The effect of gravity on the horizontal and vertical vestibulo-ocular reflex in the rat

Horizontal and vertical eye movements were recorded in alert pigmented rats using chronically implanted scleral search coils or temporary glue-on coils to test the dependence of the vestibulo-ocular reflex (VOR) upon rotation axis and body orientation. The contributions of semicircular-canal versus otolith-organ signals to the VOR were investigated by providing canal-only (vertical axis) and canal plus otolith (horizontal axis) stimulation conditions. Rotations that stimulated canals only (upright yaw and nose-up roll) produced an accurate VOR during middle- and high-frequency rotations (0.2-2 Hz). However, at frequencies below 0.2 Hz, the canal-only rotations elicited a phase-advanced VOR. The addition of a changing gravity stimulus, and thus dynamic otolith stimulation, to the canal signal (nose-up yaw, on-side yaw, and upright roll) produced a VOR response with accurate phase down to the lowest frequency tested (0.02 Hz). In order to further test the dependence of the VOR on gravitational signals, we tested vertical VOR with the head in an inverted posture (inverted roll). The VOR in this condition was advanced in phase across all frequencies tested. At low frequencies, the VOR during inverted roll was anticompensatory, characterized by slow-phase eye movement in the same direction as head movement. The substantial differences between canalonly VOR and canal plus otolith VOR suggest an important role of otolith organs in rat VOR. Anticompensatory VOR during inverted roll suggests that part of the otolith contribution arises from static tilt signals that are inverted when the head is inverted.     

Torsional vestibulo-ocular reflex during whole-body oscillation in the upright and the supine position.

In rhesus monkeys, the dynamic properties of the torsional vestibulo-ocular reflex (VOR) are modified by otolith input: compared with torsional oscillations about an earth-vertical axis (canal-only stimulation), the phase lead observed at frequencies below 0.1 Hz is cancelled when the animals are rotated about an earth-horizontal axis (canal-and-otolith stimulation); the gains of the torsional VOR, however, are nearly identical in both conditions. To test whether or not canal-otolith interaction in humans is similar to that in rhesus monkeys, we examined ten healthy human subjects on a three-axis servo-controlled motor-driven turntable. The subjects were oscillated in upright or supine position in complete darkness over a similarly wide range of frequencies (0.05-1.0 Hz) with peak velocities <40 degrees/s. Eye movements were recorded using the three-dimensional search coil technique. Compared with the torsional vestibulo-ocular gains during canal-stimulation only (earth-vertical axis), the gains obtained during combined canal-otolith-stimulation (earth-horizontal axis) were significantly higher throughout the entire frequency range (P<0.05). The gain increased by 0.100+/-0.074 (SD), independent of frequency. During the earth-horizontal axis stimulation, the phase remained always around zero, which is in contrast to the canal-stimulation only, during which one finds an increasing phase lead as frequency decreases. We conclude that, in healthy humans as in rhesus monkeys, the phase lead from the canal signals at low frequencies is effectively cancelled by the otolith input. In contrast to rhesus monkeys, however, otolith signals in healthy humans increase the gain of the torsional VOR at frequencies from 0.05 to 1.0 Hz. This normal database is crucial for the interpretation of results obtained in patients with vestibular disorders.     

Changes in the dynamics of the vertical vestibulo-ocular reflex due to linear acceleration in the frontal plane of the cat

Summary The vertical and horizontal components of the vestibulo-ocular reflex (VOR) were recorded in alert, restrained cats who were placed on their sides and subjected to whole-body rotations in the horizontal plane. The head was either on the axis or 45 cm eccentric from the axis of rotation. During off-axis rotation there was a change in the linear force acting on the otolith organs due to the presence of a centripetal acceleration along the animal's vertical axis. Otolith forces (defined to be opposite to the centripetal acceleration) directed ventrally with respect to the animal (negative) decreased both the amplitude and time constant of the first-order approximation to the slow phase eye velocity of the vertical vestibulo-ocular reflex (VVOR). Otolith forces directed dorsally (positive) increased the amplitude and time constant. The effects were greater for the up VOR. The asymmetry in the VVOR time constant also depended on the otolith forces, being less in the presence of negative otolith forces that caused the resultant otolith force to move ventrally, towards the direction along which gravity normally acts when the animal is in the upright position. The effects of otolith forces on the up VVOR were independent of whether the animals were tested in the dark or in the light with a stationary visual surround (i.e., during visual suppression). In contrast, the changes in the time constant of the down VVOR were smaller during visual suppression. Simulations of the eye velocity storage mechanism suggest that the gain of the feedback in the storage integrator was modified by the angle between the resultant otolith force and an animal-fixed reference. This could be the animal's vertical, i.e., the direction along which gravity normally acts. For larger angles the feedback was less and the amplitude and time constant of the VVOR increased. The transformation of the otolith input was the same for both the up and down VOR, even though the final effect on the eye velocity was asymmetric (larger for up VOR) due to a separate, asymmetric gain element in the velocity storage feedback pathway.     

The horizontal vestibulo-ocular reflex during linear acceleration in the frontal plane of the cat

Summary Horizontal and vertical eye movements were recorded in alert, restrained cats that were subjected to whole-body rotations with the horizontal semicircular canals in the plane of rotation and the body centered on the axis or 45 cm eccentric from the axis of rotation. Changes in the horizontal vestibulo-ocular reflex (HVOR) due to the resultant of the linear forces (i.e., gravity and linear acceleration) acting on the otolith organs were examined during off-axis rotation when there was a centripetal acceleration along the animal's interaural axis. The HVOR time constant was slightly shortened when the resultant otolith force was not parallel to the animal's vertical axis. This effect was independent of the direction of the otolith force relative to the direction of the slow phase eye velocity. No effect on the HVOR amplitude was observed. In addition to changes in the HVOR dynamics, a significant vertical component of eye velocity was observed during stimulation of the horizontal canals when the resultant otolith force was not parallel with the animal's vertical axis. The effect was greater for larger angles between the resultant otolith force and gravity. An upward or downward component was elicited, depending on the direction of the horizontal component of eye velocity and the direction of the resultant otolith force. The vertical component was always in the direction that would tend to align the eye velocity vector with the resultant otolith force and keep the eye movement in a plane that had been rotated by the angle between the resultant otolith force and gravity.     

Unilateral vestibular deafferentation causes permanent impairment of the human vertical vestibulo-ocular reflex in the pitch plane

Rapid, passive, unpredictable, low-amplitude (10–20°), high-acceleration (3000–000°/s²) head rota tions were used to study the vertical vestibulo-ocular reflex in the pitch plane (pitch-vVOR) after unilateral vestibular deafferentation. The results from 23 human subjects who had undergone therapeutic unilateral vestibular deafferentation were compared with those from 19 normals. All subjects were tested while seated in the upright position. Group means and two-tailed 95% confidence intervals are reported for the pitch-vVOR gains in normal and unilateral vestibular deafferented subjects. In normal subjects, at a head velocity of 125°/s the pitch-vVOR gains were: upward 0.89±0.06, down ward 0.91±0.04. At a head velocity of 200°/s, the pitchvVOR gains were: upward 0.92±0.06, downward 0.96±0.04. There was no significant up-down asymme try. In the 15 unilateral vestibular deafferented subjects who were studied more than 1 year after unilateral vestibular deafferentation, the pitch-vVOR was signifi cantly impaired. At a head velocity of 125°/s the pitchvVOR gains were: upward 0.67±0.11, downward 0.63 ± 0.07. At a head velocity of 200°/s, the pitch-vVOR gains were: upward 0.67±0.07, downward 0.58±0.06. There was no significant up-down asymmetry. The pitch-vVOR gain in unilateral vestibular deafferented subjects was significantly lower (P<0.05) than the pitch-vVOR gain in normal subjects at the same head velocities. These results show that total, permanent uni lateral loss of vestibular function produces a permanent symmetrical 30% (approximately) decrease in pitchv-VOR gain. This pitch-vVOR deficit is still present more than 1 year after deafferentation despite retinal slip velocities greater than 30°/s in response to head accelerations in the physiological range, indicating that compensation of pitch-vVOR function following unilat eral vestibular deafferention remains incomplete.     

Influence of eye and head position on the vestibulo-ocular reflex

Summary For the vestibulo-ocular reflex (VOR) to function properly, namely to ensure a stable retinal image under all circumstances, it should be able to take into account varying eye positions in the orbit and varying orientations of the head with respect to the axis about which it is rotating. We tested this capability by quantifying the gain and the time constant of the horizontal component of the VOR during rotation about an earth vertical axis when the line of sight (optical axis) was moved out of the plane of head rotation — either by rotating the eyes up or down in the orbit or by pitching the head up or down with respect to earth-horizontal. In either case the gain of the horizontal component of the VOR was attenuated precisely by the cosine of the angle made between the optical axis and the plane of head rotation. Furthermore, if the head was pitched up or down but the eye rotated oppositely in the orbit so as to keep the line of sight in the plane of head rotation the gain of the horizontal component of the VOR was the same value as with the head and eyes both straight ahead. In contrast, the time constant of the VOR varied only as a function of the orientation of the head and not as a function of eye position in the orbit. During rotation about an earth vertical axis, the time constant was longest (about 18 s) when the head was pitched forward to place the lateral canals near earth-horizontal and shortest (about 11 s) when the head was pitched backward to place the vertical canals near earth-horizontal. Finally, since during rotation in yaw the pattern of stimulation of the lateral and vertical semicircular canals varies with different head orientations one can use measurements of the horizontal component of the VOR, under varying degrees of pitch of the head, to calculate the relative ability of the lateral and vertical semicircular canals to transduce head velocity.Dr. Fetter is a visiting scientist from the Neurologische Universitätsklinik, Eberhard-Karls-Universität, Liebermeisterstr. 18-20, D-7400 Tübingen, Federal Republic of Germany     

Initial vestibulo-ocular reflex during transient angular and linear acceleration in human cerebellar dysfunction

During transient, high-acceleration rotation, performance of the normal vestibulo-ocular reflex (VOR) depends on viewing distance. With near targets, gain (eye velocity/head velocity) enhancement is manifest almost immediately after ocular rotation begins. Later in the response, VOR gain depends on both head rotation and translation; gain for near targets is decreased for rotation about axes anterior to the otoliths and augmented for rotation about axes posterior to the otoliths. We sought to determine whether subjects with cerebellar dysfunction have impaired modification of the VOR with target distance. Eleven subjects of average age 48 +/- 16 years (mean +/- standard deviation, SD) with cerebellar dysfunction underwent transients of directionally unpredictable whole-body yaw rotation to a peak angular acceleration of 1000 or 2800 degrees/s2 while viewing a target either 15 cm or 500 cm distant. Immediately before onset of head rotation, the lights were extinguished and were relit only after the rotation was completed. The axis of head rotation was varied so that it was located 20 cm behind the eyes, 7 cm behind the eyes (centered between the otoliths), centered between the eyes, or 10 cm anterior to the eyes. Angular eye and head positions were measured with magnetic search coils. The VOR in subjects with cerebellar dysfunction was compared with the response from 12 normal subjects of mean age 25 +/- 4 years. In the period 35-45 ms after onset of 2800 degrees/s2 head rotation, gain was independent of rotational axis. In this period, subjects with cerebellar dysfunction had a mean VOR gain of 0.5 +/- 0.2, significantly lower than the normal range of 1.0 +/- 0.2. During a later period, 125-135 ms after head rotation about an otolith-centered axis, subjects with cerebellar dysfunction had a mean VOR gain of 0.67 +/- 0.46, significantly lower than the value of 1.06 +/- 0.14 in controls. Unlike normal subjects, those with cerebellar dysfunction did not show modification of VOR gain with target distance in the early response and only one subject showed a correct effect of target distance in the later response. The effect of target distance was quantitatively assessed by subtracting gain for a target 500 cm distant from gain for a target 15 cm distant. During the period 35-45 ms after the onset of 2800 degrees/s2 head motion, only two subjects with cerebellar loss demonstrated significant VOR gain enhancement with a near target, and both of these exhibited less than half of the mean enhancement for control subjects. During the later period 125-135 ms after the onset of head rotation, when VOR gain normally depended on both target location and otolith translation, only one subject with cerebellar dysfunction consistently demonstrated gain changes in the normal direction. These findings support a role for the cerebellum in gain modulation of both the canal and otolith VOR in response to changes in distance. The short latency of gain modification suggests that the cerebellum may normally participate in target distance-related modulation of direct VOR pathways in a manner similar to that found in plasticity induced by visual-vestibular mismatch.     

Absence of vestibular habituation of the vestibulo-ocular reflex in the vertical plane in the cat

 The effect of exposure to repeated angular velocity steps about the earth-vertical axis on the vertical vestibulo-ocular reflex (VOR) during onside pitch rotation was investigated in normal cats. By contrast with the VOR in the horizontal plane, the amplitude and duration of the vertical VOR did not progressively decrease throughout the repetition of velocity steps alternated in both directions. Instead, the amplitude of VOR decreased by about 40% during the very first trials in naive cats and then stayed unchanged with repeated stimuli. Habituation of the amplitude of the vertical VOR was observed when the velocity steps were always directed in the same direction. However, the duration of the vertical VOR did not show any signs of habituation. The habituation of the amplitude of the vertical VOR during unidirectional training was due to the progressive development of an initial inhibition of the VOR. This initial inhibition appeared much earlier during the bidirectional protocol, and was presumably responsible for the larger reduction in VOR amplitude observed during the very first session. These results support the model of two distinct mechanisms for VOR habituation, one producing an increasing inhibition of nystagmus, and the other depressing the response duration, and suggest that only the first mechanism is generated during repeated stimulation in the vertical plane. The low-frequency information provided by the velocity storage mechanism during onside pitch rotation, when the otoliths are positioned so they do not signal head tilt relative to gravity, could prevent a decrease in the overall response by the second mechanism. Received: 25 March 1996 / Accepted: 29 January 1997     

European vestibular experiments on the Spacelab-1 mission: 6. Yaw axis vestibulo-ocular reflex

Summary In two Spacelab-1 crew members the lateral eye movements evoked by active angular oscillation of the head in yaw at 1 Hz were recorded in-flight and post-flight. In one, the responses to passive angular oscillation in yaw at 0.2–1 Hz were also studied pre and post-flight. In the absence of visual fixation there was no significant change in the gain of either the active or passive vestibulo-ocular reflex (VOR) attributable to exposure to microgravity. However, when the subject fixated on a visual target that moved with his head the suppressed VOR gain was lower on the first post-flight test (performed 16 h after landing) than that obtained pre-flight or on subsequent post-flight tests.     

Influence of gravity on cat vertical vestibulo-ocular reflex

Summary The vertical vestibulo-ocular reflex (VOR) was recorded in cats using electro-oculography during sinusoidal angular pitch. Peak stimulus velocity was 50°/s over a frequency range from 0.01 to 4.0 Hz. To test the effect of gravity on the vertical VOR, the animal was pitched while sitting upright or lying on its side. Upright pitch changed the cat's orientation relative to gravity, while on-side pitch did not. The cumulative slow component position of the eye during on-side pitch was less symmetric than during upright pitch. Over the mid-frequency range (0.1 to 1.0 Hz), the average gain of the vertical VOR was 14.5% higher during upright pitch than during on-side pitch. At low frequencies (<0.05 Hz) changing head position relative to gravity raised the vertical VOR gain and kept the reflex in phase with stimulus velocity. These results indicate that gravity-sensitive mechanisms make the vertical VOR more compensatory.     

Dynamic otolith stimulation improves the low frequency horizontal vestibulo-ocular reflex

Summary The horizontal vestibulo-ocular reflex was measured electrooculographically in four cats during sinusoidal rotations in the dark at frequencies from 0.01 Hz to 1.0 Hz in five body orientations. Vertical axis rotations in the prone and supine positions were used to stimulate horizontal canals only. Horizontal axis rotations, with the cat on the left or right side or nose down (pitched 90° from prone) were used to stimulate horizontal canal plus otolith organs. At frequencies below 0.05 Hz the horizontal vestibulo-ocular reflex produced by horizontal canal plus otolith stimulation showed a more accurately compensatory response than the horizontal vestibuloocular reflex produced by horizontal canal stimulation alone. Canal plus otolith horizontal vestibulo-ocular reflex gain and phase remained relatively constant across all frequencies, while the horizontal vestibulo-ocular reflex gain and phase from orientations involving canal stimulation alone changed dramatically as rotation frequency decreased. In addition, the reflex in the supine position showed gain decreases and phase advances at higher frequencies than in the prone position.     

The human horizontal vestibulo-ocular reflex during combined linear and angular acceleration

 We employed binocular magnetic search coils to study the vestibulo-ocular reflex (VOR) and visually enhanced vestibulo-ocular reflex (VVOR) of 15 human subjects undergoing passive, whole-body rotations about a vertical (yaw) axis delivered as a series of pseudorandom transients and sinusoidal oscillations at frequencies from 0.8 to 2.0 Hz. Rotations were about a series of five axes ranging from 20 cm posterior to the eyes to 10 cm anterior to the eyes. Subjects were asked to regard visible or remembered targets 10 cm, 25 cm, and 600 cm distant from the right eye. During sinusoidal rotations, the gain and phase of the VOR and VVOR were found to be highly dependent on target distance and eccentricity of the rotational axis. For axes midway between or anterior to the eyes, sinusoidal gain decreased progressively with increasing target proximity, while, for axes posterior to the otolith organs, gain increased progressively with target proximity. These effects were large and highly significant. When targets were remote, rotational axis eccentricity nevertheless had a small but significant effect on sinusoidal gain. For sinusoidal rotational axes midway between or anterior to the eyes, a phase lead was present that increased with rotational frequency, while for axes posterior to the otolith organs phase lag increased with rotational frequency. Transient trials were analyzed during the first 25 ms and from 25 to 80 ms after the onset of the head rotation. During the initial 25 ms of transient head rotations, VOR and VVOR gains were not significantly influenced by rotational eccentricity or target distance. Later in the transient responses, 25–80 ms from movement onset, both target distance and eccentricity significantly influenced gain in a manner similar to the behavior during sinusoidal rotation. Vergence angle generally remained near the theoretically ideal value during illuminated test conditions (VVOR), while in darkness vergence often varied modestly from the ideal value. Regression analysis of instantaneous VOR gain as a function of vergence demonstrated only a weak correlation, indicating that instantaneous gain is not likely to be directly dependent on vergence. A model was proposed in which linear acceleration as sensed by the otoliths is scaled by target distance and summed with angular acceleration as sensed by the semicircular canals to control eye movements. The model was fit to the sinusoidal VOR data collected in darkness and was found to describe the major trends observed in the data. The results of the model suggest that a linear interaction exists between the canal and otolithic inputs to the VOR. Received: 1 April 1996 / Accepted: 15 October 1996     

Somatosensory input influences the vestibulo-ocular reflex

To evaluate the influence of somatosensory input on the vestibulo-ocular reflex (VOR), we used sinusoidal rotation tests in 19 young, healthy volunteers. For the control condition, subjects were sinusoidally rotated in complete darkness and with eyes opened at a frequency of 0.2 Hz with a maximum angular velocity of 30°/s for 30 s, and at frequencies of 0.4 and 0.8 Hz with a maximum angular velocity of 60°/s for 30 s. Sinusoidal tests were performed at earth vertical axis rotation (EVAR). For the experimental condition, we introduced somatosensory stimulation as subjects were sinusoidally rotated at the control parameters. Subjects were told to grasp an earth-fixed metallic bar with their right hands. Thus, their right arms continued to move as the rotating chair apparatus moved. We observed a significant increment (34%) in VOR gain change only at 0.2 Hz EVAR when subjects held the bar compared to that of the controls, who did not hold the bar. Gain change did not differ significantly across the other conditions. We hypothesize that arthrokinetic input (i.e., arm movement) had an additive effect on VOR in this study. This input might relate to a low-frequency component that strongly enhances the velocity storage system. Our findings have applications to types of vestibular rehabilitation regimens that implement somatosensory input.     

The response of vestibulo-ocular reflex pathways to electrical stimulation after canal plugging

The vestibulo-ocular reflex (VOR) allows clear vision during head movements by generating compensatory eye movements. Its response to horizontal rotation is reduced after one horizontal semicircular canal is plugged, but recovers partially over time. The majority of VOR interneurons contribute to the shortest VOR pathway, the so-called three-neuron arc, which includes only two synapses in the brainstem. After a semicircular canal is plugged, transmission of signals by the three-neuron arc originating from the undamaged side may be altered during recovery. We measured the oculomotor response to single current pulses delivered to the vestibular labyrinth of alert cats between 9 h and 1 month after plugging the contralateral horizontal canal. The same response was also measured after motor learning induced by continuously-worn telescopes (optically induced motor learning). Optically induced learning did not change the peak velocity of the evoked eye movement (PEEV) significantly but, after a canal plug, the PEEV increased significantly, reaching a maximum during the first few post-plug days and then decreasing. VOR gain also showed transient changes during recovery. Because the PEEV occurred early in the eye movement evoked by a current pulse, we think the observed increase in PEEV represented changes in transmission by the three-neuron arc. Sham surgery did not result in significant changes in the response to electrical stimulation or in VOR gain. Our data suggest that different pathways and processes may underlie optically induced motor learning and recovery from plugging of the semicircular canals. Electronic Publication     

The human vertical vestibulo-ocular reflex during combined linear and angular acceleration with near-target fixation

The purpose of this study was to examine the effect of fixation target distance on the human vestibuloocular reflex (VOR) during eccentric rotation in pitch. Such rotation induces both angular and linear acceleration. Eight normal subjects viewed earth-fixed targets that were either remote or near to the eyes during wholebody rotation about an earth-horizontal axis that was either oculocentric or 15 cm posterior (eccentric) to the eyes. Eye and head movements were recorded using magnetic search coils. Using a servomotor-driven chair, passive whole-body rotations were delivered as trains of single-frequency sinusoids at frequencies from 0.8 to 2.0 Hz and as pseudorandom impulses of acceleration. In the light, the visually enhanced VOR (VVOR) was recorded while subjects were asked to fixate targets at one of several distances. In darkness, subjects were asked to remember targets that had been viewed immediately prior to the rotation. In order to eliminate slip of the retinal image of a near target when the axis of rotation of the head is posterior to the eyes, the ideal gain (compensatory eye velocity divided by head velocity) of the VVOR and VOR must exceed 1.0. Both the VOR and VVOR were found to have significantly enhanced gains during sinusoidal and pseudorandom impulses of rotation (P<0.05). Enhancement of VVOR gain was greatest at low frequencies of head rotation and decreased with increasing frequency. However, enhanced VOR gain only slightly exceeded 1.0, and VVOR gain enhancement was significantly lower than the expected ideal values for the stimulus conditions employed (P<0.05). During oculocentric rotations with near targets, both the VOR and VVOR tended to exhibit small phase leads that increased with rotational frequency. In contrast, during eccentric rotations with near targets, there were small phase lags that increased with frequency. Visual tracking contributes during ocular compensatory responses to sustained head rotation, although the latency of visual tracking reflexes exceeds 100 ms. In order to study initial vestibular responses prior to modification by visual tracking, we presented impulses of head acceleration in pseudorandom sequence of initial positions and directions, and evaluated the ocular response in the epoch from 25 to 80 ms after movement onset. As with sinusoidal rotations, pseudorandom eccentric head rotation in the presence of a near, earth-fixed target was associated with enhancement of VVOR and VOR gains in the interval from 25 to 80 ms from movement onset. Despite the inability of visual tracking to contribute to these responses, VVOR gain significantly exceeded VOR gain for pseudorandom accelerations. This gain enhancement indicates that target distance and linear motion of the head are considered by the human ocular motor system in adjustment of performance of the early VOR, prior to a contribution by visual following reflexes. Vergence was appropriate to target distance during all VVOR rotations, but varied during VOR rotations with remembered targets. For the 3-m target distance, vergence during the VOR was stable over each entire trial but slightly exceeded the ideal value. For the 0.1-m near target, instantaneous vergence during the VOR typically declined gradually in a manner not corresponding to the time course of instantaneous VOR gain change; mean vergence over entire trials ranged from 60 to 90% of ideal, corresponding to target distances for which ideal gain would be much higher than actually observed. These findings suggest a dissociation between vergence and VOR gain during eccentric rotation with near targets in the frequency range from 0.8 to 2.0 Hz.     

The initial vestibulo-ocular reflex and its visual enhancement and cancellation in humans

The gain (ratio of eye velocity to head velocity) of the initial horizontal vestibulo-ocular reflex (VOR) was calculated in 12 normal subjects over 350 ms during impulsive, unpredictable whole body rotation under three conditions: (1) darkness; (2) visual enhancement of the VOR, while the subjects fixated a stationary target; and (3) visual cancellation of the reflex, while subjects fixated a target that rotated with the head. The gain of the initial 80 ms of compensatory eye movement increased significantly during visual fixation in 5 subjects and decreased during attempted VOR cancellation in 3 subjects, when compared with VOR gain in darkness. Compensatory vestibular smooth eye movements were slowed, becoming curved at the onset of VOR cancellation, at mean latencies ranging from 78 to 149 ms in individual subjects (group mean 128 ms). At about 190 ms, quick phases moved the eyes in the same direction as head and target motion. The subsequent vestibular eye movements were about 50% slower than the initial smooth eye movements, indicating more effective cancellation. Visual enhancement of the VOR can occur prior to the onset of pursuit, providing evidence that fixation and smooth pursuit are distinct ocular motor systems. Visual cancellation of the VOR also begins prior to smooth pursuit initiation and becomes more effective after the latency of smooth pursuit.     

Impairments in the initial horizontal vestibulo-ocular reflex of older humans

To determine age-related changes, the initial horizontal vestibulo-ocular reflex (VOR) of 11 younger normal subjects (aged 20–32 years) was compared with that of 12 older subjects (aged 58–69 years) in response to random transients of whole-body acceleration of 1,000 and 2,800°/s² delivered around eccentric vertical axes ranging from 10 cm anterior to 20 cm posterior to the eyes. Eye and head positions were sampled at 1,200 Hz using magnetic search coils. Subjects fixed targets 500 cm or 15 cm distant immediately before the unpredictable onset of rotation in darkness. For all testing conditions, younger subjects exhibited compensatory VOR slow phases with early gain (eye velocity/head velocity, interval 35–45 ms from onset of rotation) of 0.90±0.02 (mean ± SEM) for the higher head acceleration, and 0.79±0.02 for the lower acceleration. Older subjects had significantly (P<0.0001) lower early gain of 0.77±0.04 for the higher head acceleration and 0.70±0.02 for the lower acceleration. Late gain (125–135 ms from onset of rotation) was similar for the higher and lower head accelerations in younger subjects. Older subjects had significantly lower late gain at the higher head acceleration, but gain similar to the younger subjects at the lower acceleration. All younger subjects maintained slow-phase VOR eye velocity to values ≥200°/s throughout the 250-ms rotation, but, after an average of 120 ms rotation (mean eccentricity 13°), 8 older subjects consistently had abrupt declines (ADs) in slow-phase VOR velocity to 0°/s or even the anticompensatory direction. These ADs were failures of the VOR slow phase rather than saccades and were more frequent with the near target at the higher acceleration. Slow-phase latencies were 14.4±0.4 ms and 16.8±0.4 ms for older subjects at the higher and lower accelerations, significantly longer than comparable latencies of 10.0±0.5 ms and 12.0±0.6 ms for younger subjects. Late VOR gain modulation with target distance was significantly attenuated in older subjects only for the higher head acceleration. Electronic Publication     

Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex

The nodulus and sublobule d of the uvula of rhesus and cynomolgus monkeys were electrically stimulated with short trains of pulses to study changes in horizontal slow-phase eye velocity. Nodulus and uvula stimulation produced a rapid decline in horizontal slow phase velocity, one aspect of the spatial reorientation of the axis of eye rotation that occurs when the head is tilted with regard to gravity during per- and post-rotatory nystagmus and optokinetic after-nystagmus (OKAN). Nodulus and uvula stimulation also reproduced the reduction of the horizontal time constant of post-rotatory nystagmus and OKAN that occurs during visual suppression. The brief electric stimuli (4–5 s) induced little slow-phase velocity and had no effect on the initial jump in eye velocity at the onset or the end of angular rotation. Effects of stimulation were unilateral, suggesting specificity of the output pathways. Activation of more caudal sites in the uvula produced nystagmus with a rapid rise in eye velocity, but the effects did not outlast the stimulus and did not affect VOR or OKAN time constants. Thus, stimulation of caudal parts of the uvula did not affect eye velocity produced by velocity storage. We postulate that the nodulus and sublobule d of the uvula control the time constant of the yaw axis (horizontal) component of slow-phase eye velocity produced by velocity storage.     

Dual-pathway model of the human vestibulo-ocular reflex

The purpose of the study was to investigate, evaluate and refine an existing dual-pathway VOR model by comparing the model responses with the responses of human subjects. Based on data of subjects' VOR responses, the physiological parameters and some gain constants in a dual-pathway model were adjusted to suit the human VOR data. As a result, the improved model can produce and exhibit the fundamental nystagmus patterns of human VOR responses to the head motions around a vertical axis for a wide range of frequencies and magnitudes. It was found that there is good agreement on quantitative analysis between the outcome of human VOR responses and the model output. Also, it was found that the quantitative analysis of slow-phase eye-movement data confirmed the previously published results.     

Canal-otolith interactions driving vertical and horizontal eye movements in the squirrel monkey

The vestibulo-ocular reflex (VOR) was studied in three squirrel monkeys subjected to rotations with the head either centered over, or displaced eccentrically from, the axis of rotation. This was done for several different head orientations relative to gravity in order to determine how canal-mediated angular (aVOR) and otolithmediated linear (lVOR) components of the VOR are combined to generate eye movement responses in three-dimensional space. The aVOR was stimulated in isolation by rotating the head about the axis of rotation in the upright (UP), right-side down (RD), or nose-up (NU) orientations. Horizontal and vertical aVOR responses were compensatory for head rotation over the frequency range 0.25–4.0 Hz, with mean gains near 0.9. The horizontal aVOR was relatively constant across the frequency range, while vertical aVOR gains increased with increasing stimulation frequency. In the NU orientation, compensatory torsional aVOR responses were of relatively low gain (0.54) compared with horizontal and vertical responses, and gains remained constant over the frequency range. When the head was displaced eccentrically, rotation provided the same angular stimuli but added linear stimulus components, due to the centripetal and tangential accelerations acting on the head. By manipulating the orientation of the head relative to gravity and relative to the axis of rotation, the lVOR response could be combined with, or isolated from, the aVOR response. Eccentric rotation in the UP and RD orientations generated aVOR and lVOR responses which acted in the same head plane. Horizontal aVOR-lVOR interactions were recorded when the head was in the UP orientation and facing toward (nose-in) or away from (nose-out) the rotation axis. Similarly, vertical responses were recorded with the head RD and in the nose-out or nose-in positions. For both horizontal and vertical responses, gains were dependent on both the frequency of stimulation and the directions and relative amplitudes of the angular and linear motion components. When subjects were positioned nose-out, the angular and linear stimuli produced synergistic interactions, with the lVOR driving the eyes in the same direction as the aVOR. Gains increased with increasing frequency, consistent with an addition of broad-band aVOR and high-pass lVOR components. When subjects were nose-in, angular and linear stimuli generated eye movements in opposing directions, and gains declined with increasing frequency, consistent with a subtraction of the lVOR from the aVOR. This response pattern was identical for horizontal and vertical eye movements. aVOR and lVOR interactions were also assessed when the two components acted in orthogonal response planes. By rotating the monkeys into the NU orientation, the aVOR acted primarily in the roll plane, generating torsional ocular responses, while the translational (lVOR) component generated horizontal or vertical ocular responses, depending on whether the head was oriented such that linear accelerations acted along the interaural or dorsoventral axes, respectively. Horizontal and vertical lVOR responses were negligible at 0.25 Hz and increased dramatically with increasing frequency. Comparison of the combined responses (UP and RD orientations) with the isolated aVOR (head-centered) and lVOR (NU orientation) responses, indicates that these VOR components sum in a linear fashion during complex head motion.