrates this information for saccadic movement planning.

Perceptual Color Space Representations in the Oculomotor System Are Modulated by Surround Suppression and Biased Selection.

The oculomotor system utilizes color extensively for planning saccades. Therefore, we examined how the oculomotor system actually encodes color and several factors that modulate these representations: attention-based surround suppression and inherent biases in selecting and encoding color categories. We measured saccade trajectories while human participants performed a memory-guided saccade task with color targets and distractors and examined whether oculomotor target selection processing was functionally related to the CIE (x,y) color space distances between color stimuli and whether there were hierarchical differences between color categories in the strength and speed of encoding potential saccade goals. We observed that saccade planning was modulated by the CIE (x,y) distances between stimuli thus demonstrating that color is encoded in perceptual color space by the oculomotor system. Furthermore, these representations were modulated by (1) cueing attention to a particular color thereby eliciting surround suppression in oculomotor color space and (2) inherent selection and encoding biases based on color category independent of cueing and perceptual discriminability. Since surround suppression emerges from recurrent feedback attenuation of sensory projections, observing oculomotor surround suppression suggested that oculomotor encoding of behavioral relevance results from integrating sensory and cognitive signals that are pre-attenuated based on task demands and that the oculomotor system therefore does not functionally contribute to this process. Second, although perceptual discriminability did partially account for oculomotor processing differences between color categories, we also observed preferential processing of the red color category across various behavioral metrics. This is consistent with numerous previous studies and could not be simply explained by perceptual discriminability. Since we utilized a memory-guided saccade task, this indicates that the biased processing of the red color category does not rely on sustained sensory input and must therefore involve cortical areas associated with the highest levels of visual processing involved in visual working memory.

Rapid accumulation of inhibition accounts for saccades curved away from distractors.

Saccades curved toward a distractor are accompanied by a burst of neuronal activation at the distractor locus in the intermediate layers of the superior colliculus (SCi) ~30 ms before the initiation of a saccade. Although saccades curve away from inactivated SCi loci, whether inhibition is restricted to a similar critical epoch for saccades curved away from a distractor remains unclear. We examined this possibility by modeling human saccade curvature as a function of the time between onset of a task irrelevant luminance- or color-modulated distractor and initiation of an impending saccade, referred to as saccade distractor onset asynchrony (SDOA). Our results demonstrated that 70 ms of luminance-modulated distractor processing or 90 ms of color-modulated distractor processing was required to modulate saccade trajectories. As these behavioral, feature-based differences were temporally consistent with the cortically mediated neurophysiological differences in visual onset latencies between luminance and color stimuli observed in the oculomotor and visual system, this method provides a noninvasive means to estimate the timing of peak activation in the oculomotor system. As such, we modeled SDOA functions separately for saccades curved toward and away from distractors and observed that a similar temporal process determined the magnitude of saccade curvatures in both contexts, suggesting that saccades deviate away from a distractor due to a rapid accumulation of inhibition in the critical epoch before saccade initiation.NEW & NOTEWORTHY In this research article, we propose a novel, noninvasive approach to behaviorally model the time course of competitive oculomotor processing. Our results highly resembled those from previously published neurophysiological experiments utilizing similar oculomotor processing contexts, thus validating our approach. Furthermore, this methodology provided new insights into the underlying neural mechanism subserving oculomotor processing given that we applied it to a context with which the neural mechanism is more contentious, and the results clearly favored one view.