The Gaze Control System

Author(s):  
John van Opstal
Keyword(s):  
2012 ◽  
Vol 108 (1) ◽  
pp. 39-56 ◽  
Author(s):  
Mathieu Boulanger ◽  
Henrietta L. Galiana ◽  
Daniel Guitton

Humans routinely use coordinated eye-head gaze saccades to rapidly and accurately redirect the line of sight (Land MF. Vis Neurosci 26: 51–62, 2009). With a fixed body, the gaze control system combines visual, vestibular, and neck proprioceptive sensory information and coordinates two moving platforms, the eyes and head. Classic engineering tools have investigated the structure of motor systems by testing their ability to compensate for perturbations. When a reaching movement of the hand is subjected to an unexpected force field of random direction and strength, the trajectory is deviated and its final position is inaccurate. Here, we found that the gaze control system behaves differently. We perturbed horizontal gaze shifts with long-duration torques applied to the head that unpredictably either assisted or opposed head motion and very significantly altered the intended head trajectory. We found, as others have with brief head perturbations, that gaze accuracy was preserved. Unexpectedly, we found also that the eye compensated well—with saccadic and rollback movements—for long-duration head perturbations such that resulting gaze trajectories remained close to that when the head was not perturbed. However, the ocular compensation was best when torques assisted, compared with opposed, head motion. If the vestibuloocular reflex (VOR) is suppressed during gaze shifts, as currently thought, what caused invariant gaze trajectories and accuracy, early eye-direction reversals, and asymmetric compensations? We propose three mechanisms: a gaze feedback loop that generates a gaze-position error signal; a vestibular-to-oculomotor signal that dissociates self-generated from passively imposed head motion; and a saturation element that limits orbital eye excursion.


1998 ◽  
Vol 79 (6) ◽  
pp. 3060-3076 ◽  
Author(s):  
Martin Paré ◽  
Daniel Guitton

Paré, Martin and Daniel Guitton. Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. J. Neurophysiol. 79: 3060–3076, 1998. When the head is unrestrained, rapid displacements of the visual axis—gaze shifts (eye-re-space)—are made by coordinated movements of the eyes (eye-re-head) and head (head-re-space). To address the problem of the neural control of gaze shifts, we studied and contrasted the discharges of omnipause neurons (OPNs) during a variety of combined eye-head gaze shifts and head-fixed eye saccades executed by alert cats. OPNs discharged tonically during intersaccadic intervals and at a reduced level during slow perisaccadic gaze movements sometimes accompanying saccades. Their activity ceased for the duration of the saccadic gaze shifts the animal executed, either by head-fixed eye saccades alone or by combined eye-head movements. This was true for all types of gaze shifts studied: active movements to visual targets; passive movements induced by whole-body rotation or by head rotation about stationary body; and electrically evoked movements by stimulation of the caudal part of the superior colliculus (SC), a central structure for gaze control. For combined eye-head gaze shifts, the OPN pause was therefore not correlated to the eye-in-head trajectory. For instance, in active gaze movements, the end of the pause was better correlated with the gaze end than with either the eye saccade end or the time of eye counterrotation. The hypothesis that cat OPNs participate in controlling gaze shifts is supported by these results, and also by the observation that the movements of both the eyes and the head were transiently interrupted by stimulation of OPNs during gaze shifts. However, we found that the OPN pause could be dissociated from the gaze-motor-error signal producing the gaze shift. First, OPNs resumed discharging when perturbation of head motion briefly interrupted a gaze shift before its intended amplitude was attained. Second, stimulation of caudal SC sites in head-free cat elicited large head-free gaze shifts consistent with the creation of a large gaze-motor-error signal. However, stimulation of the same sites in head-fixed cat produced small “goal-directed” eye saccades, and OPNs paused only for the duration of the latter; neither a pause nor an eye movement occurred when the same stimulation was applied with the eyes at the goal location. We conclude that OPNs can be controlled by neither a simple eye control system nor an absolute gaze control system. Our data cannot be accounted for by existing models describing the control of combined eye-head gaze shifts and therefore put new constraints on future models, which will have to incorporate all the various signals that act synergistically to control gaze shifts.


Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 371-371
Author(s):  
R M Steinman ◽  
T I Forofonova ◽  
J Epelboim ◽  
M R Stepanov

Epelboim et al (1996 Vision Research35 3401 – 3422) reported that cyclopean gaze errors were smaller than either eye's during tapping and looking-only tasks. This raised two questions: (i) does cyclopean gaze accuracy require binocular input, and (ii) when only one eye sees, is its gaze more accurate than the patched eye's? Most oculomotorists probably expect an affirmative answer to both. Neither expectation was fulfilled. The Maryland Revolving Field Monitor recorded, with exceptional accuracy, eye movements of two unrestrained subjects tapping or only looking, in a specified order, at four randomly positioned LEDs, with monocular or binocular viewing. Subjects either tapped with their finger tips naturally, or unnaturally via a rod (2 mm diameter, 1.5 cm long), glued to a sewing thimble. Instructions were to be fast, but make no order errors. With binocular viewing, cyclopean gaze accuracy was best during looking-only. During natural tapping, gaze errors increased, becoming no smaller than success required. Both tasks were learned equally fast, but as expected, the younger subject (aged 27 years) performed ∼ 40% faster than the older subject (aged 69 years). Unnatural, monocular viewing produced odd results, eg cyclopean gaze error was smallest when only one eye could see in some conditions. Only the older subject served in the unnatural tapping task because the younger's errors were too close to his gaze control limit. The older subject, who was suitable, reduced his cyclopean gaze error by 56%, from 1.4 to 0.9 deg. These results support our claim that the gaze error allowed is adjusted to the visuomotor demands of different tasks.


2003 ◽  
Vol 90 (4) ◽  
pp. 2770-2776 ◽  
Author(s):  
Julio C. Martinez-Trujillo ◽  
Eliana M. Klier ◽  
Hongying Wang ◽  
J. Douglas Crawford

Most of what we know about the neural control of gaze comes from experiments in head-fixed animals, but several “head-free” studies have suggested that fixing the head dramatically alters the apparent gaze command. We directly investigated this issue by quantitatively comparing head-fixed and head-free gaze trajectories evoked by electrically stimulating 52 sites in the superior colliculus (SC) of two monkeys and 23 sites in the supplementary eye fields (SEF) of two other monkeys. We found that head movements made a significant contribution to gaze shifts evoked from both neural structures. In the majority of the stimulated sites, average gaze amplitude was significantly larger and individual gaze trajectories were significantly less convergent in space with the head free to move. Our results are consistent with the hypothesis that head-fixed stimulation only reveals the oculomotor component of the gaze shift, not the true, planned goal of the movement. One implication of this finding is that when comparing stimulation data against popular gaze control models, freeing the head shifts the apparent coding of gaze away from a “spatial code” toward a simpler visual model in the SC and toward an eye-centered or fixed-vector model representation in the SEF.


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