Visually-induced adaptive plasticity in the human vestibulo-ocular reflex

Summary The vestibulo-ocular reflex (VOR) is under adaptive control which corrects VOR performance when visual-vestibular mismatch arises during head movements. However, the dynamic characteristics of VOR adaptive plasticity remain controversial. In this study, eye movements (coil technique) were recorded from normal human subjects during sinusoidal rotations in darkness before and after 8 h. of adaptation to 2X binocular lenses. The VOR was studied at 7 frequencies between 0.025 and 4.0 Hz at 50°/s peak head velocity (less for 2.5–4 Hz). For 0.025 and 0.25 Hz, the VOR was tested at 4 peak head velocities between 50 and 300° /s. Before 2X lens adaptation, VOR gain was around 0.9 at 2.5–4.0 Hz and dropped gradually with decreasing frequency to under 0.6 at 0.025 Hz. Phase showed a small lead at the highest frequencies which declined to 0° as frequency decreased to 0.5–0.25 Hz, but then rose to 14° by 0.025 Hz. VOR gain was independent of head velocity in the range 50–300°/s at both 0.025 and 0.25 Hz. However, Phase lead rose with increasing head velocity, more so at 0.025 than at 0.25 Hz. After 2X lens adaptation, gain rose across the frequency bandwidth. However, the proportional gain enhancement was frequency dependent; it was greatest at 0.025 Hz (44%), and declined with increasing frequency to reach a minimum at 4 Hz (19%). Phase lead increased after 2X lens adaptation at lower frequencies, but decreased at higher frequencies. New velocity-dependent gain nonlinearities also developed which were not present prior to adaptation; gain declined as peak head velocity increased from 50 to 300°/s at both 0.025 (23% drop) and 0.25 Hz (15% drop). This may suggest an amplitude-dependent limitation in VOR adaptive plasticity. Results indicate both frequency and amplitude dependent nonlinearities in human VOR response dynamics before and after adaptive gain recalibration.     

The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey

The aim of this study was to determine if the angular vestibulo-ocular reflex (VOR) in response to pitch, roll, left anterior–right posterior (LARP), and right anterior–left posterior (RALP) head rotations exhibited the same linear and nonlinear characteristics as those found in the horizontal VOR. Three-dimensional eye movements were recorded with the scleral search coil technique. The VOR in response to rotations in five planes (horizontal, vertical, torsional, LARP, and RALP) was studied in three squirrel monkeys. The latency of the VOR evoked by steps of acceleration in darkness (3,000°/s² reaching a velocity of 150°/s) was 5.8±1.7 ms and was the same in response to head rotations in all five planes of rotation. The gain of the reflex during the acceleration was 36.7±15.4% greater than that measured at the plateau of head velocity. Polynomial fits to the trajectory of the response show that eye velocity is proportional to the cube of head velocity in all five planes of rotation. For sinusoidal rotations of 0.5–15 Hz with a peak velocity of 20°/s, the VOR gain did not change with frequency (0.74±0.06, 0.74±0.07, 0.37±0.05, 0.69±0.06, and 0.64±0.06, for yaw, pitch, roll, LARP, and RALP respectively). The VOR gain increased with head velocity for sinusoidal rotations at frequencies 4 Hz. For rotational frequencies 4 Hz, we show that the vertical, torsional, LARP, and RALP VORs have the same linear and nonlinear characteristics as the horizontal VOR. In addition, we show that the gain, phase and axis of eye rotation during LARP and RALP head rotations can be predicted once the pitch and roll responses are characterized.This work was supported by NIH grant R01 DC02390     

Compensation of the human vertical vestibulo-ocular reflex following occlusion of one vertical semicircular canal is incomplete

The vestibulo-ocular reflex (VOR) was studied in nine human subjects 2–15 months after permanent surgical occlusion of one posterior semicircular canal. The stimuli used were rapid, passive, unpredictable, low-amplitude (10–20°), high-acceleration (3000–4000°/s²) head rotations in pitch and yaw planes. The responses measured were vertical and horizontal eye rotations, and the results were compared with those from 19 normal subjects. After unilateral occlusion of the posterior semi-circular canal, the gain of the head-up pitch vertical VOR — the vertical VOR generated by excitation from only one and disfacilitation from two vertical semicircular canals — was reduced to 0.61±0.06 (normal 0.92±0.06) at a head velocity of 200°/s. In contrast the gain of the head-down pitch vertical VOR — the VOR still generated by excitation from two, but disfacilitation from only one vertical semicircular canal — was within normal limits: 0.86±0.11 (normal 0.96±0.04). The gain of the horizontal VOR in response to yaw head rotations — ipsilesion 0.81±0.06 (normal 0.88±0.05) and contralesion 0.80±0.11 (normal 0.92±0.11) — was within normal limits in both directions (group means ± two-tailed 95% confidence intervals given in each case). These results show that occlusion of just one vertical semicircular canal produces a permanent deficit of about 30% in the vertical VOR gain in response to rapid pitch head rotations in the excitatory direction of the occluded canal. This observation indicates that, in response to a stimulus in the higher dynamic range, compensation of the human VOR for the loss of excitatory input from even one vertical semicircular canal is incomplete.     

Combined influence of vergence and eye position on three-dimensional vestibulo-ocular reflex in the monkey

This study examined two kinematical features of the rotational vestibulo-ocular reflex (VOR) of the monkey in near vision. First, is there an effect of eye position on the axes of eye rotation during yaw, pitch and roll head rotations when the eyes are converged to fixate near targets? Second, do the three-dimensional positions of the left and right eye during yaw and roll head rotations obey the binocular extension of Listing's law (L2), showing eye position planes that rotate temporally by a quarter as far as the angle of horizontal vergence? Animals fixated near visual targets requiring 17 or 8.5 degrees vergence and placed at straight ahead, 20 degrees up, down, left, or right during yaw, pitch, and roll head rotations at 1 Hz. The 17 degrees vergence experiments were performed both with and without a structured visual background, the 8.5 degrees vergence experiments with a visual background only. A 40 degrees horizontal change in eye position never influenced the axis of eye rotation produced by the VOR during pitch head rotation. Eye position did not affect the VOR eye rotation axes, which stayed aligned with the yaw and roll head rotation axes, when torsional gain was high. If torsional gain was low, eccentric eye positions produced yaw and roll VOR eye rotation axes that tilted somewhat in the directions predicted by Listing's law, i.e., with or opposite to gaze during yaw or roll. These findings were seen in both visual conditions and in both vergence experiments. During yaw and roll head rotations with a 40 degrees vertical change in gaze, torsional eye position followed on average the prediction of L2: the left eye showed counterclockwise (ex-) torsion in down gaze and clockwise (in-) torsion in up gaze and vice versa for the right eye. In other words, the left and right eye's position plane rotated temporally by about a quarter of the horizontal vergence angle. Our results indicate that torsional gain is the central mechanism by which the brain adjusts the retinal image stabilizing function of the VOR both in far and near vision and the three dimensional eye positions during yaw and roll head rotations in near vision follow on average the predictions of L2, a kinematic pattern that is maintained by the saccadic/quick phase system.     

Senescence of human visual-vestibular interactions: smooth pursuit,optokinetic, and vestibular control of eye movements with aging

Natural aging entails progressive deterioration in a variety of biological systems. This study focuses on visual and vestibular influences on human eye movements as a function of aging. Eye movements were recorded (search-coil technique) during visual, vestibular, and combined stimuli in subjects across a broad range of ages (18–89 years). Two types of visual following were assessed: smooth pursuit (SP) of a small discrete target, and optokinetic (OKR) following of a large-field striped image. The vestibulo-ocular reflex (VOR) was studied during head rotation in darkness. Visualvestibular interactions were recorded during rotation in two ways: when the optokinetic scene was earth-fixed, resulting in visual enhancement of the VOR (VVOR), and when the visual image was head-fixed, allowing visual suppression of the VOR (VSVOR). Stimuli consisted of horizontal sinusoidal oscillations over the frequency range 0.025–4 Hz. Trials were analyzed to yield response gain (peak horizontal eye/stimulus velocities) and phase (asynchrony, in degrees, between eye and stimulus velocity signals). VOR gain in young subjects was greatest (near 0.9) at 2.5–4 Hz but declined steadily with decreasing frequency, while phase hovered near zero until 0.1 Hz and then developed a progressively increasing lead. Effects of advancing age were small, given the modest head velocities presented, and were most noticeable as an increase in phase lead and decline in gain at the lowest frequencies (0.1 Hz). The two forms of visual following and all conditions of visual-vestibular interactions displayed more prominent age-dependent changes. OKR and SP response characteristics (0.25–4 Hz) closely resembled each other. Gain was greatest at 0.25 Hz, while phase was near 0°. As frequency increased, gain declined while phase lag rose. However, both gain and phase lag tended to be slightly greater for OKR than for SP responses. Both SP and OKR response properties deteriorated progressively with increasing age, as witnessed by a progressive decline in gain and increase in phase lag, even at modest frequencies (e.g., 0.25–1.0 Hz). VVOR responses were generally closer to the ideal of 1.0 in gain and 0° in phase than either the VOR or visual following alone. A subtle but significant age-dependent decline in VVOR performance occurred at the lowest frequencies. VSVOR response characteristics were close to those of the VOR and VVOR at 4 Hz, where visual influences on eye movements are generally inconsequential. As frequency declined, visual suppression became more robust and gain dropped. The SP stimulus seemed surprisingly more effective than the OK scene in suppressing the VOR, but this effect is predicted by a linear model of visual-vestibular interactions. As age increased, visual influences on the VOR became progressively weaker, in concert with deterioration of visual following. The subjective sensation of circular vection (CV), a psychophysical measure of VVI, was assessed during optokinetic stimulation at 0.025 Hz. Interestingly, the likelihood and intensity of CV increased with aging, suggesting that visual inputs to the perception of self-motion are enhanced in the elderly. This may represent a form of visual compensation for age-dependent loss of vestibular self-rotation cues. In brief, the VOR, visual following, and their interactions display specific changes in response properties as a function of natural aging. The modifications may be interpreted as age-dependent deteriorations in the performance of systems underlying the control of human eye movements.     

Response of the human vestibulo-ocular reflex following long-term 2x magnified visual input

Summary This study examines the contribution of predictive motor programming to the adjustment of vestibulo-ocular reflex (VOR) gains after exposure to spectacles with a 2x magnification. When fully adapted, subjects exhibited two-fold gain increases with a 3 Hz sinewave stimulus with both an imaginary earth-fixed and imaginary moving target. Before complete adaptation was achieved, quick phases embedded in the slow component were observed intermittently which compensated for insufficient VOR gain. At 0.5 Hz in the same state of full adaptation during fixation of an imaginary earth-fixed target subjects exhibited a gain increase of only approximately 75% indicating that the contribution of VOR adjustment is not sufficient for perfect visual stabilization at lower frequencies. Over the range of random stimulation (0.5–5 Hz), the VOR failed to exhibit complete adaptation. The degree of adaptation derived with a VOR-cancellation task was less overall than that with a task requiring perfect compensatory eye movements. These findings indicate that central motor programmes are required in the adaptive process to achieve visual stability.Supported by the Medical Research Council of Canada and the Ontario Ministry of Health     

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.     

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.     

Human vestibulo-ocular responses to rapid,helmet-driven head movements

High-frequency head rotations in the 2–20 Hz range and passive, unpredictable head acceleration impulses were produced by a new technique, utilizing a helmet with a torque motor oscillating a mass. Unrestrained head and eye movements were recorded using magnetic sensor coils in a homogeneous magnetic field. In order to analyze the influence of the visual system on the vestibulo-ocular reflex (VOR), we took measurements under three experimental conditions: (1) with a stationary visual target; (2) in total darkness with the subject imagining the stationary target; and (3) with a head-fixed target. The results in 15 healthy subjects were highly consistent. At 2 Hz, VOR gain was near unity; above 2 Hz, VOR gain started to decrease, but this trend reversed beyond 8 Hz, where the gain increased continuously up to 1.1–1.3 at 20 Hz. Phase lag increased with frequency, from a few deg at 2 Hz to about 45 degrees at 20 Hz. Above 2 Hz, VOR gain was not significantly different for the three experimental conditions. Head acceleration impulses produced a VOR with near-unity gain in both directions. We also tested three subjects with clinically total bilateral loss of labyrinthine functions. These labyrinthine-defective subjects showed, in comparison to the normal subjects, strikingly lower gains and much longer delays in the VOR during sinu-soidal and step-like head movements. These results suggest that our new torque-driven helmet technique is effective, safe and convenient, enabling the assessment of the VOR at relatively high frequencies where both visual and mental influences are minimized.     

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.     

Deficits of gaze stability in multiple axes following unilateral vestibular lesions

 Abnormalities in the vestibulo-ocular reflex (VOR) after unilateral vestibular injury may cause symptomatic gaze instability. We compared five subjects who had unilateral vestibular lesions with normal control subjects. Gaze stability and VOR gain were measured in three axes using scleral magnetic search coils, in light and darkness, testing different planes of rotation (yaw and pitch), types of stimulus (sinusoids from 0.8 to 2.4 Hz, and transient accelerations) and methods of rotation (active and passive). Eye velocity during horizontal tests reached saturation during high-velocity/acceleration ipsilesional rotation. Rapid vertical head movements triggered anomalous torsional rotation of the eyes. Gaze instability was present even during active rotation in the light, resulting in oscillopsia. These abnormal VOR responses are a consequence of saturating nonlinearities, which limit the usefulness of frequency-domain analysis of rotational test data in describing these lesions. Received: 22 April 1996 / Accepted: 18 February 1997     

Normal performance and expression of learning in the vestibulo-ocular reflex (VOR) at high frequencies

The rotatory vestibulo-ocular reflex (VOR) keeps the visual world stable during head movements by causing eye velocity that is equal in amplitude and opposite in direction to angular head velocity. We have studied the performance of the VOR in darkness for sinusoidal angular head oscillation at frequencies ranging from 0.5 to 50 Hz. At frequencies of > or = 25 Hz, the harmonic distortion of the stimulus and response were estimated to be <14 and 22%, respectively. We measured the gain of the VOR (eye velocity divided by head velocity) and the phase shift between eye and head velocity before and after adaptation with altered vision. Before adaptation, VOR gains were close to unity for frequencies < or = 20 Hz and increased as a function of frequency reaching values of 3 or 4 at 50 Hz. Eye velocity was almost perfectly out of phase with head velocity for frequencies < or = 12.5 Hz, and lagged perfect compensation increasingly as a function of frequency. After adaptive modification of the VOR with magnifying or miniaturizing optics, gain showed maximal changes at frequencies <12.5 Hz, smaller changes at higher frequencies, and no change at frequencies larger than 25 Hz. Between 15 and 25 Hz, the phase of eye velocity led the unmodified VOR by as much as 50 degrees when the gain of the VOR had been decreased, and lagged when the gain of the VOR had been increased. We were able to reproduce the main features of our data with a two-pathway model of the VOR, where the two pathways had different relationships between phase shift and frequency.     

Torsional and horizontal vestibular ocular reflex adaptation: three-dimensional eye movement analysis

This study used visual-vestibular conflict to effect short-term torsional and horizontal adaptation of the vestibulo-ocular reflex (VOR). Seven normal subjects underwent sinusoidal whole-body rotation about the earth-vertical axis for 40 min (±37°/s, 0.3 Hz) while viewing a stationary radial pattern fixed to the chair (×0 viewing). During adaptation and testing in darkness, the head was pitched either up or down 35° to excite both the horizontal and torsional VOR. The eyes were kept close to zero orbital elevation. Eye movements were recorded with a dual search coil in a three-field magnetic system. VOR gain was determined by averaging peak eye velocity from ten cycles of chair oscillation in complete darkness. The gain of the angular horizontal VOR (response to rotation about the head rostral-caudal axis) was significantly reduced after training in both head orientations. Angular torsional VOR gain (head rotation about the naso-occipital axis) was reduced in both head orientations, but this reached statistical significance only in the head down position. These results suggest that torsional and horizontal VOR gain adaptation, even when elicited together, may be subject to different influences depending upon head orientation. Differences between head up and down could be due to the relatively greater contribution of the horizontal semicircular canals with nose-down pitch. Alternatively, different VOR-adaptation processes could depend on the usual association of the head down posture to near viewing, in which case the torsional VOR is relatively suppressed.     

Voluntary modulation of the vestibuloocular reflex in humans and its relation to smooth pursuit

Summary Human subjects attempted to modify their vestibuloocular reflex (VOR) in the dark by fixating imagined targets while experiencing predictable (SIN) sinusoidal (0.01–2.5 Hz) and unpredictable (SSN) sum of sines rotational stimuli (0.02–1.9 Hz). Modification was attempted under 2 instructional sets: VOR enhancement, ie tracking an imaginary earth-fixed target; VOR suppression, ie fixation of a chair fixed target. When compared to gain characteristics exhibited during the relax state with the same stimuli, subjects were able to alter VOR gain under both experimental conditions, raising it during the enhance paradigm and lowering it during the suppress paradigm. While ability to suppress the VOR was dependent on stimulus frequency, decreasing as frequency of rotation increased, subjects were equally able to modify their responses to the unpredictable and the predictable stimuli. Response phase did not change and was maintained close to 180 deg, regardless of instructional set, predictability, or frequency of stimulation for frequencies greater than 0.1 Hz. At frequencies below 0.1 Hz, a phase lead developed that was similar for all paradigms and rotational stimuli. In contrast, when subjects attempted to pursue visual targets that matched closely the velocities and frequencies of the chair rotation during predictable (SIN) and unpredictable stimulation (SSN), success was dependent on predictability of the stimulus. SSN target motion caused a significant decrease in pursuit velocity as compared to results using SIN target motion. Phase characteristics for both types of stimuli were similar, demonstrating a slight lead at lower frequencies and lagging as frequency of target oscillation increased. The results suggest that voluntary modulation of the VOR is not mediated by a neural control mechanism that is based on prediction. In addition, pursuit does not appear to contribute significantly to ability to cancel VOR. Instead, VOR modulation may be a cognitive event that involves use of a mechanism that produces simple parametric gain changes.Supported by Coleman, Hearst and Regenstein Foundation grants and National Institute of Handicapped Research grant no. G008300079     

Adaptation of the angular vestibulo-ocular reflex to head movements in rotating frames of reference

Head movements in a rotating frame of reference are commonly encountered, but their long term effects on the angular vestibulo-ocular reflex (aVOR) are not well understood. To study this, monkeys were oscillated about a naso-occipital (roll) axis for several hours while rotating about a spatial vertical axis (roll-while-rotating, RWR). This induced oscillations in roll and pitch eye velocity and continuous horizontal (yaw) nystagmus. For several hours thereafter, simple roll in darkness induced horizontal nystagmus and pitch and roll oscillations. The rising and falling time constants of the horizontal velocity indicated that the nystagmus arose in velocity storage. The continuous nystagmus was correlated with a phase shift of vertical eye velocity from 90° to 0° re head position. As the phases reverted toward pre-adaptive values, the horizontal velocity declined. Similar yaw nystagmus and pitch and roll velocities were produced by oscillation in roll after adaptation with roll and horizontal optokinetic nystagmus (OKN), but not after adaptation with pitch-while-rotating (PWR). Findings were explained by a model that shifted the roll orientation vector of velocity storage toward the pitch axis during adaptation with RWR and Roll & OKN. This shift produced modulation in vertical eye velocity in the post adaptive state, which was approximately in phase with roll head position, generating horizontal nystagmus. Similar orientation changes to prolonged exposure to complex motion environments may be responsible for producing post-stimulus motion sickness and/or mal de debarquement. Supported by DC007847, EY04148, DC05204, EY01867, DC05222.     

Vestibulo-oculomotor testing during the course of a spaceflight mission

Summary The experimental concept and findings from a recent manned orbital spaceflight are presented. In a single-case, longitudinal study, vestibulo-oculomotor function was examined by caloric testing and active head oscillations. The results from preflight, inflight, and postflight measurements of the human vestibulo-ocular reflex, together with those of ongoing terrestrial studies, should enable separation of the canalicular and otolithic contributions to ocular torsion. This analysis enables an accurate evaluation of the adaptation of the otolithic system to the inflight microgravity and, after landing, to the 1- force environment. Video-oculography was employed throughout for the comprehensive measurement of eye and head movements. Caloric testing involved air insufflation at 15° C over 90 s, followed by an observation interval of 2 min. During inflight testing this was continued with a 30-s free-floating interval. Active head oscillations were performed at four discrete frequencies (0.12, 0.32, 0.80, 2.0 Hz) and over a frequency sweep between 0.1 and 2.0 Hz. These head oscillations were performed in yaw, pitch, and roll and for three visual conditions (head-fixed target, space-fixed target, no target). The concomitant stimulation of the semicircular canals and otolithic receptors during these oscillations should yield different oculomotor responses under 1-g and 0-g adaptations. Both the short-form caloric test and the active head movement test were performed on 4 of the 5 available mission days. The results of the caloric tests yield a caloric nystagmus intensity (slow-phase velocity) of approximately 60% of that measured before flight and indicate an adaptation in response over the 10-day period after landing. The preliminary results from the head movement tests about the roll axis indicate an adaptive response in this aspect of the vestibulo-ocular reflex during prolonged microgravity. Some changes in sensomotoric control were also apparent during the inflight and postflight phases.Abbreviations SPV slow phase velocity (%s) - VOR vestibulo-ocular reflex     

Inluence of eye motion on adaptive modifications of the vestibulo-ocular reflex in the rat

While sustained retinal slip is assumed to be the basic conditioning stimulus in adaptive modifications of the vestibulo-ocular reflex (VOR) gain, several observations suggest that eye motion-related signals might also be involved. We oscillated pigmented rats over periods of 20 min around the vertical axis, at 0.3 Hz and 20°/s peak velocity, in different retinal slip and/or eye motion conditions in order to modify their VOR gain. The positions of both eyes were recorded by means of a phase-detection coil system with the head restrained. The main findings came from the comparison of two basic conditions — including their respective controls — in which one or both eyes were reversibly immobilised by threads sutured to the eyes. In the first condition the animals were rotated in the light with one eye immobilised and the other eye free to move but covered. Rotation in the light in this open-loop condition immediately elicited high-gain compensatory eye movements of the non-impeded, covered eye. At the end of this training procedure, the VOR gain increased by 42.3%. In the second condition, both eyes were immobilised and one eye was covered. The result was an increase in the VOR gain of 26.3%. These two conditions were similar as to the visuo-vestibular drive during the exposure, but different as to the resulting — and allowed — eye motion, showing that the condition where the larger eye movements occurred yielded the larger VOR gain change. Our data support the idea proposed by Collewijn and Grootendorst (1979, p. 779) and Collewijn (1981, p. 146) that [retinal] slip and eye movements seem to be relevant signals for the adaptation of the rabbit's visuo-vestibular oculomotor reflexes. Our data also suggest that sensory information related to eye movements, more likely than efference copy, is the coding signal for eye movement which combines with the retinal slip signal to generate adaptive changes of the VOR.     

The three-dimensional vestibulo-ocular reflex during prolonged microgravity

Single-case, longitudinal studies of the three-dimensional vestibulo-ocular response (VOR) were conducted with two spaceflight subjects over a 180-day mission. For reference, a control study was performed in the laboratory with 13 healthy volunteers. Horizontal, vertical and torsional VOR was measured during active yaw, pitch and roll oscillations of the head, performed during visual fixation of real and imaginary targets. The control group was tested in the head-upright position, and in the gravity-neutral, onside and supine positions. Binocular eye movements were recorded throughout using videooculography, yielding eye position in Fick co-ordinates. Eye velocity was calculated using quaternion algebra. Head angular velocities were measured by a head-mounted rate sensor. Eye/head velocity gain and phase were evaluated for the horizontal, vertical and torsional VOR. The inclination of Listing's plane was also calculated for each test session. Control group gain for horizontal and vertical VOR was distributed closely around unity during real-target fixation, and reduced by 30-50% during imaginary-target trials. Phase was near zero throughout. During head pitch in the onside position, vertical VOR gain did not change significantly. Analysis of up/down asymmetry indicated that vertical VOR gain for downward head movement was significantly higher than for upward head movement. Average torsional VOR gain with real-target fixation was significantly higher than with imaginary-target fixation. No difference in phase was found. In contrast to vertical VOR gain, torsional VOR gain was significantly lower in the gravity-neutral supine position. Spaceflight subjects showed no notable modification of horizontal or vertical VOR gain or phase during real-target fixation over the course of the mission. However, the up/down asymmetry of vertical VOR gain was inverted in microgravity. Torsional VOR gain was clearly reduced in microgravity, with some recovery in the later phase. After landing, there was a dip in gain during the first 24 h, with subsequent recovery to near baseline over the 13-day period tested. Listing's plane appeared to remain stable throughout the mission. The findings reflect various functions of the otolith responses. The reduced torsional VOR gain in microgravity is attributed to the absence of the gravity-dependent, dynamic stimulation to the otoliths (primarily utricles). On the other hand, the reversal of vertical VOR up/down gain asymmetry in microgravity is attributed to the off-loading of the constant 1-g bias (primarily to the saccules) on Earth. The observed increase in torsional VOR gain from the 1st to the 6th month in microgravity demonstrates the existence of longer-term adaptive processes than have previously been considered. Likely factors are the adaptive reweighting of neck-proprioceptive afferents and/or enhancement of efference copy.     

Static roll and the vestibulo-ocular reflex (VOR)

Summary We measured the effect of static lateral tilt (roll) on the gain and time constant of the vestibulo-ocular reflex (VOR) in five normal subjects by recording both the horizontal and vertical components of eye velocity in space for rotation about an earth vertical axis with the head either upright or rolled to either side. The time constant of the VOR in the upright position was 19.6 ±3.2s (mean ± standard deviation). The time constant of the horizontal component with respect to the head decreased to 15.7±4.0s for 30° roll and to 12.7±2.7s for 60° roll. The time constant of the vertical component with respect to the head was 11.0±1.4 s for 30° roll and 7.5±1.6 s for 60° roll. The gain of the horizontal VOR with respect to space did not vary significantly with roll angle but a small space-vertical component to the VOR appeared during all rotations when the head was rolled away from upright. This non-compensatory nystagmus built up to a maximum of 2–3°/s at 17.0±4.7s after the onset of rotation and then decayed. These data suggest that static otolith input modulates the central storage of semicircular canal signals, and that head-horizontal and head-vertical components of the VOR can decay at different rates.     

Gravity and the vertical vestibulo-ocular reflex

Summary We studied the vertical vestibulo-ocular reflex (VOR) and vertical visual-vestibular interaction induced by voluntary pitch in the upright and onside positions in eight normal human subjects. Subjects were trained to produce sinusoidal (0.4 to 1.6 Hz) pitch head movements guided by a frequency modulated sound signal. Eye and head movements were recorded with a magnetic search coil. There was no significant difference between the pooled average gain (eye velocity/head velocity) of the vertical VOR in the upright and onside positions. Vertical VOR gain in any position could be more or less than 1.0 for individual subjects. By contrast, gain with an earth-fixed visual target was always near 1.0. Asymmetries in the gain of upward and downward VOR, pursuit and fixation suppression of the VOR were found in individual subjects, but in the group of normal subjects there was no significant difference between gain of up and down eye movements induced by vestibular, visual or visual-vestibular stimulation in any position. We conclude that during voluntary pitch otolith signals are not critical for normal functioning of the vertical VOR.