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.     

Direction and angle of active head tilts influencing the Purkinje effect and the inhibition of postrotatory nystagmus I and II

Postrotatory nystagmus I and II (P I, P II) were evoked in four normal humans by velocity steps (prior velocity of rotating chair 90 degrees/s). 4 s after the stop the head was actively tilted by the subject 90 degrees forwards, backwards, to the shoulder of the previous direction of rotation -'ipsilaterally', or to the other shoulder-'contralaterally'. In control trials, the head was kept in the previous erect position. Compared with the control experiments, P I was significantly reduced by all head tilts. Inhibition of P I was strongest with forward and weakest with backward tilts. This difference is explained by the inclination of the utricular base by 30 degrees backward with respect to the horizontal of the skull and by the elastic properties of the sensory matrix. A smaller amplitude (45 degrees) of head tilt about the roll axis leads to a weaker inhibition (28.5%) than a 90 degree tilt, which corresponds to the difference of the sine of the tilt angle and thereby reflects the mechanical force acting on the receptor layer.     

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.     

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.     

Changes in the perceived head transversal plane and the subjective visual horizontal induced by Coriolis stimulation during gondola centrifugation

For studying the influence of the vertical semicircular canals on spatial orientation in roll, the subjective visual horizontal (SVH) and the subjective transversal plane of the head (STP) were measured in a situation where the vertical canals sense a roll-velocity stimulus while the otolith organs persistently signal that the head is upright in roll. During gondola centrifugation (resultant gravitoinertial force vector 2.5 G, gondola inclination 66 degrees) subjects were exposed to controlled rotational head movements (angular speed 27 degrees/s, magnitude 40 degrees) about the yaw (body z-) axis, produced by means of a motor-driven helmet. This causes a roll-plane Coriolis stimulus to the canals, while the otoliths persistently sense upright head position in roll. The subjects reported intense sensations of rotation and tilt in the roll plane. This was reflected in tilts of both the SVH and STP. The initial tilt of the SVH was 13.0 +/- 9.7 degrees (mean +/- S.D., n=10). The STP was changed in the opposite direction. The initial tilt was 23.8 +/- 12.2 degrees (mean +/- S.D., n=5). The changes in the SVH and STP were not of equal magnitude. A few subjects who had almost no deviations in the SVH showed pronounced tilts of the STP. The time constant for exponential decay of the tilts of the SVH and STP was on average approximately 1 minute. These findings indicate that a difference in activity of the vertical canals in the right versus left ear may cause substantial tilts of the SVH even if there is no asymmetry in the activity of the otolith system. Further, the canal stimulus may induce a tilt of the fundamental egocentric frame of reference.     

Effects of static orientation upon human optokinetic afternystagmus

"Normal" human subjects were placed in a series of 5 static orientations with respect to gravity and were asked to view an optokinetic display moving at a constant angular velocity. The axis of rotation coincided with the subject's rostro-caudal axis and produced horizontal optokinetic nystagmus and afternystagmus. Wall (1) previously reported that these optokinetic afternystagmus responses were not well characterized by parametric fits to slow component velocity. The response for nose-up, however, was larger than for nose-down. This suggested that the horizontal eye movements measured during optokinetic stimulation might include an induced linear VOR component as presented in the body of this paper. To investigate this hypothesis, another analysis of these data has been made using cumulative slow component eye position. Some subjects' responses had reversals in afternystagmus direction. These reversals were "filled in" by a zero slow component velocity. This method of analysis gives a much more consistent result across subjects and shows that, on average, responses from the nose-down horizontal (prone) orientation are greatly reduced (p < 0.05) compared to other horizontal and vertical orientations. Average responses are compared to responses predicted by a model previously used to predict successfully the responses to post-rotatory nystagmus after earth horizontal axis rotation. Ten of 11 subjects had larger responses in their supine than their prone orientation. Application of horizontal axis optokinetic afternystagmus for clinical otolith function testing, and implications for altered gravity experiments are discussed.     

Eye instability in the rabbit induced by vestibular stimulation in the vertical plane

OBJECTIVE: Sinusoidal vestibular stimulation in the horizontal plane induces periodic eye instability in the intact rabbit and the hypothesis of an intrinsically unstable velocity storage mechanism has been conceived. The present research examined the stability of the vestibulo-ocular reflex (VOR) in the vertical plane, considering that the time constant values of vertical and horizontal VORs differ and that separate regions of the vestibulo-cerebellum affect the horizontal and vertical slow VOR components differently. MATERIAL AND METHODS: Normal pigmented rabbits were sinusoidally oscillated in the dark about their vertical and longitudinal axes to evoke horizontal and vertical eye responses. RESULTS: Frequency and peak-to-peak amplitude stimulation parameters ranged from 0.1 to 0.8 Hz and from 5 degrees to 20 degrees, respectively. During horizontal VOR, periodic alternating drift (PAD) was superimposed on the ocular response, and both peak velocity and period were directly correlated with stimulation amplitude. Vestibular stimulation in the vertical plane induced PAD: the period of vertical PAD was shorter and the amplitude smaller than the corresponding horizontal PAD values. A further difference in vertical PAD occurred in the lack of modulation of period and peak velocity by the stimulus amplitude. CONCLUSION: These results support the hypothesis of different instabilities of the velocity storage mechanism in the vertical and horizontal planes, possibly due to separate sensory-motor systems sub-serving the vertical and horizontal VORs.     

Spatial orientation of postrotatory nystagmus during static roll tilt in cats

While the stimulation of otolith inputs reduces the duration of postrotatory nystagmus (PRN), there is still room for dialogue about the effect of static tilt on the orientation of PRN. We studied one possible influence of static roll tilt on the spatial orientation of PRN in cats. The animal was rotated about an earth-vertical axis (EVA) at a constant velocity of 100 deg/s with an acceleration and deceleration of 120 deg/s2. Within two seconds after stopping EVA rotation, the animal was passively tilted at 45 deg/s about its longitudinal axis by as much as +/- 90 deg in steps of 15 deg. Eye movements were measured with magnetic search coils. The angle of the PRN plane and its slow phase eye velocity were measured. The time constant of PRN decreased with an increase in roll tilt. The PRN plane remained earth horizontal within a range of +/- 30 deg roll tilt. Beyond this range, the velocity of PRN decreased too rapidly to measure any change in orientation. Our results indicate a spatially limited and temporally short interaction of the semicircular canal and otolith signals in the velocity storage mechanism of cat PRN. Our data, along with previous studies, suggest that different species show different solutions to the problem of the imbalance and spatial disorientation during contradictory stimuli.     

Visual-vestibular interaction in humans during earth-horizontal axis rotation

Visual-vestibular interaction (VVI) using 60 degrees/s constant velocity earth horizontal axis (EHA) yaw rotation was measured in 7 human subjects. This so-called 'barbecue spit' rotation stimulated both the horizontal semicircular canals and the otolith organs. Subjects were tested with their eyes open in the dark (EOD), while fixating upon a target rotating with them (FIX), and while observing stationary optokinetic stripes (VVR). The resulting nystagmus slow component velocity (SCV) was analyzed. During EOD, subjects showed an exponentially decaying SCV response with a time constant of between 10 and 15 s that decayed to a non-zero baseline value (bias). Superimposed was a cyclic activity, modulation, whose period equalled the time for a complete revolution of the subject. During FIX, the average value of SCV was nearly zero indicating almost complete abolition of the exponential decay and bias components. The modulation component was reduced by half. During VVR, an exponential decay was observed in most subjects and the average value of the bias component nearly equalled that of the velocity of rotation. Modulation during VVR varied on a cycle-by-cycle basis. On average, the modulation component was nearly twice that for the EOD condition. We conclude that visual-vestibular interactions during EHA differ significantly from those during rotation about the vertical; specifically, there is a non-linear interaction between linear acceleration and optokinetic nystagmus.     

Eye Instability in the Rabbit Induced by Vestibular Stimulation in the Vertical Plane

Objective—Sinusoidal vestibular stimulation in the horizontal plane induces periodic eye instability in the intact rabbit and the hypothesis of an intrinsically unstable velocity storage mechanism has been conceived. The present research examined the stability of the vestibulo-ocular reflex (VOR) in the vertical plane, considering that the time constant values of vertical and horizontal VORs differ and that separate regions of the vestibulo-cerebellum affect the horizontal and vertical slow VOR components differently. Material and Methods—Normal pigmented rabbits were sinusoidally oscillated in the dark about their vertical and longitudinal axes to evoke horizontal and vertical eye responses. Results—Frequency and peak-to-peak amplitude stimulation parameters ranged from 0.1 to 0.8 Hz and from 5° to 20°, respectively. During horizontal VOR, periodic alternating drift (PAD) was superimposed on the ocular response, and both peak velocity and period were directly correlated with stimulation amplitude. Vestibular stimulation in the vertical plane induced PAD: the period of vertical PAD was shorter and the amplitude smaller than the corresponding horizontal PAD values. A further difference in vertical PAD occurred in the lack of modulation of period and peak velocity by the stimulus amplitude. Conclusion—These results support the hypothesis of different instabilities of the velocity storage mechanism in the vertical and horizontal planes, possibly due to separate sensory-motor systems sub-serving the vertical and horizontal VORs.     

Eye movements in response to electric stimulation of the human posterior ampullary nerve

OBJECTIVES: The concept of a vestibular implant to restore balance, similar to that of a cochlear implant to restore hearing in deaf patients, has been investigated in animal models. It remains to be shown, however, that electric stimulation of the human end organ or its vestibular nerve branches is capable of eliciting a nystagmic eye movement response. METHODS: Three subjects were given electric stimulation of their posterior ampullary nerve, which was surgically exposed under local anesthesia, by a procedure developed by Gacek. The stimulus was a multiphasic, charge-balanced train of electric pulses. RESULTS: In all subjects, a pulse repetition rate of 200 pulses per second produced a robust vertical nystagmus without any apparent change in the slow component velocity of the preexisting horizontal nystagmus. CONCLUSIONS: We have been able to replicate in humans a finding somewhat similar to that of Suzuki and Cohen in monkeys for electric stimulation of the posterior semicircular canal. The similarity is an eye movement with a large, predominant vertical component. The difference is that we saw no horizontal response component, and were not able to measure a torsional response, because we used 2-dimensional video methods. In addition, we found a robust nystagmus with slow component velocities that are large enough to compensate for vertical head movements. This is an essential step in demonstrating the feasibility of a vestibular prosthesis using electric stimulation.     

Chronic unilateral loss of otolith function revealed by the subjective visual vertical during off center yaw rotation

Assessing the subjective visual vertical, SVV, in a static upright position is an easy clinical test in which a deviation of some 10 degrees from true vertical indicates an acute loss of unilateral (otolithic) vestibular function on the side to which the SVV is tilted. Because this deviation of the SVV is compensated during the following months, patients with chronic unilateral vestibular loss do no longer differ from normal subjects. This study presents an experimental set-up that allows for clear detection of compensated chronic loss of unilateral otolithic function by testing the SVV. 21 normals and 17 unilaterally vestibular deafferentiated (UVD) patients (vestibular neurectomies) were first rotated on a human centrifuge about an earth vertical yaw axis through the midsagittal plane of the head (240 degrees/s). This induced tilts of the gravito-inertial force (GIF) vectors, which differed at the two inner ears by 8 degrees. During constant velocity rotation, the subjects were moved in pseudo-randomized steps laterally up to 16 cm apart from the rotation axis, inducing roll tilts of the GIF vectors up to 16 degrees. Normal subjects set their SVV to pre-centrifugation values at positions with the midsagittal plane of their head close to the rotation axis, while chronic UVD patients indicated pre-centrifugation values during positions with the rotation axis 5.9 +/- 2.5 cm paramedian on the side of the intact ear. Tilts of the GIF vectors shifted the SVV with a gain of 0.70 in normals and only 0.32 in UVD patients. Roll gains for laterally directed GIF vectors relative to the intact inner ear did not differ from medially directed roll gains in the UVD patients. The roll gains observed in this experimental set-up were lower than those observed with static body tilts or during eccentric rotation with a larger radius, which might be at least partially due to conflicting stimulation between otolithic and extra-vestibular cues.     

Spatial orientation of periodic alternating drift (PAD)

Sinusoidal vestibular stimulation induces in the intact rabbit in prone position a periodic alternating drift (PAD), evident in the earth horizontal plane when the animal is rotated about the vertical axis but weak in the vertical one when the animal is rotated about the longitudinal axis. It has been hypothesized that these oscillations are related to an intrinsic instability of the velocity storage, due to the length of its time constant. The velocity storage has the longest time constant aligned with the vertical axis, and it changes its orientation with the gravity vector. The present research examined the spatial orientation of PAD in relation to changes of the animal position with respect to gravity. Normal pigmented rabbits were sinusoidally oscillated about their longitudinal axes to evoke vertical eye responses. The stimulation was carried out with the animal in prone position and with the animal in nose-up condition. With the animal in prone position, PAD had a weak vertical component, but an evident horizontal component was visible. When the animal was in nose-up position, the horizontal component of PAD was clearly visible, while the vertical component was negligible. In both stimulation conditions PAD period and peak velocity were not modulated by the stimulus characteristics. These results are consistent with a model of PAD based on an interaction between velocity storage and the cerebellar adaptation-habituation circuit.     

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.     

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.     

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.     

Cross-coupling between horizontal and vertical eye movements during optokinetic nystagmus and optokinetic afternystagmus elicited in microgravity

The occurrence of horizontal jerks with larger amplitudes than on Earth was observed during vertical optokinetic nystagmus in astronauts tested throughout a 7-day spaceflight. During early exposure to microgravity, a horizontal spontaneous-like nystagmus was recorded in darkness following both vertical and horizontal optokinetic stimulation. In addition, the time constant of vertical OKAN with slow phase up was larger than on the ground. These effects disappeared on flight day 2. Then, the horizontal and vertical OKAN time constants decreased, and gradually returned to the preflight values, as previously observed with the gain of the vestibulo-ocular reflex. The early changes in microgravity are in agreement with those obtained on Earth in monkeys and humans during static tilt relative to gravity. Our findings suggest that the absence of otolithic input in microgravity may have an effect on the optokinetic system which could be mediated by the velocity storage mechanism.     

Ocular torsion induced by static visual stimulation and static whole body roll

Objective. This study was aimed to improve the reliability of clinical statolith testing by quantifying the influence of visual orientation and stimulation on the statolith-ocular reflex. Materials and methods. Ocular torsion was induced in 12 healthy adults by visual stimulation and by static whole body roll with and without simultaneous visual orientation. Visual stimulation was achieved by a horizontal grating oscillating sinusoidally in a frontal plane. Visual orientation during whole body roll was established by mounting an illuminated horizontal grating either on a tilting device (head-fixed) or on the wall in the frontal plane (earth-fixed). Results. No eye torsion was observed in static visual tilts of the grating. Dynamic visual stimulation elicited substantial eye torsion. Static whole body roll in the dark induced static ocular counter-rolling. Visual orientation either head- or earth-fixed did not affect the amplitude or gain of the body roll induced ocular counter-rolling. Conclusion. Dynamic visually induced torsional eye movements can be used to test the ability of the oculomotor system to generate torsional eye movements prior to quantifying the statolith-ocular reflex. Simultaneously visual information does not affect the gain of the static statolith-ocular reflex.     

Human Visual and Vestibular Heading Perception in the Vertical Planes

Heading estimation has not previously been reported in the vertical planes. This is a potentially interesting issue because although distribution of neuronal direction sensitivities is near uniform for vertical headings, there is an overrepresentation of otolith organs sensitive to motion in the horizontal relative to the vertical plane. Furthermore, thresholds of horizontal motion perception are considerably lower than those of vertical motion which has the potential to bias heading perception. The current data from 14 human subjects (age 19 to 67) measured heading estimation in response to vestibular motion of 14 cm (28 cm/s) over a 360 ° of headings at 5 ° intervals. An analogous visual motion was tested in separate trials. In this study, earth and head vertical/horizontal were always aligned. Results demonstrated that the horizontal component of heading was overestimated relative to the vertical component for vestibular heading stimuli in the coronal (skew) and sagittal (elevation) planes. For visual headings, the bias was much smaller and in the opposite direction such that the vertical component of heading was overestimated. Subjects older than 50 had significantly worse precision and larger biases relative to that of younger subjects for the vestibular conditions, although visual heading estimates were similar. A vector addition model was fit to the data which explains the observed heading biases by the known distribution of otolith organs in humans. The greatly decreased precision with age is explained by the model with decreases in end organ numbers, and relatively greater loss of otoliths that are sensitive to vertical motion.     

Ocular torsion induced by static and dynamic visual stimulation and static whole body roll

By means of real-time infra-red video-oculography we studied eye torsion in 12 normal healthy subjects. Ocular torsion was induced by visual stimulation or static whole body roll with and without visual orientation (“head-fixed” or “earth-fixed”). Visual stimulation was achieved by a horizontal grating that oscillated sinusoidally in a frontal plane. The oscillation frequency varied from 0 to 0.6 Hz while amplitude varied from 6° to 33°. Visual orientation during whole body roll was established by mounting a 32 lx illuminated horizontal grating either on a tilting device (head-fixed) or on the wall in the frontal plane (earth-fixed). Maximum visual-induced eye torsion gain was reached at about 0.2 Hz. No eye torsion was observed in static (0 Hz) visual tilts of the grating. Maximum gain was about 0.36 at amplitudes between 6° and 10°. Eye torsion gain decreased with increasing amplitude and increasing frequency (> 0.2 Hz). Static whole body roll in the dark up to 180° clockwise and counter-clockwise induced static ocular counter rolling with a maximum amplitude of 12° and a maximum gain of 0.22. Gain decreased with increasing roll down to zero at 180°. Visual orientation with either head or earth fixed did not affect the amplitude or gain of the body roll induced ocular counter-rolling. The results are interpreted in terms of improving the reliability of clinical statolith testing and understanding the processes involved in motion sickness.