Presaccadic motion integration drives a predictive postsaccadic following response

Abstract

Saccadic eye movements sample the visual world and ensure high acuity across the visual field. To compensate for delays in processing, saccades to moving targets require predictions: The eyes must intercept the target's future position to then pursue its direction of motion. Although prediction is crucial to voluntary pursuit, it is unclear whether it is an obligatory feature of saccade planning. Saccade planning involves an involuntary enhanced processing of the target, called presaccadic attention. Does this presaccadic attention recruit smooth eye movements automatically? To test this, we had human participants perform a saccade to one of four apertures, which were static, but each contained a random dot field with motion tangential to the required saccade. In this task, saccades were deviated along the direction of target motion, and the eyes exhibited a following response upon saccade landing. This postsaccadic following response (PFR) increased with spatial uncertainty of the target position and persisted even when we removed the motion stimulus in midflight of the saccade, confirming that it relied on presaccadic information. Motion from 50-100 ms prior to the saccade had the strongest influence on PFR, consistent with the time course of perceptual enhancements reported in presaccadic attention. Finally, the PFR magnitude related linearly to the logarithm of stimulus velocity and generally had low gain, similar to involuntary ocular following movements commonly observed after sudden motion onsets. These results suggest that presaccadic attention selects motion features of targets predictively, presumably to ensure successful immediate tracking of saccade targets in motion.

Perceptual restoration fails to recover unconscious processing for smooth eye movements after occipital stroke

“…It is well established that sensory processing among neurons in MT and MST can be strongly influenced by attention (Treue & Maunsell, 1996; Treue & Trujillo, 1999) and also by target selection immediately prior to saccades (Ferrera & Lisberger, 1997; Recanzone & Wurtz, 2000). Recent studies suggest that like target selection in voluntary pursuit, selective attention can modulate ocular following responses (Souto & Kerzel, 2014), and our findings here and previously (Kwon et al, 2019) support this notion. Pre-saccadic attention is thought to operate through feedback from oculomotor planning areas to visual cortex (Moore & Armstrong, 2003; Moore & Fallah, 2004), and while its impact has been studied mainly in visual area V4, it is also thought to occur in MT/MST.…”

“…This reflects a perceptual mis-localization error along the target motion direction that also influences saccade programming by causing saccade end-points to be shifted along the target motion (Kosovicheva et al, 2014). Consistent with previous studies, our earlier study in visually-intact controls found the position of saccade end-points to be displaced along the direction of dot motion contained in a peripheral target aperture (Kwon et al, 2019). Thus, like the PFR, saccade end-points are also influenced by pre-saccadic selection of target motion, providing another measure of the predictive influence of target motion.…”

“…As shown in Supplementary Fig. 2 , visually-intact controls (from Kwon et al, 2019) showed a net positive saccade angular deviations that differed significantly from 0 (t(7)=11.53, p<0.001 – leftmost grey bar). This was also observed in CB patients, in intact portions of their visual fields (t(7)=5.28, p=0.001) - white bar in Supplementary Fig.…”

“… A : Plot of mean PFR gain in visually-intact controls (Kwon et al, 2019), and in V1-stroke patients’ intact and blind-fields during the open-loop period. The PFR gain is here represented as a proportion of pursuit gain along the target motion direction (1 = perfect following, 0 = no following, −1 = following in the opposite direction).…”

Introduction to special issue on “Prediction in Perception and Action”

“… Goettker et al (2019) show that the pursuit and saccadic system share a common internal representation of the target movement and interact closely to improve tracking responses rapidly. Congruently, Kwon et al (2019) show that the integration of position and motion information extends to the ocular following response. Rothwell et al (in press) compared the role of different cues in driving anticipatory smooth pursuit and anticipatory ocular torsion and found that the predictive drive for these two types of eye movements might be partly decoupled.…”