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.     

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.     

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.     

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.     

Suppression of optokinetic velocity storage in humans by static tilt in pitch.

The effects of static tilts about the pitch axis on human horizontal optokinetic after-nystagmus OKAN (HOKAN) were examined. Static tilts in pitch produced tilt-dependent HOKAN suppression. The slow decay (indirect pathway) component (coefficient C and long time constant 1/D) of the two-component model for OKAN was significantly reduced, while the short decay (direct pathway) component (coefficient A and short time constant 1/B) remained invariant as angle of tilt was increased. These results provide further evidence that otolith organ activity can couple to horizontal velocity storage in humans, in accordance with models proposed in the literature.     

Effect of alertness and visual attention on optokinetic nystagmus in humans

The effect of alertness and visual attention on optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN) was studied in 20 volunteers. Electroencephalographic (EEG) activity was recorded over the occipital lobe. Exposure to sound and vibration caused a significant increase in the mean slow-phase velocity of OKN, whereas its maximum slow-phase velocity remained unaffected. Vibration tended to increase the mean slow-phase velocity of OKN more than sound did, though the difference was not statistically significant. Vibration also significantly increased the OKAN. When alpha rhythm appeared in the occipital EEG during OKN, the velocity of concurrent slow phases was reduced. However, the periods of alpha rhythm did not differ between the different stimulus conditions. The findings suggest that sound and vibration activate the subcortical optokinetic mechanism, thus causing an increase in the mean velocity of OKN. Abatement of visual attention is reflected in temporary reduction of OKN in conjunction with the appearance of alpha waves and is to be interpreted as transient quiescence of the cortical optokinetic mechanism.     

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.     

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.     

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.     

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.     

Transfer of optokinetic activity to vestibular nystagmus

Transfer of activity generated by prior optokinetic (OK) stimuli of one minute's duration to nystagmus induced in darkness by a subsequent vestibular stimulus consisting of step velocities to and from 40 degrees/s-1 was studied in 10 normal subjects. Four types of OK stimuli were used: (a) full field 'passive'; (b) full field 'active'; (c) full field in the presence of optic fixation, and (d) small OK drum stimulation. Transfer (T) was evident under all conditions and resulted in an enhancement of the vestibulo-ocular (VO) response when activity from the two stimuli were in the same direction (S) and a suppression when in the opposite (O). Expressed by the equation: Formula See Text. the respective transfer values obtained for the above conditions were (a) 66%, (b) 58%, (c) 22%, and (d) 54%. In all tests, rightward OK drum movement was more effective than leftward. In respect of passive OKN the resultant response can be well represented as the algebraic summation of the expected optokinetic after-nystagmus (OKAN) and the VO response, though opposing OKAN is more effective than enhancing. Passive OKN is more effective than active and this can be accounted for by the small contribution made by retinal slip in the former (the indirect path). Surprisingly, the small drum proved almost as effective as active OKN in terms of transfer. Fixation in the presence of full-field OK stimuli induces a non-directionally specific depression of the subsequent VO response, implying that retinal slip could contribute to the mechanism of VO response suppression.     

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.     

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.     

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.     

Human optokinetic afternystagmus. Effects of repeated stimulation

Normal human subjects were exposed to repeated optokinetic afternystagmus (OKAN) testing in either one direction or alternating directions of stripe movement. Sessions were conducted at intervals of either one week or several weeks. Repeated exposure to OKAN stimulation in one direction produced significant response decrements in cumulative displacement, short time constant, long time constant, and the coefficient of the long time constant component (C). The data suggest that the decrease in C and cumulative displacement occurred most noticeably between trials 3 and 4 of the first session. Retesting after 1 week, and up to 8 weeks later revealed no recovery. Repeated exposure to alternating leftward and rightward stimuli resulted in response decrement in both cumulative displacement and C. Responses to leftward stimuli were indistinguishable from responses to rightward stimuli.     

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     

Slow cumulative eye position to quantify optokinetic afternystagmus.

In 30 normal subjects we computed the slow cumulative eye position (SCEP) of optokinetic afternystagmus (OKAN) that followed 60 seconds of full-field optokinetic stimulation at 60 degrees/s. The mean SCEP was 112.8 degrees +/- 65.0 degrees. The lower and upper fifth percentile limits for directional preponderance of the SCEP were -38.8% and 44.3%, respectively. The time constant, which we calculated by dividing the SCEP by the initial velocity, was 12.0 +/- 7.4 seconds. This value is nearly identical to the time constant obtained from semilogarithmic regression of the decay of OKAN slow-phase velocity versus time. We conclude that the SCEP is a good measure of OKAN and that it reflects the substantial amount of variability and directional asymmetry observed in the optokinetic responses of normal subjects.     

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.     

The effect of saccular ablation on vertical optokinetic after-nystagmus in squirrel monkeys

Summary The effect of bilateral saccular ablation on the asymmetry of vertical optokinetic after-nystagmus (OKAN) was studied in squirrel monkeys. No significant changes occurred in the initial slow-phase eye velocity (SPEV) or the time constant of the upward or downward OKAN first phase (OKAN-I) under various stimulus conditions. However, with a protracted downward stimulus, the maximum SPEV and the number of beats of the slow-phase-up OKAN second phase (OKAN-II) significantly increased. This increase should be the result from enhancement of the downward optokinetic input. In contrast, there was only minimal change in the slow-phase-down OKAN-II. Thus, the asymmetrical dominance of the vertical OKAN (dominance upward) remained the same after saccular deafferentation. Offprint request to: M. Igarashi