Human eye-head gaze shifts preserve their accuracy and spatiotemporal trajectory profiles despite long-duration torque perturbations that assist or oppose head motion

Abstract

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...

Hierarchical control of two-dimensional gaze saccades

“…When the gaze movement is accompanied by a blink, the eye and gaze velocities become double-peaked. This is a particularly interesting finding, because previous literature shows either single-peaked (Boulanger et al 2012; Choi and Guitton 2006; Guitton and Volle 1987a) or double-peaked (Freedman and Spark 1997, 2000) traces. We infer from Gandhi’s study that double-peaked velocity traces may not be a normal feature of eye-head coordination.…”

“…Finally, Boulanger et al (2012) have shown that long duration torques (up to 700 ms), which oppose or assist intended head movements, can be compensated even before the torque ends. This would not be possible for any head control model without some feedback information about head displacement.…”

“…The results of Sylvestre and Cullen (2006) show that after a brief head brake is applied, the head movement recovers with a time constant of much less than 100 ms. Furthermore, Boulanger et al (2012) showed that when long duration torques were applied to the head, the head could get on target even before the torque ends. As the model of Kardamakis et al (2010) used a plant with two time constants (105 and 181 ms) and no head feedback, their model could not reproduce either of these head perturbation studies because the fastest recovery would have a time constant of 105 ms.…”

Modelling eye-head coordination without pre-planning — A reflex-based approach

“…Vestibular compensation during saccades: After saccades, it is accepted that passive head perturbations are compensated using the VOR. However, passive head perturbations during gaze saccades can also be compensated especially if they are in the direction of the gaze shift 'assisting perturbations' [2,19]. Since the activity of PVP neurons during the saccadic part of gaze orientation is much reduced, this compensation cannot be the result of the VOR in its classical sense [3].…”

“…Simulated 40 degree gaze orientation with assisting head perturbation during the saccadic interval[2].…”