Slower velocity perception with stronger optokinetic nystagmus: A paradoxical perception in virtual reality.

BACKGROUND: Optokinetic nystagmus (OKN) was studied in an immersive virtual reality (VR) environment with both typical optokinetic stimulation (OKs) wherein the head-tracking is active (similar to be sitting in front of a rotating drum) or a unique stimulus (VR-OKs) wherein the head-tracking is turned off, so head movements do not update the visual image (which moves with the head). OBJECTIVE: To study both the perception of the stimulus velocity and eye movements while subjects rotated their head from side to side and the visual scene was either a typical OKs or VR-OKs. METHODS: 9 healthy participants (aged 23 ± 2.4 y/o) had head and eye movements recorded under typical OKs and VR-OKS while smoothly rotating their head horizontally from side to side. Stimulation was delivered using a virtual reality setup on top of an eye movements recording system. RESULTS: Under VR-OKs participants perceived faster stimulus velocity when the head and stimulus had the same direction as compared to the head and stimulus in opposite directions. When the head turned in the same direction as the stimulus, there were fewer fast phase eye movements than when it rotated counter to stimulus motion direction. Conversely, with typical OKs, participants perceived faster stimulus velocity when the head and stimulus had opposite directions as compared to the head and stimulus having the same direction. CONCLUSIONS: The seemingly paradoxical results in which slower stimulus velocity is perceived in tandem with stronger nystagmus can be explained by the simultaneous activation of the Vestibulo-Ocular Reflex and OKN in accordance with the various visual and vestibular stimuli.

Sequential processing deficits of reading disabled persons is independent of inter-stimulus interval.

Developmental dyslexia is a language-based learning disability with frequently associated non-linguistic sensory deficits that have been the basis of various perception-based theories. It remains an open question whether the underlying deficit in dyslexia is a low level impairment that causes speech and orthographic perception deficits that in turn impedes higher phonological and reading processes, or a high level impairment that affects both perceptual and reading related skills. We investigated by means of contrast detection thresholds two low-level theories of developmental dyslexia, the magnocellular and the fast temporal processing hypotheses, as well as a more recent suggestion that dyslexics have difficulties in sequential comparison tasks that can be attributed to a higher-order deficit. It was found that dyslexics had significantly higher thresholds only on a sequential, but not a spatial, detection task, and that this impairment was found to be independent of the inter-stimulus interval. We also found that the poor performance of dyslexics on the temporal task was dependent on the size of the required memory trace of the image rather than on the number of images. Our findings do not support the magnocellular theory and challenge the fast temporal deficit hypothesis. We suggest that dyslexics may have a higher order, dual mechanism impairment. We also discuss the clinical implications of our findings.

Rhesus monkeys behave as if they perceive the Duncker Illusion.

The visual system uses the pattern of motion on the retina to analyze the motion of objects in the world, and the motion of the observer him/herself. Distinguishing between retinal motion evoked by movement of the retina in space and retinal motion evoked by movement of objects in the environment is computationally difficult, and the human visual system frequently misinterprets the meaning of retinal motion. In this study, we demonstrate that the visual system of the Rhesus monkey also misinterprets retinal motion. We show that monkeys erroneously report the trajectories of pursuit targets or their own pursuit eye movements during an epoch of smooth pursuit across an orthogonally moving background. Furthermore, when they make saccades to the spatial location of stimuli that flashed early in an epoch of smooth pursuit or fixation, they make large errors that appear to take into account the erroneous smooth eye movement that they report in the first experiment, and not the eye movement that they actually make.

The saccadic system more readily co-processes orthogonal than co-linear saccades.

Real-life visual tasks such as tracking jumping objects and scanning visual scenes often require a sequence of saccadic eye movements. The ability of the ocular motor system to parallel process saccades has been previously demonstrated. We recorded the monocular eye movements of five normal human subjects using the magnetic search coil technique in a double step paradigm. Initial target jumps were always purely horizontal or purely vertical. We were interested in the latency to onset of the second saccade as a function of direction in relation to the first saccade. When the inter stimulus interval (ISI) was 150 or 180 ms orthogonal second saccades were of significantly shorter latency than second co-linear saccades. When the ISI was 250 ms the latencies of orthogonal and co-linear second saccades were statistically indistinguishable. Based on these findings it is postulated that the ocular motor system can more readily co-process orthogonal than co-linear saccades.

Target selection for pursuit and saccadic eye movements in humans.

Eye movements were recorded from three subjects as they initiated tracking of a small circle ("target") moving leftward or rightward, above or below the horizontal meridian, either alone or in the presence of a small square ("distractor") moving leftward or rightward on the other side of the horizontal meridian. At the start of each trial, subjects were provided with either a "form" cue (always centrally positioned and having the circular shape and color of the upcoming moving target) or a "location" cue (a small white square positioned where the upcoming target would appear). The latency of pursuit increased in the presence of an oppositely moving distractor when subjects were provided the form cues but not when they were provided the location cues. The latency of saccades showed similar, but smaller, increases when subjects were given the form cues. On many trials with the form cues, pursuit started in the direction of the distractor and then reversed to follow the target. On these trials, the initial saccade often, but not always, also followed the distractor. These results indicate that the mechanisms of target selection for pursuit and saccades are tightly coordinated but not strictly yoked. The shared effects of the distractor on the latencies of pursuit and saccades probably reflect the common role of visual attention in filtering the inputs that guide these two types of eye movements. The differences in the details of the effects on pursuit and saccades suggest that the neural mechanisms that trigger these two movements can be independently regulated.

Saccades to remembered targets: the effects of saccades and illusory stimulus motion.

In 10 human subjects, we measured the accuracy of saccades to remembered locations of targets that were flashed on a 20 x 30 deg random dot display, while they tracked a spot of light that stepped between three vertical locations. The background was either stationary or stepping horizontally in synchrony with vertical motion of the spot of light, a condition that induced a strong illusion of diagonal target motion. Memory-guided saccades were less accurate horizontally, but not vertically, when the background moved compared with when it was stationary. The horizontal component of memory-guided saccades correlated better with the position of the background when the target was flashed than with the position of the background at the end of the memory period. We conclude that the visual illusion corrupted the working memory of target-location, but had a lesser effect on the estimate of gaze at the end of the memory period, which seemed to depend more on extraretinal signals.

Properties of horizontal saccades accompanied by blinks.

Using the magnetic search coil technique to record eye and lid movements, we investigated the effect of voluntary blinks on horizontal saccades in five normal human subjects. The main goal of the study was to determine whether changes in the dynamics of saccades with blinks could be accounted for by a superposition of the eye movements induced by blinks as subjects fixated a stationary target and saccadic movements made without a blink. First, subjects made voluntary blinks as they fixed on stationary targets located straight ahead or 20 degrees to the right or left. They then made saccades between two continuously visible targets 20 or 40 degrees apart, while either attempting not to blink, or voluntarily blinking, with each saccade. During fixation of a target located straight ahead, blinks induced brief downward and nasalward deflections of eye position. When subjects looked at targets located at right or left 20 degrees, similar initial movements were made by four of the subjects, but the amplitude of the adducted eye was reduced by 65% and was followed by a larger temporalward movement. Blinks caused substantial changes in the dynamic properties of saccades. For 20 degrees saccades made with blinks, peak velocity and peak acceleration were decreased by approximately 20% in all subjects compared with saccades made without blinks. Blinks caused the duration of 20 degrees saccades to increase, on average, by 36%. On the other hand, blinks had only small effects on the gain of saccades. Blinks had little influence on the relative velocities of centrifugal versus centripetal saccades, and abducting versus adducting saccades. Three of five subjects showed a significantly increased incidence of dynamic overshoot in saccades accompanied by blinks, especially for 20 degrees movements. Taken with other evidence, this finding suggests that saccadic omnipause neurons are inhibited by blinks, which have longer duration than the saccades that company them. In conclusion, the changes in dynamic properties of saccades brought about by blinks cannot be accounted for simply by a summation of gaze perturbations produced by blinks during fixation and saccadic eye movements made without blinks. Our findings, especially the appearance of dynamic overshoots, suggest that blinks affect the central programming of saccades. These effects of blinks need to be taken into account during studies of the dynamic properties of saccades.

Memory-guided saccadic eye movements: effects of cerebellar disease.

We compared the accuracy of oblique, memory-guided saccades if the eye is stationary or moves horizontally during the memory period. We studied 11 patients with cerebellar disease and 11 age-matched control subjects. Normal subjects showed similar accuracy of saccades for both conditions. In contrast, all patients showed greater errors if the eye moved horizontally during the memory period; however, errors of both vertical and horizontal components of memory-guided saccades were similar. Thus, inaccuracy of memory-guided saccades could not be simply attributed to failure to internally monitor change in horizontal gaze during the memory period. Instead, we propose that the greater saccadic errors which occurred when gaze changed during the memory period reflected a disruption of predictive mechanisms governing eye movements.

Torsional eye movements in patients with skew deviation and spasmodic torticollis: responses to static and dynamic head roll.

We measured torsional eye movements induced by sinusoidal rotation or static tilt, of the head in roll while viewing a far or near target in 4 patients with skew deviation due to brainstem lesions, 4 patients with spasmodic torticollis (ST), 2 patients with unilateral eighth nerve section (VIIIS), and 10 normal subjects. Torsional nystagmus was present in all 4 patients with skew deviation. In subjects and patients, responses to both sinusoidal and static roll were larger while viewing the far target, consistent with factors dictated by geometry. Response gains to sinusoidal roll were abnormal in 3 patients with skew (increased in one, decreased in two), abnormal in 3 with ST (increased in 1, decreased in 2), and in abnormal both VIIIS patients (decreased). Greater abnormalities were evident in 3 skew patients while rolling away from the side of their brainstem lesions and in both VIIIS patients while rolling toward their lesioned ears. There were similar but less pronounced changes during static head roll. We conclude that patients with skew, ST, and VIIIS may all have abnormal ocular counter-rolling that is more evident during dynamic testing while viewing a far target. Such abnormalities endure because of the limited influence exerted by vision on torsional eye movements.

Evidence for independent feedback control of horizontal and vertical saccades from Niemann-Pick type C disease.

We measured the eye movements of three sisters with Niemann-Pick type C disease who had a selective defect of vertical saccades, which were slow and hypometric. Horizontal saccades, and horizontal and vertical pursuit and vestibular eye movements were similar to control subjects. The initial movement of oblique saccades was mainly horizontal and most of the vertical component occurred after the horizontal component ended; this resulted in strongly curved trajectories. After completion of the horizontal component of an oblique saccade, the eyes oscillated horizontally at 10-20 Hz until the vertical component ended. These findings are best explained by models that incorporate separate feedback loops for horizontal and vertical burst neurons, and in which the disease selectively affects vertical burst neurons.

Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion.

1. Measurements were made in four normal human subjects of the accuracy of saccades to remembered locations of targets that were flashed on a 20 x 30 deg random dot display that was either stationary or moving horizontally and sinusoidally at +/-9 deg at 0.3 Hz. During the interval between the target flash and the memory-guided saccade, the "memory period" (1.4 s), subjects either fixated a stationary spot or pursued a spot moving vertically sinusoidally at +/-9 deg at 0.3 Hz. 2. When saccades were made toward the location of targets previously flashed on a stationary background as subjects fixated the stationary spot, median saccadic error was 0.93 deg horizontally and 1.1 deg vertically. These errors were greater than for saccades to visible targets, which had median values of 0.59 deg horizontally and 0.60 deg vertically. 3. When targets were flashed as subjects smoothly pursued a spot that moved vertically across the stationary background, median saccadic error was 1.1 deg horizontally and 1.2 deg vertically, thus being of similar accuracy to when targets were flashed during fixation. In addition, the vertical component of the memory-guided saccade was much more closely correlated with the "spatial error" than with the "retinal error"; this indicated that, when programming the saccade, the brain had taken into account eye movements that occurred during the memory period. 4. When saccades were made to targets flashed during attempted fixation of a stationary spot on a horizontally moving background, a condition that produces a weak Duncker-type illusion of horizontal movement of the primary target, median saccadic error increased horizontally to 3.2 deg but was 1.1 deg vertically. 5. When targets were flashed as subjects smoothly pursued a spot that moved vertically on the horizontally moving background, a condition that induces a strong illusion of diagonal target motion, median saccadic error was 4.0 deg horizontally and 1.5 deg vertically; thus the horizontal error was greater than under any other experimental condition. 6. In most trials, the initial saccade to the remembered target was followed by additional saccades while the subject was still in darkness. These secondary saccades, which were executed in the absence of visual feedback, brought the eye closer to the target location. During paradigms involving horizontal background movement, these corrections were more prominent horizontally than vertically. 7. Further measurements were made in two subjects to determine whether inaccuracy of memory-guided saccades, in the horizontal plane, was due to mislocalization at the time that the target flashed, misrepresentation of the trajectory of the pursuit eye movement during the memory period, or both. 8. The magnitude of the saccadic error, both with and without corrections made in darkness, was mislocalized by approximately 30% of the displacement of the background at the time that the target flashed. The magnitude of the saccadic error also was influenced by net movement of the background during the memory period, corresponding to approximately 25% of net background movement for the initial saccade and approximately 13% for the final eye position achieved in darkness. 9. We formulated simple linear models to test specific hypotheses about which combinations of signals best describe the observed saccadic amplitudes. We tested the possibilities that the brain made an accurate memory of target location and a reliable representation of the eye movement during the memory period, or that one or both of these was corrupted by the illusory visual stimulus. Our data were best accounted for by a model in which both the working memory of target location and the internal representation of the horizontal eye movements were corrupted by the illusory visual stimulus. We conclude that extraretinal signals played only a minor role, in comparison with visual estimates of the direction of gaze, in planning eye movements to remembered targ

Measuring eye movements during locomotion: filtering techniques for obtaining velocity signals from a video-based eye monitor.

Video-based eye-tracking systems are especially suited to studying eye movements during naturally occurring activities such as locomotion, but eye velocity records suffer from broad band noise that is not amenable to conventional filtering methods. We evaluated the effectiveness of combined median and moving-average filters by comparing prefiltered and postfiltered records made synchronously with a video eye-tracker and the magnetic search coil technique, which is relatively noise free. Root-mean-square noise was reduced by half, without distorting the eye velocity signal. To illustrate the practical use of this technique, we studied normal subjects and patients with deficient labyrinthine function and compared their ability to hold gaze on a visual target that moved with their heads (cancellation of the vestibulo-ocular reflex). Patients and normal subjects performed similarly during active head rotation but, during locomotion, patients held their eyes more steadily on the visual target than did subjects.

Quantitative measurements of eye movements in a patient with Tullio phenomenon.

The Tullio phenomenon consists of vestibular symptoms on exposure to high-intensity acoustic stimuli, reflecting pathological stimulation of semicircular canals or otoliths. We report a patient with posttraumatic Tullio phenomenon to illustrate how precise measurement of eye movements during auditory stimulation, using the magnetic search coil technique, may characterize movements that are not clinically apparent or easily measured by other means. Such measurements in patients with surgically verified lesions may further elucidate the mechanisms responsible for this phenomenon.

Comparison of horizontal, vertical and diagonal smooth pursuit eye movements in normal human subjects.

We compared horizontal and vertical smooth pursuit eye movements in five healthy human subjects. When maintenance of pursuit was tested using predictable waveforms (sinusoidal or triangular target motion), the gain of horizontal pursuit was greater, in all subjects, than that of vertical pursuit; this was also the case for the horizontal and vertical components of diagonal and circular tracking. When initiation of pursuit was tested, four subjects tended to show larger eye accelerations for vertical as opposed to horizontal pursuit; this trend became a consistent finding during diagonal tracking. These findings support the view that different mechanisms govern the onset of smooth pursuit, and its subsequent maintenance when the target moves in a predictable waveform. Since the properties of these two aspects of pursuit differ for horizontal and vertical movements, our findings also point to separate control of horizontal and vertical pursuit.

Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes.

We studied dynamic properties of horizontal, vertical, and oblique eye movements in 23 patients with the following parkinsonian syndromes: idiopathic parkinsonism (PD), multiple system atrophy (MSA), pure akinesia (PA), progressive supranuclear palsy (PSP), and cortical-basal ganglionic degeneration (CBGD). Compared with age-matched controls, only PSP patients showed slowing of saccades. Patients in all groups showed saccadic hypometria that was most marked vertically. The trajectories of saccades made to diagonal target jumps were deviated toward the horizontal plane, due to the vertical hypometria; this was most marked in PA and PSP groups. Saccade latency was only increased in the CBGD group. Sinusoidal smooth pursuit did not differentiate between controls and patients; however, with step-ramp stimuli, pursuit eye acceleration was impaired in all patient groups compared with controls. The vestibulo-ocular reflex, with or without visual enhancement, was similar in patients and controls. These findings indicate that (1) in parkinsonian syndromes apart from PSP, the saccade-generating brainstem burst neurons are probably spared, but the signals that they receive, specifying the size and direction of saccades, are flawed; and (2) measurements of the gain and trajectory of oblique saccades, and initiation of smooth pursuit, may aid in diagnosing these different types of parkinsonism.

Tracking of illusory target motion: differences between gaze and head responses.

We compared ocular and eye-head tracking responses to an illusion of diagonal motion produced when vertical movement of a small visual target was synchronized to horizontal movement of a background display. In response to sinusoidal movement, smooth ocular pursuit followed vertical target motion, with only a small horizontal component. In response to regular stepping movement, all anticipatory saccades were in the direction of the illusion; these erroneous oblique movements were followed by corrective horizontal saccades. When the head was free to move, it usually showed a diagonal trajectory that, for both sinusoidal and stepping target motion, was always in the direction of the illusion; no corrective movements were present. Thus, for our illusory stimuli, eye and head tracking showed qualitative differences that imply that ocular tracking was ultimately controlled by actual target motion but head tracking was controlled by illusory target motion.

Head perturbations during walking while viewing a head-fixed target.

BACKGROUND: Inexpensive, head-fixed computer displays are now available that subjects can wear during locomotion. HYPOTHESIS: Viewing a head-fixed visual display will change the characteristics of rotational head perturbations during natural walking. METHODS: Using a 3-axis angular rate sensor, we measured head rotations during natural or treadmill walking, in 10 normal subjects and 2 patients with deficient vestibular function, as they attempted to view (A) a stationary target at optical infinity; and (B) a target at a distance of 20 cm rigidly attached to the head. RESULTS: Normal subjects and patients showed no significant change in the predominant frequency of head rotations in any plane (ranging 0.7-5.7 Hz) during the two different viewing tasks (p > 0.1). Mean peak head velocities (ranging 6-36 degrees.s-1) also showed no difference during the two viewing conditions except in the yaw plane, in which values were greater while viewing the near target (p < 0.005). Predominant frequencies of head rotations were similar in the pitch plane during natural or treadmill walking; however, peak velocities of pitch head rotations were substantially greater during natural walking (p < 0.05). One vestibular patient showed modest increases of head velocity during natural walking compared with normal subjects. CONCLUSIONS: Rotational head perturbations that occur during natural walking are largely unaffected when subjects view a head-fixed target. There is need to study how such perturbations, which induce vestibular eye movements, affect vision of head-fixed displays.

Modulation of high-frequency vestibuloocular reflex during visual tracking in humans.

1. Humans may visually track a moving object either when they are stationary or in motion. To investigate visual-vestibular interaction during both conditions, we compared horizontal smooth pursuit (SP) and active combined eye-head tracking (CEHT) of a target moving sinusoidally at 0.4 Hz in four normal subjects while the subjects were either stationary or vibrated in yaw at 2.8 Hz. We also measured the visually enhanced vestibuloocular reflex (VVOR) during vibration in yaw at 2.8 Hz over a peak head velocity range of 5-40 degrees/s. 2. We found that the gain of the VVOR at 2.8 Hz increased in all four subjects as peak head velocity increased (P < 0.001), with minimal phase changes, such that mean retinal image slip was held below 5 degrees/s. However, no corresponding modulation in vestibuloocular reflex gain occurred with increasing peak head velocity during a control condition when subjects were rotated in darkness. 3. During both horizontal SP and CEHT, tracking gains were similar, and the mean slip speed of the target's image on the retina was held below 5.5 degrees/s whether subjects were stationary or being vibrated at 2.8 Hz. During both horizontal SP and CEHT of target motion at 0.4 Hz, while subjects were vibrated in yaw, VVOR gain for the 2.8-Hz head rotations was similar to or higher than that achieved during fixation of a stationary target. This is in contrast to the decrease of VVOR gain that is reported while stationary subjects perform CEHT.(ABSTRACT TRUNCATED AT 250 WORDS)

Evaluation of a video tracking device for measurement of horizontal and vertical eye rotations during locomotion.

We have evaluated a video-based method for measuring binocular horizontal and vertical eye movements of human subjects by comparing it with the magnetic search coil technique. This video tracking system (VTS) uses multiple infrared light sources and small video cameras to simultaneously measure the positions of reflected corneal images and the center of the pupil. The system has a linear range of approximately +/- 40 degrees horizontally and +/- 30 degrees vertically, a sampling rate of 120 Hz (180 Hz with the head fixed), and system noise with standard deviation of < 0.04 degree. The binocular eye-tracking system is light-weight (190 g), being mounted on goggles that, with the eyes in primary position, permit a field of view of 60 degrees horizontally and vertically. The VTS is insensitive to translations of the tracker relative to the eyes. By placing the video preprocessing unit on a cart, eye movements may be recorded while subjects walk through distances up to 100 feet. In comparison with the magnetic search coil technique, the VTS generally provides reliable measurements of horizontal and vertical eye position; eye velocity is noisier than corresponding coil signals, but superior to electro-oculography.