Learning the trajectory of a moving visual target and evolution of its tracking in the monkey

Abstract

An object moving in the visual field triggers a saccade that brings its image onto the fovea. It is followed by a combination of slow eye movements and catch-up saccades that try to keep the target image on the fovea as long as possible. The accuracy of this ability to track the "here-and-now" location of a visual target contrasts with the spatiotemporally distributed nature of its encoding in the brain. We show in six experimentally naive monkeys how this performance is acquired and gradually evolves during successive daily sessions. During the early exposure, the tracking is mostly saltatory, made of relatively large saccades separated by low eye velocity episodes, demonstrating that accurate (here and now) pursuit is not spontaneous and that gaze direction lags behind its location most of the time. Over the sessions, while the pursuit velocity is enhanced, the gaze is more frequently directed toward the current target location as a consequence of a 25% reduction in the number of catch-up saccades and a 37% reduction in size (for the first saccade). This smoothing is observed at several scales: during the course of single trials, across the set of trials within a session, and over successive sessions. We explain the neurophysiological processes responsible for this combined evolution of saccades and pursuit in the absence of stringent training constraints. More generally, our study shows that the oculomotor system can be used to discover the neural mechanisms underlying the ability to synchronize a motor effector with a dynamic external event.

The caudal fastigial nucleus and the steering of saccades toward a moving visual target

“…In this study, we describe how the unilateral injection of muscimol in the cFN affects interceptive saccades toward a moving visual target. The experiments started several months after the monkeys were extensively trained (Ͼ1 yr) to make saccades to targets moving in the peripheral visual field (Bourrelly et al 2013(Bourrelly et al , 2016Quinet and Goffart 2015a) or moving away from the central target. Each experiment consisted of several preinjection (control) sessions and one postinjection session.…”

Neurophysiology of visually guided eye movements: critical review and alternative viewpoint

“…The evolution of oculomotor tracking with practice has recently been documented in a study testing a relatively large number of naive rhesus monkeys (M. mulatta). In this study, Bourrelly et al (2016) show how inexperienced monkeys track a visual target that moves with a constant speed along a horizontal path and how the time course of their tracking eye movements gradually evolves across several days of practice with barely any spatiotemporal constraints. Indeed, the "electronic window" around the moving target within which the monkey had to direct its gaze was very large (10 -12°horizontally and 6 -10°vertically).…”

“…They were faster because the visual tracking was selected by experimental constraints to become so, smooth and devoid of saccades. In the study of Bourrelly et al (2016), catch-up saccades were permitted, especially those that would aim at a future location of the target (because the electronic window extended beyond the current target location). However, these "predictive" saccades landing ahead of the moving target just did not happen; gaze direction lagged behind the target most of the time.…”

“…Contrary to the claim that "in [their] programming [...], target motion is used to predict the future target position so as to assure a spatial lead of the gaze at the saccade end, instead of attempting a precise capture of the target" (Klam et al 2001; see also Berthoz 2012), most behavioral studies show that the saccades are such that they do not direct gaze toward a location where the target will be in the future. They direct gaze either toward its current location or toward a location lagging behind (Barmack 1970;Bourrelly et al 2016Bourrelly et al , 2018aFleuriet et al, 2011;Fuchs 1967aFuchs , 1967bKeller and Johnsen 1990;Robinson 1965). The saccades do not orient the foveae toward a location where gaze would wait for the target (like the traveler waits for a bus) to enter within the foveal field and initiate the pursuit.…”

“…Concerning the first group of During the other randomly interleaved trials, the target moved similarly, horizontally and away from the vertical meridian, but in the lower right, the lower left, or the upper left quadrant. Additional methodological information can be found in Bourrelly et al (2016). signals, it is quite possible that after the moving target disappears activity persists within the visuomotor channels.…”