Optokinetic afternystagmus in humans: normal values of amplitude, time constant, and asymmetry

It has been suggested that the appearance of directional asymmetry and/or a reduced time constant of optokinetic afternystagmus (OKAN) might be a clinical index of vestibular imbalance. However, we do not know the limits for OKAN parameters in normal humans. Accordingly, we studied OKAN in 30 normal subjects using a "sampling" method, in which a number of values of OKAN are obtained by turning out the lights periodically during optokinetic stimulation. We found that the initial velocity of OKAN has a large intrasubject variability. Accordingly, if precision is desired so as to obtain 95% confidence that the measured mean of the initial velocity of OKAN is within 25% of the true mean in an individual subject, at least eight measurements of the initial OKAN velocity must be taken. When 12 measurements are made, all subjects had a minimum value of 5 degrees/s initial OKAN, and there was little directional asymmetry (mean of -0.47 degree/s +/- 3.13 degrees/s). The intrasubject variability of the time constant of OKAN was similar to the variability of initial OKAN velocity. However, because it is not possible to obtain repeated measures of the time constant in a short period of time, the time constant of OKAN is less likely to be useful in clinical testing.     

Human optokinetic after-nystagmus: variability in serial test results.

Test-retest variability of values for directional asymmetry in primary and secondary horizontal optokinetic after-nystagmus (OKAN I and OKAN II, respectively) was studied in 16 apparently healthy subjects. OKAN was induced by 60 s of whole-field optokinetic stimulation at speeds of 60 degrees/s and 90 degrees/s in either direction (left and right), each subject being tested on the same respective weekday once a week for 4 consecutive weeks. Values for directional asymmetry were calculated as the relative side-difference between response to drum rotation toward the right and toward the left. The subjects manifested considerable variation in values for directional asymmetry in OKAN I. This suggests prediction of a given individual's true value for directional asymmetry in OKAN I to require several measurements. On the other hand, 15/16 subjects manifested no asymmetry in OKAN II (the 16th subject was a further investigation found to have significant asymmetric caloric responses). As both OKAN I and OKAN II are known to reflect asymmetric vestibular function it is suggested that studying OKAN II may require fewer measurements of directional asymmetry, compared with studying OKAN I, when assessing the course of peripheral vestibular asymmetry.     

Effect of body positions in human optokinetic nystagmus and optokinetic after nystagmus

We determined whether whole body tilt would shift the axis of optokinetic nystagmus (OKN) and optokinetic-after nystagmus (OKAN) induced by full-field rotation at 35 degrees/sec. Fifteen normal people were positioned upright or tilted 30 degrees, 60 degrees or 90 degrees to both sides. Stripes of 5 degrees were projected on a 10-foot dome around the subject's yaw axis. Each trial lasted 45 sec. The lights were then extinguished, and the subject remained in darkness for 30 sec, while after nystagmus (OKAN) was recorded. Horizontal and vertical eye movements were recorded by video-oculography at 60 Hz. Eye position and velocity data were stored on optic disk cartridge by use of the data acquisition system. A. OKAN: For the subject in the upright position, the OKN velocity vector was aligned with both gravity and the subject's yaw axis with two minor exceptions. When the subject was tilted, a vertical OKN component (VOKN) appeared in a majority of subjects. For all 15 subjects, the mean angle of the OKN velocity vector regravity (Vectorg) was 22.6 +/- 7.2 degrees at 30 degrees tilted position. The Vectorg were 48.5 +/- 10.3 degrees at 60 degrees tilted position, and 76.4 +/- 12.6 degrees at 90 degrees tilted position. This represented shifts of the OKN velocity vector from the body axis of 7.4 degrees, 11.5 degrees and 13.6 degrees, respectively. The horizontal OKN (HOKN) gain remained unchanged in different positions. B. OKAN: The duration of HOKAN and initial slow phase velocity (SPV) of HOKAN decreased as the body position increased from upright to 30 degrees, 60 degrees and 90 degrees tilted position, respectively. The incidence and initial SPV of VOKAN and Re-Body did not change as the body position increased from upright to 30 degrees, 60 degrees and 90 degrees tilted position, respectively. Thus, VOKN was observed during HOKN as subjects were tilted and tended to vector to gravity, but VOKAN was not always observed during horizontal OKAN when subjects were tilted.     

Human optokinetic afternystagmus. Slow-phase characteristics and analysis of the decay of slow-phase velocity

Events following the extinction of lights after 1-minute exposures of naive, normal subjects to an optokinetic stimulus at 40 deg/sec have been closely examined and quantified. Mean eye displacement in each slow phase decreased from 10.12 +/- 1.61 deg during optokinetic nystagmus (OKN) to 3.36 +/- 2.32 deg during optokinetic afternystagmus (OKAN). Slow-phase duration increased from 0.26 +/- 0.03 sec during OKN to 0.45 +/- 0.195 sec during OKAN. Eye displacement per slow phase remained fairly constant during OKAN, suggesting a spatial reference for the resetting of gaze. OKAN decay is a two-component process which can be closely approximated by a sum of two exponentials, one with a short time constant of 1.15 sec and the other with a long time constant of 48.8 sec. OKAN decay commenced at a time after lights out which depended upon the presence and timing of an intervening fast phase. When a fast phase intervened, OKAN decay commenced about 230 msec after it, and about 460 msec after lights out. When lights out occurred during the fast phase, OKAN decay commenced about 340 msec later.     

Reverse optokinetic after-nystagmus generated by gaze fixation during optokinetic stimulation

Gaze fixation during optokinetic stimulation generates an after-nystagmus with a slow component towards the reverse direction of the optokinetic stimulation. The duration and maximum slow component velocity (SCV) of this "reverse OKAN" were observed by changing the duration, velocity and direction of the optokinetic stimulation in nine normal volunteers. The duration of reverse OKAN increased with increasing stimulation time but was unaffected by changes in the stimulation velocity. The maximum SCV of reverse OKAN decreased with an increase in the stimulation velocity but was not significantly affected by changes in the optokinetic stimulation time. There was no directional difference among the horizontal, upwards and downwards reverse OKANs. The reverse OKAN was thought to be generated by a mechanism different from the velocity storage mechanism which produced optokinetic nystagmus and the first phase of OKAN. Retinal slip during the optokinetic stimulation was considered to be an input to the mechanism which generated the reverse OKAN. We hypothesize that the mechanism causing the reverse OKAN may be a generator of the second phase of OKAN, which was also intimately connected with self-motion sensation during the optokinetic stimulation.     

Reverse Optokinetic After-nystagmus Generated by Gaze Fixation During Optokinetic Stimulation

Gaze fixation during optokinetic stimulation generates an after-nystagmus with a slow component towards the reverse direction of the optokinetic stimulation. The duration and maximum slow component velocity (SCV) of this "reverse OKAN" were observed by changing the duration, velocity and direction of the optokinetic stimulation in nine normal volunteers. The duration of reverse OKAN increased with increasing stimulation time but was unaffected by changes in the stimulation velocity. The maximum SCV of reverse OKAN decreased with an increase in the stimulation velocity but was not significantly affected by changes in the optokinetic stimulation time. There was no directional difference among the horizontal, upwards and downwards reverse OKANs. The reverse OKAN was thought to be generated by a mechanism different from the velocity storage mechanism which produced optokinetic nystagmus and the first phase of OKAN. Retinal slip during the optokinetic stimulation was considered to be an input to the mechanism which generated the reverse OKAN. We hypothesize that the mechanism causing the reverse OKAN may be a generator of the second phase of OKAN, which was also intimately connected with self-motion sensation during the optokinetic stimulation.     

The velocity storage mechanism in human optokinetic nystagmus

The velocity storage mechanism was studied in 12 normal human subjects. For optokinetic stimulation, we principally used step stimuli of 80 deg/sec generated by an Ohm type optokinetic stimulation drum. The charge characteristics of the velocity storage mechanism in the human optokinetic nystagmus were closely approximated by the first-degree delay formula having an average time constant of 26.1 sec. This value was much longer than that reported in other animals. The OKN slow phase eye velocity reached nearly 100% of the stimulus velocity immediately after the onset of stimuli. Then, the velocity gradually decreased during first 30 seconds to approximately 70% of the stimulus velocity, and it increased again to velocity the initial during the next 50-60 seconds of the continuous stimuli. These findings, indicating the characteristics specific in the human OKN may be related to the long time constant in the charge characteristics in human OKN as compared to other animals.     

Human optokinetic afternystagmus. Stimulus velocity dependence of the two-component decay model and involvement of pursuit

The dependence of human OKAN characteristics on optokinetic (OK) stimulus velocity was examined using the two-component double exponential model for OKAN decay. Drum velocities studied were between 10 degrees and 70 degrees deg/sec over a constant exposure period of 60 sec. Results reveal two distinct types of response: a 'low'-level response at lower drum velocities (10 degrees, 20 degrees, 30 degrees/sec) and a 'high'-level response at higher drum velocities (40 degrees, 60 degrees, 70 degrees /sec). These findings support our previous proposal that OKAN decay is a two-component process, and extend it by demonstrating that these two components have differing stimulus velocity sensitivities, as would be predicted if it were assumed that they represented direct (pursuit) and indirect (non-pursuit) pathways respectively.     

Experimental parameter estimation of a visuo-vestibular interaction model in humans

Visuo-vestibular interactions in monkeys can be accurately modelled using the classical Raphan and Cohen's model. This model is composed of direct vestibular and visual contributions to the vestibulo-ocular reflex (VOR) and of a velocity storage. We applied this model to humans and estimated its parameters in a series of experiments: yaw rotations at moderate (60°/s) and high velocities (240°/s), suppression of the VOR by a head-fixed wide-field visual stimulus, and optokinetic stimulation with measurements of optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN). We found the velocity storage time constant to be 13 s, which decreased to 8 s during visual suppression. OKAN initial velocity was 12% of the OKN stimulus velocity. The gain of the direct visual pathway was 0.75 during both visual suppression and OKN; however, the visual input to the velocity storage was higher during visual suppression than during OKN. We could not estimate the time constant of the semicircular canals accurately. Finally, we inferred from high-velocity rotations that the velocity storage saturates around 20-30°/s. Our results indicate that the dynamics of visuo-vestibular interactions in humans is similar as in monkeys. The central integration of visual cues, however, is weaker in humans.     

Human optokinetic afternystagmus. Charging characteristics and stimulus exposure time dependence in the two-component model

The dependence of human optokinetic afternystagmus (OKAN) velocity storage (charging) and optokinetic nystagmus (OKN) characteristics on optokinetic (OK) stimulus exposure time was investigated, using the two-component double exponential model for OKAN decay. Results are compatible with our previously proposed concept of two velocity storage integrators, one responsible for the short time constant decay (pursuit-mediated) and the other for the long time constant decay (OK system-mediated). The dependence of the long time constant integrator of OKAN on stimulus exposure time was clearly demonstrated. The short time constant integrator appeared to be independent of stimulus exposure time within the range studied. We conclude that the charging time-course of each component is distinct from that of the other. The time constants of each component decay were found to be invariant. A left-right asymmetry observed in both OKN and OKAN responses suggests that the integrators are direction sensitive.     

The effects of intense click sounds on velocity storage in optokinetic after-nystagmus

Vestibular evoked myogenic potentials (VEMP) occurring after click stimulation in cervical muscles are thought to be a polysynaptic response of otolith-vestibular nerve origin. In optokinetic after-nystagmus (OKAN) the direction of after-nystagmus changes and slow-phase velocity decreases with head tilt. This phenomenon may be an otolith response to the direction of gravity. We assumed that intense clicks might have some influence on OKAN via the otolith-vestibular nerve. Twelve normal subjects who showed VEMP at 75 dB normal hearing level (nHL) clicks were examined. The OKAN was recorded under four conditions: right monaural, left monaural and binaural stimulation by 75 dB nHL clicks, and absence of click stimulation. Horizontal optokinetic stimulation was applied using stepwise increasing speeds from 30 deg/s to 90 deg/s. Two seconds before the stimulus ended, clicks were sounded. The slow-phase velocity of the recorded electro-nystagmography was manually measured. There was no effect on OKAN with unilateral stimulation but binaural stimulation suppressed it. These results suggest that a velocity storage integrator is influenced by intense clicks via the otolithic area. Received: 17 November 1999 / Accepted: 30 May 2000     

Quantitative analysis of horizontal and vertical optokinetic nystagmus and optokinetic after-nystagmus in the cat

This study reported on the horizontal optokinetic nystagmus (OKN) and vertical OKN of cats under the same conditions with quantitative parameters. Using the search coil method, the horizontal and vertical OKN was investigated in 5 alert cats in an upright position. As the optokinetic stimulus, a stepped random dot pattern was used. We recorded the quantitative parameters in both the horizontal and vertical OKN (for the direct pathway parameters, initial fast rise and fast fall; for the indirect pathway parameters, steady state slow phase velocity [SPV] and the optokinetic after-nystagmus [OKAN] area) in cats. The SPV of the horizontal OKN increased with the stimulus amplitude up to 40-60 degrees/s but saturated thereafter (in some cats even more). Right and left OKN were almost symmetrical. The SPV of the downward OKN increased with the stimulus amplitude up to 20 degrees/s but saturated thereafter. This was lower than the horizontal OKN. On the other hand, the SPV of the upward OKN was weak and irregular. As for the OKAN, the right and left OKAN was also almost symmetrical. A downward OKAN was also observed but was weaker than the horizontal OKAN. A fast fall in the SPV of the OKAN was observed in the horizontal and downward OKN. On the other hand, there was little upward OKAN. OKN in cats was composed of both a direct pathway and an indirect pathway. This study suggested that directional differences of OKN were mainly responsible for the indirect pathway. Both the direct and indirect pathways of cats were smaller than those of monkeys. This suggested that the differences in OKN between cats and monkeys were mainly responsible for the direct pathway.     

Effects of prolonged optokinetic stimulation on oculomotor and locomotor balance functions

Squirrel monkeys were exposed to optokinetic stimulus (90 degrees/sec constant speed, unidirectional) for 60 min. Eye movements during and after the stimulus exposure were recorded. Comparison of the data between very early and late stages of exposure showed the oculomotor gain increase and the nystagmic frequency decline. Slow phase eye velocity of bilaterally labyrinthectomized squirrel monkeys in the late exposure stage could reach almost to the level of normal animals. Post-stimulus analysis in normal monkeys showed that amphetamine enhanced the optokinetic after-nystagmus duration, the maximum slow phase eye velocity, and the time constant. In contrast, the effect of amphetamine on reversed optokinetic after-nystagmus was not at the significant level in all parameters studied. The manifestation of directional reciprocity of optokinetic after-nystagmus was inconsistent. In bilaterally labyrinthectomized animals, ipsilateral optokinetic after-nystagmus did not appear after the stimulus cessation. Instead, immediate reversed optokinetic after-nystagmus appeared. When the normal animal was kept in the light after the stimulus cessation, slow phase eye velocity of reversed optokinetic after-nystagmus declined relatively rapidly. Reversed optokinetic after-nystagmus and vestibular evoked nystagmus were summated or deducted, in velocity domain, depending upon the direction. Optokinetically induced system imbalance did not depict when the monkey's spinal locomotor function was measured by the platform runway test with the availability of vision.     

Effects on the optokinetic system of midline lesions in the pretectum of monkeys

The nucleus of the optic tract (NOT), an important visuo-motor relay between the retina and preoculomotor structures, is responsible for mediating horizontal optokinetic nystagmus (OKN) in monkeys, cats, rabbits and rats. In addition to its projection to the vestibular nuclei, the NOT has a prominent projection to the contralateral NOT via the posterior commissure. In order to evaluate the role of the commissural fibers between the NOTs in OKN, we cut the posterior commissure in three Macaca fuscata. The animals viewed the OKN stripes under three conditions: right eye viewing, left eye viewing, and both eyes viewing. OKN was recorded in response to counter-clockwise and clockwise stimulation at stimulus velocities of 30 degrees/s, 60 degrees/s and 90 degrees/s. After control data were gathered, the posterior commissure was transected with an operating knife. Before the animal was sacrificed, biocytin, an anterograde tracer, was injected into the left NOT in order to confirm that all of the commissural fibers had been cut. Although the midline lesions decreased the initial rapid rise and steady state OKN slow-phase velocity in all three animals, there were no directional differences observed during monocular clockwise or counter-clockwise visual stimulation to either eye. In two of the three animals, there were no significant differences in the time-constants of optokinetic after nystagmus (OKAN) after the lesion. In the remaining animal, the time-constants decreased at stimulus velocities of 30 degrees/s and 60 degrees/s. In conclusion, gain reduction in the rapid rise and steady state slow-phase velocity of OKN can be explained by removal of an excitatory signal mediated by commissural fibers to inhibitory interneurons in the contralateral NOT. However, interrupting the commissural fibers had no effect on the velocity storage mechanism, because the time-constants of OKAN mostly remained largely unchanged by the lesion.     

Vestibular velocity step test and normal limits for the Chinese]

Vestibular velocity steps test (VVST) to impulsive stimulus of horizontal rotation (90 degrees/S and 180 degrees/S) were performed in 22 normal subjects. Gain (G) was defined as the ratio of the initial slow phase eye velocity (ISPV) to head velocity. The time constant (T) was the time to find the point where it was 0.37 of ISPV. Duration (D) of induced nystagmus was the time between first and final nystagmus. The directional preponderance (DP) for G, T and D was calculated from the formula, (R-L)/(R+L) x 100%. These normal limits were 0.37-1.09 and 0.27-0.83 for G, 8.0--20.4s and 6.5-17.3s for T, 30.4-65.0s and 30.0-54.4s for D, +/- 21.4% and +/- 21.5% for DP(G), +/- 24.2% and +/- 20.3% for DP(T), +/- 16.5% and +/- 17.9% for DP(D) of 90 degrees/S and 180 degrees/S, respectively. The advantages and shortcomings of VVST and its value were discussed.     

Optokinetic nystagmus and after-nystagmus during a 6 hour bedrest study

CONCLUSIONS: A lengthy alteration of gravity direction produced different effects on the intrinsic horizontal and vertical optokinetic oculomotor systems. OBJECTIVE: To examine both optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN) in a 6 h 6 degrees head-down bedrest study, in which the subjects were kept lying under simulated micro-gravity conditions. SUBJECTS AND METHODS: In six normal healthy adults, we repeatedly (five times) and comparatively studied OKN and OKAN evoked by horizontal and vertical stimuli. Stage 1 was an upright sitting position. During the 6 h bedrest condition, we studied OKN and OKAN in 90 degrees recumbent lateral positions (stages 2, 3, and 4). In stage 5 the subject returned to an upright position. RESULTS: We confirmed that the change in gravity direction had various effects on the condition of OKN and OKAN. Also, we found that it took more than 3 h to reach a desirable level of systemic adaptive modification to the unique environmental condition. We considered that the early change was basically due to the changes in sensory inputs through the otolith organs, and the latter changes represented the adaptive process of the spatial orientation system. During the tilt, the occurrence rates of both horizontal and vertical OKANs were decreased; however, the conditions of these changes were different.     

Effect of vestibulo-cerebellar lesions on asymmetry of vertical optokinetic functions in the squirrel monkey

The role of the cerebellar uvula and nodulus in vertical optokinetic after-nystagmus (OKAN) was studied in 4 squirrel monkeys. Aspiration ablation of the uvula and nodulus resulted in no significant change in the initial or peak gain of vertical optokinetic nystagmus (OKN) during the 24-week post-operative observation. However, the asymmetry of vertical OKAN was significantly altered. Using a protracted upward OK stimulus, slow phase-down OKAN-II, which was not seen pre-operatively, was significantly increased. In contrast, a downward OK stimulus produced little change in slow phase-up OKAN-II. Thus, the asymmetric degree of vertical OKAN-II was decreased after uvulonodulectomy. In addition, there was a post-operative reduction in the vertical oculomotor stability. When slow-phase eye velocity of OKAN was plotted along the time scale, the amplitude and frequency of the sinusoidal pattern was increased. OKAN-III and OKAN-IV were found in 50% of the monkeys after uvulonodulectomy. It is therefore thought that inhibition and directional control from the uvula and nodulus influence the stability and asymmetrical behaviour of the leaky integrator in the second order output system.     

Galvanically induced asymmetric optokinetic after-nystagmus

The effect of an asymmetric vestibular input on the symmetry of horizontal optokinetic after-nystagmus (OKAN) was studied in twenty healthy subjects. Optokinetic nystagmus (OKN) was elicited by a whole-field optokinetic drug, rotating at 90 degrees/s, and eye-movements were recorded by a DC electro-oculographic technique (EOG). The ratio of OKAN following right and left-beating OKN respectively was computed. An asymmetric vestibular input was generated by a continuous bi-polar, bi-aural galvanic stimulus (1 mA) to the vestibular nerves during the optokinetic stimulation and the recording of the OKAN. During galvanic stimulation the relation between left and right-beating OKAN was asymmetric, compared with the OKAN found after optokinetic stimulation only. The galvanic stimulus caused a preponderance for OKAN with the fast phase beating toward the cathode. Thus, the small vestibular asymmetry induced by the galvanic stimulus, which was not strong enough to produce nystagmus by itself, caused an asymmetric OKAN. These findings suggest that examination of OKAN may be of value to detect small vestibular asymmetries in peripheral vestibular disorders in man.     

Asymmetry of vertical optokinetic after-nystagmus in squirrel monkeys

Asymmetry of vertical optokinetic after-nystagmus (OKAN) was studied in 6 squirrel monkeys. The slow-phase eye velocity (SPEV) of upward OKAN first-phase (OKAN-I) increased with increasing stimulus velocity, whereas the SPEV of downward OKAN-I diminished. The time constant of OKAN-I was shortened with the increase in stimulus speed in both directions. With a downward stimulus, the short stimulus duration failed to produce OKAN second-phase (OKAN-II) (upward slow-phase); however, with an increase in stimulus duration, the percentage appearance increased. There was no change in percentage appearance, regardless of the duration of upward stimulus. The asymmetry of OKAN-I and that of OKAN-II differed to a certain degree.     

Effect of otolith end organ ablation on horizontal optokinetic nystagmus, and optokinetic afternystagmus in the squirrel monkey.

Horizontal optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN) (stimulus speed 0-200 degrees/sec with 1 degree/sec constant angular acceleration) were examined before and after utriculo-sacculectomy (bilateral, two-stage) in squirrel monkeys. OKN exhibited a slight decline only after bilateral otolith and organ ablations. OKAN showed a minimal decline after unilateral operation but no change after bilateral operations. Severe OKN reduction and disappearance of OKAN after bilateral labyrinthectomy in primates should basically reflect the elimination of inputs from the cristae ampullares, and not from the maculae.