Synchronizing the tracking eye movements with the motion of a visual target: Basic neural processes

Abstract

In primates, the appearance of an object moving in the peripheral visual field elicits an interceptive saccade that brings the target image onto the foveae. This foveation is then maintained more or less efficiently by slow pursuit eye movements and subsequent catch-up saccades. Sometimes, the tracking is such that the gaze direction looks spatiotemporally locked onto the moving object. Such a spatial synchronism is quite spectacular when one considers that the target-related signals are transmitted to the motor neurons through multiple parallel channels connecting separate neural populations with different conduction speeds and delays. Because of the delays between the changes of retinal activity and the changes of extraocular muscle tension, the maintenance of the target image onto the fovea cannot be driven by the current retinal signals as they correspond to past positions of the target. Yet, the spatiotemporal coincidence observed during pursuit suggests that the oculomotor system is driven by a command estimating continuously the current location of the target, i.e., where it is here and now. This inference is also supported by experimental perturbation studies: when the trajectory of an interceptive saccade is experimentally perturbed, a correction saccade is produced in flight or after a short delay, and brings the gaze next to the location where unperturbed saccades would have landed at about the same time, in the absence of visual feedback. In this chapter, we explain how such correction can be supported by previous visual signals without assuming "predictive" signals encoding future target locations. We also describe the basic neural processes which gradually yield the synchronization of eye movements with the target motion. When the process fails, the gaze is driven by signals related to past locations of the target, not by estimates to its upcoming locations, and a catch-up is made to reinitiate the synchronization.

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

“…2-4 in Fleuriet and Goffart 2012 and also Fig. 4 in Goffart et al 2017a). In these experiments, the target was made invisible for a brief interval (150 or 300 ms) to avoid the possibility that visual signals guided the correction.…”

“…Although most studies viewed this improvement as a gain increase in the positive feedback loop, to our knowledge, none of them explained what this gain change meant in neurophysiological words. Recently, the proposal was made that the enhancement of pursuit velocity could result from the recruitment of neurons in pursuit-related regions targeted by the oculomotor cerebellum and/or from the acquisition of a saccade-contingent burst by pursuit-related neurons (Bourrelly et al 2018b;Goffart et al 2017a). Finally, although the target moved along the same horizontal path and the reward was always given at the end of the trial, the monkeys did not make saccades directly toward the rewarded location.…”

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

“…These notions are mathematical instruments used to describe the motion of a rigid body in the external world. A complete homeomorphism between the set of behavioral measurements and the inner working of the brain is quite questionable (Goffart et al 2017a;Pellionisz 1986;Pellionisz and Llinás 1982). We propose that the dysmetria that affects interceptive saccades after cFN inactivation is not due to the suppression of a signal compensating for the target motion; it is the mere consequence of perturbing the process by which the MPC adjusts the population of neurons that, in the reticular formation, drive the horizontal component of saccades, regardless of whether they are made during fixation (Guerrasio et al 2010) or aimed at a visual target (static or moving) with the head fixed (Goffart et al 2004) or free to move (Quinet and Goffart 2005, 2009, 2015b.…”

“…While the first option implies the existence of internal signals encoding the kinematics of the visual target (e.g., Blazquez et al 2017;Cerminara et al 2009;de Brouwer et al 2002;Ferrera and Barborica 2010), the second option does not. Moreover, because a complete homeomorphism between the set of timevarying measurements (position, velocity) and the inner working of the brain is questionable (Goffart et al 2017a;Pellionisz 1986;Pellionisz and Llinás 1982), we prefer not to assume that target velocity is encoded within the brain activity.…”

Ups and downs in catch-up saccades following single-pulse TMS-methodological considerations

“…to update adequately eye motor commands for the novel target position). Moreover, although the notion of internal model is often evoked for a self-moved target [ 34 – 36 ], this is less obvious for an externally-moved target following a random trajectory [ 37 ]. Overall it seems simpler to consider that TMS altered both the programming and the initiation of catch-up saccades.…”