Boulanger M, Galiana HL, Guitton D. Human eye-head gaze shifts preserve their accuracy and spatiotemporal trajectory profiles despite long-duration torque perturbations that assist or oppose head motion. J Neurophysiol 108: 39 -56, 2012. First published March 28, 2012 doi:10.1152/jn.01092.2011.-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.eye-head coordination; orienting gaze shifts; trajectory planning THERE IS MUCH DEBATE about how coordinated eye-head gaze shifts are controlled. About a half-dozen models have been proposed, and they can be roughly subdivided into two conceptual frameworks. In models that employ gaze feedback control, the eye and head components of gaze saccades are driven by a gaze position error (GPE) signal obtained in a feedback loop that subtracts estimates of actual from desired gaze displacement (Galiana and Guitton 1992;Goossens and Van Opstal 1997;Guitton and Volle 1987;Guitton et al. 2003Guitton et al. , 2004Laurutis and Robinson 1986). Feedback forces GPE toward zero, thereby compensating for internal motor "noise" and/or unexpected external perturbation in either the eye or head trajectories.Gaze control models that do not use gaze feedback control subdivide the initial gaze error vector into specified eye and head contributions. In these models there is no updated GPE signal, b...
Humans routinely scan their environment for useful information using saccadic eye movements and/or coordinated movements of the eyes and other body segments such the head and the torso. Most previous eye movement studies were conducted with seated subject and showed that single saccades and sequences of saccades (e.g. double-step saccades) made to briefly flashed stimuli were equally accurate and precise. As one can easily appreciate, most gaze shifts performed daily by a given person are not produced from a seated position, but rather from a standing position either as subjects perform an action from an upright stance or as they walk from one place to another. In the experiments presented here, we developed a new dual-task paradigm in order to study the interaction between the gaze control system and the postural system. Healthy adults (n = 12) were required to both maintain balance and produce accurate single-step and double-step eye saccades from a standing position. Visually-induced changes in head sway were evoked using wide-field background stimuli that either moved in the mediolateral direction or in the anteroposterior direction. We found that, as in the seated condition, single- and double-step saccades were very precise and accurate when made from a standing position, but that a tighter control of head sway was necessary in the more complex double-step saccades condition for equivalent results to be obtained. Our perturbation results support the “common goal” hypothesis that state that if necessary, as was the case during the more complex oculomotor task, context-dependent modulations of the postural system can be triggered to reduced instability and therefore support the accomplishment of a suprapostural goal.
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