Gaze Control in Microgravity: 1. Saccades, Pursuit, Eye-Head Coordination

1993 ◽  
Vol 3 (3) ◽  
pp. 331-343
Author(s):  
C. André-Deshays ◽  
I. Israël ◽  
O. Charade ◽  
A. Berthoz ◽  
K. Popov ◽  
...  

During the long-duration spaceflight Aragatz on board the Mir station, an experiment exploring the different oculomotor subsystems involved in gaze control during orientation to a fixed target or when tracking a moving target was executed by two cosmonauts. Gaze orientation: with head fixed, the “main sequence” relationships of primary horizontal saccades were modified, peak velocity was higher and saccade duration was shorter in flight than on earth, latency was decreased and saccade accuracy was better in flight. With head free, gaze orientation toward the target was achieved by coordinated eye and head movements, their timing was maintained in the horizontal plane; when gaze was stabilized on the target, there was a trend of a larger eye than head contribution not seen in preflight tests. Pursuit: Horizontal pursuit at 0.25 and 0.5 Hz frequency remained smooth with a 0.98 gain and minor phase lag, on earth and in flight. In the vertical plane, the eye did not track the target with a pure smooth pursuit eye movement, but the saccadic system contributed to gaze control. Upward tracking was mainly achieved with a succession of saccades, whereas downward tracking was due to combined smooth pursuit and catch-up saccades. This asymmetry was maintained during flight in head fixed and head free situations. On earth head pea velocity was maxima upward, and in flight it was maximal downward.

1999 ◽  
Vol 81 (6) ◽  
pp. 3105-3109 ◽  
Author(s):  
T. Belton ◽  
R. A. McCrea

Contribution of the cerebellar flocculus to gaze control during active head movements. The flocculus and ventral paraflocculus are adjacent regions of the cerebellar cortex that are essential for controlling smooth pursuit eye movements and for altering the performance of the vestibulo-ocular reflex (VOR). The question addressed in this study is whether these regions of the cerebellum are more globally involved in controlling gaze, regardless of whether eye or active head movements are used to pursue moving visual targets. Single-unit recordings were obtained from Purkinje (Pk) cells in the floccular region of squirrel monkeys that were trained to fixate and pursue small visual targets. Cell firing rate was recorded during smooth pursuit eye movements, cancellation of the VOR, combined eye-head pursuit, and spontaneous gaze shifts in the absence of targets. Pk cells were found to be much less sensitive to gaze velocity during combined eye–head pursuit than during ocular pursuit. They were not sensitive to gaze or head velocity during gaze saccades. Temporary inactivation of the floccular region by muscimol injection compromised ocular pursuit but had little effect on the ability of monkeys to pursue visual targets with head movements or to cancel the VOR during active head movements. Thus the signals produced by Pk cells in the floccular region are necessary for controlling smooth pursuit eye movements but not for coordinating gaze during active head movements. The results imply that individual functional modules in the cerebellar cortex are less involved in the global organization and coordination of movements than with parametric control of movements produced by a specific part of the body.


Author(s):  
Kerstin Rosander

Gaze control involves eyes, head, and body movements and is guided by mainly three types of information: visual, vestibular, and proprioceptive. Appropriate gaze control is a basis for actions such as reaching, grasping, eating, and manipulation, all of which develop during the first year of life. The development of gaze control is about how young infants gain access to these different kinds of information, how they come to use them, and how they come to coordinate head and eyes to accomplish it. This control develops during the first few weeks of life. A major challenge for the gaze controlling system is how gaze is stabilized on a moving target to keep vision clear, including during self-motion or the compensation of other sudden movements. Furthermore, the tracking has to be timed relative to the object motion. This requires prediction, which is a part of smooth pursuit that emerges at around six weeks and is in full function at three months. The smooth eye and head movements must add up in time and space to the object motion. Then the vestibular and visual neural signals must be properly added. Catch-up saccades compensate when the smooth pursuit is insufficient. In other situations, saccades shift the gaze between objects or situations. Moreover, if a moving object temporarily disappears out of view, one or several saccades predictively recapture the object at the reappearance position (four months). The complex and fast development of gaze has inspired the design of robotic vision (iCub) through processes similar to human development, thus increasing the robot’s flexibility and learning abilities


2009 ◽  
Vol 101 (2) ◽  
pp. 934-947 ◽  
Author(s):  
Masafumi Ohki ◽  
Hiromasa Kitazawa ◽  
Takahito Hiramatsu ◽  
Kimitake Kaga ◽  
Taiko Kitamura ◽  
...  

The anatomical connection between the frontal eye field and the cerebellar hemispheric lobule VII (H-VII) suggests a potential role of the hemisphere in voluntary eye movement control. To reveal the involvement of the hemisphere in smooth pursuit and saccade control, we made a unilateral lesion around H-VII and examined its effects in three Macaca fuscata that were trained to pursue visually a small target. To the step (3°)-ramp (5–20°/s) target motion, the monkeys usually showed an initial pursuit eye movement at a latency of 80–140 ms and a small catch-up saccade at 140–220 ms that was followed by a postsaccadic pursuit eye movement that roughly matched the ramp target velocity. After unilateral cerebellar hemispheric lesioning, the initial pursuit eye movements were impaired, and the velocities of the postsaccadic pursuit eye movements decreased. The onsets of 5° visually guided saccades to the stationary target were delayed, and their amplitudes showed a tendency of increased trial-to-trial variability but never became hypo- or hypermetric. Similar tendencies were observed in the onsets and amplitudes of catch-up saccades. The adaptation of open-loop smooth pursuit velocity, tested by a step increase in target velocity for a brief period, was impaired. These lesion effects were recognized in all directions, particularly in the ipsiversive direction. A recovery was observed at 4 wk postlesion for some of these lesion effects. These results suggest that the cerebellar hemispheric region around lobule VII is involved in the control of smooth pursuit and saccadic eye movements.


2007 ◽  
Vol 97 (2) ◽  
pp. 1149-1162 ◽  
Author(s):  
Mario Prsa ◽  
Henrietta L. Galiana

Models of combined eye-head gaze shifts all aim to realistically simulate behaviorally observed movement dynamics. One of the most problematic features of such models is their inability to determine when a saccadic gaze shift should be initiated and when it should be ended. This is commonly referred to as the switching mechanism mediated by omni-directional pause neurons (OPNs) in the brain stem. Proposed switching strategies implemented in existing gaze control models all rely on a sensory error between instantaneous gaze position and the spatial target. Accordingly, gaze saccades are initiated after presentation of an eccentric visual target and subsequently terminated when an internal estimate of gaze position becomes nearly equal to that of the target. Based on behavioral observations, we demonstrate that such a switching mechanism is insufficient and is unable to explain certain types of movements. We propose an improved hypothesis for how the OPNs control gaze shifts based on a visual-vestibular interaction of signals known to be carried on anatomical projections to the OPN area. The approach is justified by the analysis of recorded gaze shifts interrupted by a head brake in animal subjects and is demonstrated by implementing the switching mechanism in an anatomically based gaze control model. Simulated performance reveals that a weighted sum of three signals: gaze motor error, head velocity, and eye velocity, hypothesized as inputs to OPNs, successfully reproduces diverse behaviorally observed eye-head movements that no other existing model can account for.


2005 ◽  
Vol 93 (3) ◽  
pp. 1223-1234 ◽  
Author(s):  
Daniel J. Tollin ◽  
Luis C. Populin ◽  
Jordan M. Moore ◽  
Janet L. Ruhland ◽  
Tom C. T. Yin

In oculomotor research, there are two common methods by which the apparent location of visual and/or auditory targets are measured, saccadic eye movements with the head restrained and gaze shifts (combined saccades and head movements) with the head unrestrained. Because cats have a small oculomotor range (approximately ±25°), head movements are necessary when orienting to targets at the extremes of or outside this range. Here we tested the hypothesis that the accuracy of localizing auditory and visual targets using more ethologically natural head-unrestrained gaze shifts would be superior to head-restrained eye saccades. The effect of stimulus duration on localization accuracy was also investigated. Three cats were trained using operant conditioning with their heads initially restrained to indicate the location of auditory and visual targets via eye position. Long-duration visual targets were localized accurately with little error, but the locations of short-duration visual and both long- and short-duration auditory targets were markedly underestimated. With the head unrestrained, localization accuracy improved substantially for all stimuli and all durations. While the improvement for long-duration stimuli with the head unrestrained might be expected given that dynamic sensory cues were available during the gaze shifts and the lack of a memory component, surprisingly, the improvement was greatest for the auditory and visual stimuli with the shortest durations, where the stimuli were extinguished prior to the onset of the eye or head movement. The underestimation of auditory targets with the head restrained is explained in terms of the unnatural sensorimotor conditions that likely result during head restraint.


2006 ◽  
Vol 16 (1-2) ◽  
pp. 1-22 ◽  
Author(s):  
Junko Fukushima ◽  
Teppei Akao ◽  
Sergei Kurkin ◽  
Chris R.S. Kaneko ◽  
Kikuro Fukushima

In order to see clearly when a target is moving slowly, primates with high acuity foveae use smooth-pursuit and vergence eye movements. The former rotates both eyes in the same direction to track target motion in frontal planes, while the latter rotates left and right eyes in opposite directions to track target motion in depth. Together, these two systems pursue targets precisely and maintain their images on the foveae of both eyes. During head movements, both systems must interact with the vestibular system to minimize slip of the retinal images. The primate frontal cortex contains two pursuit-related areas; the caudal part of the frontal eye fields (FEF) and supplementary eye fields (SEF). Evoked potential studies have demonstrated vestibular projections to both areas and pursuit neurons in both areas respond to vestibular stimulation. The majority of FEF pursuit neurons code parameters of pursuit such as pursuit and vergence eye velocity, gaze velocity, and retinal image motion for target velocity in frontal and depth planes. Moreover, vestibular inputs contribute to the predictive pursuit responses of FEF neurons. In contrast, the majority of SEF pursuit neurons do not code pursuit metrics and many SEF neurons are reported to be active in more complex tasks. These results suggest that FEF- and SEF-pursuit neurons are involved in different aspects of vestibular-pursuit interactions and that eye velocity coding of SEF pursuit neurons is specialized for the task condition.


2019 ◽  
Author(s):  
Benedikt V. Ehinger ◽  
Katharina Groß ◽  
Inga Ibs ◽  
Peter König

ABSTRACTEye-tracking experiments rely heavily on good data quality of eye-trackers. Unfortunately, it is often that only the spatial accuracy and precision values are available from the manufacturers. These two values alone are not sufficient enough to serve as a benchmark for an eye-tracker: Eye-tracking quality deteriorates during an experimental session due to head movements, changing illumination or calibration decay. Additionally, different experimental paradigms require the analysis of different types of eye movements, for instance smooth pursuit movements, blinks or microsaccades, which themselves cannot readily be evaluated by using spatial accuracy or precision alone. To obtain a more comprehensive description of properties, we developed an extensive eye-tracking test battery. In 10 different tasks, we evaluated eye-tracking related measures such as: the decay of accuracy, fixation durations, pupil dilation, smooth pursuit movement, microsaccade detection, blink detection, or the influence of head motion. For some measures, true theoretical values exist. For others, a relative comparison to a gold standard eye-tracker is needed. Therefore, we collected our gaze data simultaneously from a gold standard remote EyeLink 1000 eye-tracker and compared it with the mobile Pupil Labs glasses.As expected, the average spatial accuracy of 0.57° for the EyeLink 1000 eye-tracker was better than the 0.82° for the Pupil Labs glasses (N=15). Furthermore, we detected less fixations and shorter saccade durations for the Pupil Labs glasses. Similarly, we found fewer microsaccades using the Pupil Labs glasses. The accuracy over time decayed only slightly for the EyeLink 1000, but strongly for the Pupil Labs glasses. Finally we observed that the measured pupil diameters differed between eye-trackers on the individual subject level but not the group level.To conclude, our eye-tracking test battery offers 10 tasks that allow us to benchmark the many parameters of interest in stereotypical eye-tracking situations, or addresses a common source of confounds in measurement errors (e.g. yaw and roll head movements).All recorded eye-tracking data (including Pupil Labs’ eye video files), the stimulus code for the test battery and the modular analysis pipeline are available (https://github.com/behinger/etcomp).BVE, KG, IIandPKconceived the experiment.IIandBVEcreated the experiment and recorded the gaze data.BVEandKGperformed the analysis.BVE, KGandPKreviewed the manuscript critically.


1991 ◽  
Vol 1 (2) ◽  
pp. 161-170
Author(s):  
Jean-Louis Vercher ◽  
Gabriel M. Gauthier

To maintain clear vision, the images on the retina must remain reasonably stable. Head movements are generally dealt with successfully by counter-rotation of the eyes induced by the combined actions of the vestibulo-ocular reflex (VOR) and the optokinetic reflex. A problem of importance relates to the value of the so-called intrinsic gain of the VOR (VORG) in man, and how this gain is modulated to provide appropriate eye movements. We have studied these problems in two situations: 1. fixation of a stationary object of the visual space while the head moves; 2. fixation of an object moving with the head. These two situations were compared to a basic condition in which no visual target was allowed in order to induce “pure” VOR. Eye movements were recorded in seated subjects during stationary sinusoidal and transient rotations around the vertical axis. Subjects were in total darkness (DARK condition) and involved in mental arithmetic. Alternatively, they were provided with a small foveal target, either fixed with respect to earth (earth-fixed target: EFT condition), or moving with them (chair-fixed-target: CFT condition). The stationary rotation experiment was used as baseline for the ensuing experiment and yielded control data in agreement with the literature. In all 3 visual conditions, typical responses to transient rotations were rigorously identical during the first 200 ms. They showed, sequentially, a 16-ms delay of the eye behind the head and a rapid increase in eye velocity during 75 to 80 ms, after which the average VORG was 0.9 ± 0.15. During the following 50 to 100 ms, the gain remained around 0.9 in all three conditions. Beyond 200 ms, the VORG remained around 0.9 in DARK and increased slowly towards 1 or decreased towards zero in the EFT and CFT conditions, respectively. The time-course of the later events suggests that visual tracking mechanisms came into play to reduce retinal slip through smooth pursuit, and position error through saccades. Our data also show that in total darkness VORG is set to 0.9 in man. Lower values reported in the literature essentially reflect predictive properties of the vestibulo-ocular mechanism, particularly evident when the input signal is a sinewave.


2000 ◽  
Vol 84 (3) ◽  
pp. 1614-1626 ◽  
Author(s):  
Timothy Belton ◽  
Robert A. McCrea

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive (≈43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.


2002 ◽  
Vol 87 (2) ◽  
pp. 912-924 ◽  
Author(s):  
H. Rambold ◽  
A. Churchland ◽  
Y. Selig ◽  
L. Jasmin ◽  
S. G. Lisberger

The vestibuloocular reflex (VOR) generates compensatory eye movements to stabilize visual images on the retina during head movements. The amplitude of the reflex is calibrated continuously throughout life and undergoes adaptation, also called motor learning, when head movements are persistently associated with image motion. Although the floccular-complex of the cerebellum is necessary for VOR adaptation, it is not known whether this function is localized in its anterior or posterior portions, which comprise the ventral paraflocculus and flocculus, respectively. The present paper reports the effects of partial lesions of the floccular-complex in five macaque monkeys, made either surgically or with stereotaxic injection of 3-nitropropionic acid (3-NP). Before and after the lesions, smooth pursuit eye movements were tested during sinusoidal and step-ramp target motion. Cancellation of the VOR was tested by moving a target exactly with the monkey during sinusoidal head rotation. The control VOR was tested during sinusoidal head rotation in the dark and during 30°/s pulses of head velocity. VOR adaptation was studied by having the monkeys wear ×2 or ×0.25 optics for 4–7 days. In two monkeys, bilateral lesions removed all of the flocculus except for parts of folia 1 and 2 but did not produce any deficits in smooth pursuit, VOR adaptation, or VOR cancellation. We conclude that the flocculus alone probably is not necessary for either pursuit or VOR learning. In two monkeys, unilateral lesions including a large fraction of the ventral paraflocculus produced small deficits in horizontal and vertical smooth pursuit, and mild impairments of VOR adaptation and VOR cancellation. We conclude that the ventral paraflocculus contributes to both behaviors. In one monkey, a bilateral lesion of the flocculus and ventral paraflocculus produced severe deficits smooth pursuit and VOR cancellation, and a complete loss of VOR adaptation. Considering all five cases together, there was a strong correlation between the size of the deficits in VOR learning and pursuit. We found the strongest correlation between the behavior deficits and the size of the lesion of the ventral paraflocculus, a weaker but significant correlation for the full floccular complex, and no correlation with the size of the lesion of the flocculus. We conclude that 1) lesions of the floccular complex cause linked deficits in smooth pursuit and VOR adaptation, and 2) the relevant portions of the structure are primarily in the ventral paraflocculus, although the flocculus may participate.


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