Linear Vestibulo-ocular Reflex Research Articles

Effect of aging on the human initial interaural linear vestibulo-ocular reflex

To determine age-related changes, the initial linear vestibulo-ocular reflex (LVOR) of eight older subjects of mean age 65+/-7 years (mean +/- SD, range 56-75 years) was compared with that of nine younger subjects of mean age 24+/-5 years (range 18-31 years) in response to random transients of whole-body heave (interaural) translation at peak acceleration of 0.5 g delivered by a pneumatic actuator. Binocular eye rotations were measured with magnetic search coils, while linear head position and acceleration were measured with a potentiometer and piezoelectric accelerometer. Subjects viewed targets 200 cm, 50 cm, or 15 cm distant immediately before the unpredictable onset of randomly directed translation in darkness (LVOR) and in light (LVVOR). All subjects maintained ideal vergence of 1.5-2 degrees for the 200-cm target, 6-8 degrees for the 50-cm target, and 21-26 degrees for the 15-cm target, with actual vergences depending on individual interpupillary distances. Search coil recording of angular position of the upper teeth showed head rotation to be negligible (less than 0.5 degrees ) for the first 250 ms after onset of head translation, excluding a role for the angular VOR in the responses studied. The LVOR response to heave translation was an oppositely directed eye rotation occurring after a mean latency of 62+/-3 ms for older and 42+/-3 ms (mean +/- SD) for younger subjects ( P<0.0001). The peak of the latency distribution was 60-100 ms for older and 20-60 ms for younger subjects. During the early interval, 70-80 ms from head motion onset prior to a pursuit contribution or saccades, all subjects had significantly enhanced LVOR with decreasing target distance. In this interval, the LVOR position amplitude of younger subjects was 0.17+/-0.01 degrees, 0.40+/-0.01 degrees, 0.57+/-0.01 degrees (mean +/- SE), respectively, in descending order of target distance. Early sensitivities were significantly reduced for older subjects to 0.07+/-0.01 degrees, 0.23+/-0.01 degrees, 0.40+/-0.01 degrees ( P<0.0001). There was no significant effect of target visibility in either group during the first 110 ms ( P>0.05). Visual-otolith interaction was mainly reflected not by the vestibular slow phase, but by vestibular catch-up saccades (VCUS) in the compensatory direction. The effect of aging on the initial human LVOR is thus to: prolong latency, reduce early sensitivity, and reduce occurrence of vestibular catch-up saccades.

Otolith function: basis for modern testing.

The major challenge in developing a robust test of otolith function, particularly with regard to linear vestibulo-ocular reflex (LVOR) and perceptual measures, is to find a way in which graded lesions are reflected in graded response properties and abnormalities. The ability of the vestibulo-ocular reflex (VOR) to compensate and adapt to dysfunction and pathology presents formidable challenges for registering localizing clinical findings, whether in the angular vestibulo-ocular reflex (AVOR), the LVOR, or both. Based on a variety of considerations, various forms of eccentric rotation seem to provide the most convenient, and potentially the most useful, means to generate motion profiles from which otolith function can be directly assessed. Both translational and tilt responses can be recorded depending on the stimulus profile. The near-centric version is particularly enticing because of the ability to study one labyrinth at a time, much like calorics. In that case and in others in which the tilt-LVOR is prominent, measures of the perceived visual vertical are useful and by all accounts similar to ocular torsion. The latter does hold the important advantage of being an objective measure, requiring no intervention on the part of the patient. The translational-LVOR can be derived from eccentric rotation responses with the head displaced forward as well as backward, while viewing near targets in hopes of generating a large addition or subtraction (even inversion) of an otherwise AVOR-driven reflex. These considerations provide an impetus to pursue improved methods of quantifying otolith function in a clinical population. The sobering caveat is that the diagnosis of total unilateral vestibular loss presents little challenge either clinically or by classic testing (e.g., calorics), and yet most of our efforts in developing quantifiable measures of dysfunction over the years have yielded results that are modest and hardly compelling.

Principles of linear and angular vestibuloocular reflex organization in the frog.

We compared the spatial organization patterns of linear and angular vestibuloocular reflexes in frogs by recording the multiunit spike activity from cranial nerve branches innervating the lateral rectus, the inferior rectus, or the inferior obliquus eye muscles. Responses were evoked by linear horizontal and/or vertical accelerations on a sled or by angular accelerations about an earth-vertical axis on a turntable. Before each sinusoidal oscillation test in darkness, the static head position was systematically altered to determine those directions of horizontal linear acceleration and those planes of angular head oscillation that were associated with minimal response amplitudes. Inhibitory response components during angular accelerations were clearly present, whereas inhibitory response components during linear accelerations were absent. Likewise was no contribution from the vertical otolith organs (i.e., lagena and saccule) observed during vertical linear acceleration. Horizontal linear acceleration evoked responses that originated from eye muscle-specific sectors on the contralateral utricular macula. The sectors of the inferior obliquus and lateral rectus muscles on the utricle had an opening angle of 45 and 60 degrees, respectively and overlapped to a large extent in the laterorostral part of the utricle. Both sectors were coplanar with the horizontal semicircular canals. The sector of the inferior rectus muscle was narrow (opening 5 degrees), laterocaudally oriented, and slightly pitched up by 6 degrees. Angular acceleration evoked maximal responses in the inferior obliquus muscle nerve that originated from the ipsilateral horizontal and the contralateral anterior vertical canals in a ratio of 50:50. Lateral rectus excitation originated from the contralateral horizontal and anterior vertical semicircular canals in a ratio of 80:20. The excitatory responses of the inferior rectus muscle nerve originated exclusively from the contralateral posterior vertical canal. Measured data and known semicircular canal plane vectors were used to calculate the spatial orientation of maximum sensitivity vectors for the investigated eye muscle nerves in semicircular canal coordinates. Comparison of the directions of maximal sensitivity vectors of responses evoked by linear or angular accelerations in a given eye muscle nerve showed that the two vector directions were oriented about orthogonally with respect to each other. With this arrangement the linear and the angular vestibuloocular reflex can support each other dynamically whenever they are co-activated without a change in the spatial response characteristics. The mutual adaptation of angular and linear vestibuloocular reflexes as well as the differences in their organization described here for frogs may represent a basic feature common for vertebrates in general.

Otolith function in cerebellar ataxia due to mutations in the calcium channel gene CACNA1A.

The vestibulo-ocular reflexes stabilize retinal images during head movements. While there is a wealth of information about the interaction between the cerebellum and vestibulo-ocular reflexes mediated by the semicircular canals, little is known about the role of the cerebellum in the generation of the otolith-mediated linear vestibulo-ocular reflex (LVOR). By means of transient linear acceleration of the whole body along the interaural axis, we examined the LVOR in six patients with hereditary cerebellar ataxia due to mutations of the calcium channel gene CACNA1A, five with spinocerebellar ataxia type 6 (SCA6) and one with episodic ataxia type 2 (EA-2). Six age-matched normal subjects served as controls. Using a peak acceleration of 0.5 g in combination with recording by the binocular scleral magnetic search coil method, it was possible to study the latency and sensitivity of the LVOR in the first 150 ms after motion onset. The normal LVOR showed a significant dependence on viewing distance and covaried with vergence angle, and could be enhanced by the presence of a visible target. In contrast, the LVOR of ataxic patients had normal latency but significantly decreased sensitivity that was not enhanced with visible or nearer targets despite normal vergence. Substituting for the normal smooth LVOR slow phase, ataxic patients employed catch-up saccades 150-250 ms after motion onset. These findings suggest a critical role of the cerebellum in the modulation of otolith-ocular signals that is independent of motor vergence.

Orientation of the eyes to gravitoinertial acceleration.

Orientation of the eyes to gravitoinertial acceleration, i.e., to the sum of gravity and the linear accelerations acting on the head and body, is a basic property of the linear vestibulo-ocular reflex to support vision. Present in a wide range of species from the lateral-eyed rabbit to frontal-eyed monkeys and humans, the eyes deviate in pitch, roll and yaw in response to pitch, roll and yaw head movements. The eyes also converge in response to naso-occipital linear acceleration. This paper provides examples of ocular orientation generated by static tilt and off-vertical axis rotation in three dimensions and demonstrates specifically how vergence would support vision in the rabbit.

Initiation of the linear vestibulo-ocular reflex in cerebellar dysfunction.

Initiation of the linear vestibulo-ocular reflex in cerebellar dysfunction.

New tests of vestibular function.

The vestibulo-ocular reflex (VOR) is the only drive for short-latency eye movements stabilizing the retina during externally imposed, sudden, high-head accelerations. New strategies can exploit this unique VOR feature to study it under conditions relevant to the daily lives of patients, and to exclude the contributions from confounding nonvestibular mechanisms. Testing of the yaw vestibulo-ocular reflex (VOR) during random, whole-body rotational transients at < or = 2800 degrees/s2 delivered about centered and eccentric axes enables measurement of gains and millisecond latencies of the canal and otolith VORs in humans. Repeated measurements in acute unilateral deafferentation show sequential recovery of canal and otolith VORs to contralesional rotation, but severe and permanent deficits to ipsilesional rotation. Patients with bilateral loss of caloric responses show severe bilateral loss of VORs to transient rotation, suggesting that the apparent preservation of their VORs during sinusoidal rotations at moderate frequencies may be due instead to somatosensory inputs. Since visual acuity is degraded by retinal image motion, dynamic visual acuity (DVA) measured during imposed head-on-body or whole-body transient motion can correlate closely with VOR performance only if optotypes are presented during directionally and temporally unpredictable, high-acceleration head motion. Prediction and efference copy are relentlessly employed by vestibulopathic patients to enable good DVA during predictable or low-acceleration head motion. The linear VOR to transient lateral acceleration is strongly dependent upon viewing distance. The latency of this otolith VOR is slightly longer and more variable than the canal VOR. Unlike the canal VOR, the otolith VOR does not develop a strong directional asymmetry in unilateral deafferentation. The otolith VOR is bilaterally attenuated in bilateral vestibulopathy, and loses target distance dependence in cerebellar degeneration.

Use of a genetic algorithm for the analysis of eye movements from the linear vestibulo-ocular reflex.

It is common in vestibular and oculomotor testing to use a single-frequency (sine) or combination of frequencies [sum-of-sines (SOS)] stimulus for head or target motion. The resulting eye movements typically contain a smooth tracking component, which follows the stimulus, in which are interspersed rapid eye movements (saccades or fast phases). The parameters of the smooth tracking--the amplitude and phase of each component frequency--are of interest; many methods have been devised that attempt to identify and remove the fast eye movements from the smooth. We describe a new approach to this problem, tailored to both single-frequency and sum-of-sines stimulation of the human linear vestibulo-ocular reflex. An approximate derivative is used to identify fast movements, which are then omitted from further analysis. The remaining points form a series of smooth tracking segments. A genetic algorithm is used to fit these segments together to form a smooth (but disconnected) wave form, by iteratively removing biases due to the missing fast phases. A genetic algorithm is an iterative optimization procedure; it provides a basis for extending this approach to more complex stimulus-response situations. In the SOS case, the genetic algorithm estimates the amplitude and phase values of the component frequencies as well as removing biases.

Dynamics of the human linear vestibulo-ocular reflex at medium frequency and modification by short-term training

We study here the effect of a short-term training paradigm on the gain and phase of the human translational VOR (the linear VOR: LVOR). Subjects were exposed to lateral sinusoidal translations on a sled, at 0.5 Hz, 0.3 g peak acceleration. With subjects tracking a remembered target at 1.2 m, the LVOR (slow-phase) under these conditions typically has a phase lead or lag, and a gain that falls short of compensatory. To induce short-term adaptation (training), we presented an earth-fixed visual scene at 1.2 m during sinusoidal translation (x 1 viewing) for 20 minutes, so as to drive the LVOR toward compensatory phase and gain. We examined both the slow-phase and the saccadic responses to these stimuli. Testing after training showed changes in slow-component gain and phase which were mostly but not always in the compensatory direction. These changes were more consistent in naive subjects than in subjects who had previous LVOR experience. Changes in gain were seen with step as well as sinusoidal test stimuli; gain changes were not correlated with vergence changes. There was a strong correlation between gain changes and phase changes across subjects. Fast phases (catch-up saccades) formed a large component of the LVOR under our testing conditions (approximately 30% of the changes in gain but not in phase due to training.

The human linear vestibulo-ocular reflex to transient accelerations: Visual modulation of suppression and enhancement

Visual modulation of the linear vestibulo-ocular reflex (LVOR) was investigated in 4 normal subjects exposed to translational interaural transient accelerations of 0.08 g and 0.17 g. Binocular eye movements were recorded with the scleral search-coil technique. LVOR modulation with target proximity was studied using earth-fixed targets at distances of 30 and 60 cm (LVOR-E). LVOR suppression (LVOR-S) was provoked by similar targets which were head-fixed. For both conditions, linear acceleration evoked compensatory slow-phases whose velocities were, from onset, enhanced in proportion to acceleration and target proximity. At 80 ms after motion onset, i.e. before visually-guided eye movements could aid target fixation, gains (eye velocity/relative target velocity) during LVOR-E averaged 0.32 (S.D. 0.07) over all combinations of accelerations and target distances. At this time, eye velocities for LVOR-S were on average 33% lower than for LVOR-E (1.8 degrees/s vs. 2.7 degrees/s). During LVOR-S, a marked suppression of eye movements appeared at 102 ms (S.D. 10 ms). We conclude that mechanisms other than pursuit can be used to attenuate the LVOR at < 80 ms but their effect is weak. The marked suppression observed around 100 ms might be due to an early visual effect on vestibular pathways or by some independent voluntary control mechanism.

Adaptation of the phase of the human linear vestibulo-ocular reflex (LVOR) and effects on the oculomotor neural integrator

The phase of the translational linear VOR (LVOR) can be adaptively modified by exposure to a visual-vestibular mismatch. We extend here our earlier work on LVOR phase adaptation, and discuss the role of the oculomotor neural integrator. Ten subjects were oscillated laterally at 0.5 Hz, 0.3 g peak acceleration, while sitting upright on a linear sled. LVOR was assessed before and after adaptation with subjects tracking the remembered location of a target at 1 m in the dark. Phase and gain were measured by fitting sine waves to the desaccaded eye movements, and comparing sled and eye position. To adapt LVOR phase, the subject viewed a computer-generated stereoscopic visual display, at a virtual distance of 1 m, that moved so as to require either a phase lead or a phase lag of 53 deg. Adaptation lasted 20 min, during which subjects were oscillated at 0.5 Hz/0.3 g. Four of five subjects produced an adaptive change in the lag condition (range 4-45 deg), and each of five produced a change in the lead condition (range 19-56 deg), as requested. Changes in drift on eccentric gaze suggest that the oculomotor velocity-to-position integrator may be involved in the phase changes.

Effect of adaptive plasticity of linear vestibulo-ocular reflex upon angular vestibulo-ocular reflex

Objective: The vestibulo-ocular reflex (VOR) produces compensatory eye movements during head movements. The VOR consists of the angular VOR and the linear VOR. The VOR is under adaptive control that corrects VOR performance when visual-vestibular mismatch arises during head movements. Most experiments concerning plasticity of the VOR have used the angular VOR. So far, there has been no investigation on the effect of adaptive plasticity of the linear VOR on the angular VOR. In this study, using a linear sled, we tested the hypothesis that the angular VOR is altered by changes in the linear VOR. Methods: To modify the linear VOR, we used an adaptation paradigm. Eight subjects were translated sinusoidally at 0.125 Hz and 0.16 g peak acceleration along their inter-aural axis for 40 min, while viewing earth-fixed vertical stripes on the wall while wearing the binocular magnifying lenses. Six of the eight subjects showed an increase in linear VOR sensitivity after adaptation. Each of the six subjects who showed an increase in linear VOR sensitivity after adaptation also showed an increased angular VOR gain at 0.125 Hz. Conclusion: These results suggest that the linear VOR and the angular VOR share common neural pathways in such a way that a change in the synaptic efficacy of one pathway is accompanied by a commensurate change in the other.

Effect of adaptation to telescopic spectacles on the initial human horizontal vestibuloocular reflex.

Gain of the vestibuloocular reflex (VOR) not only varies with target distance and rotational axis, but can be chronically modified in response to prolonged wearing of head-mounted magnifiers. This study examined the effect of adaptation to telescopic spectacles on the variation of the VOR with changes in target distance and yaw rotational axis for head velocity transients having peak accelerations of 2,800 and 1,000 degrees /s(2). Eye and head movements were recorded with search coils in 10 subjects who underwent whole body rotations around vertical axes that were 10 cm anterior to the eyes, centered between the eyes, between the otoliths, or 20 cm posterior to the eyes. Immediately before each rotation, subjects viewed a target 15 or 500 cm distant. Lighting was extinguished immediately before and was restored after completion of each rotation. After initial rotations, subjects wore 1.9x magnification binocular telescopic spectacles during their daily activities for at least 6 h. Test spectacles were removed and measurement rotations were repeated. Of the eight subjects tolerant of adaptation to the telescopes, six demonstrated VOR gain enhancement after adaptation, while gain in two subjects was not increased. For all subjects, the earliest VOR began 7-10 ms after onset of head rotation regardless of axis eccentricity or target distance. Regardless of adaptation, VOR gain for the proximate target exceeded that for the distant target beginning at 20 ms after onset of head rotation. Adaptation increased VOR gain as measured 90-100 ms after head rotation onset by an average of 0.12 +/- 0.02 (SE) for the higher head acceleration and 0.19 +/- 0.02 for the lower head acceleration. After adaptation, four subjects exhibited significant increases in the canal VOR gain only, whereas two subjects exhibited significant increases in both angular and linear VOR gains. The latencies of linear and early angular target distance effects on VOR gain were unaffected by adaptation. The earliest significant change in angular VOR gain in response to adaptation occurred 50 and 68 ms after onset of the 2,800 and 1,000 degrees /s(2) peak head accelerations, respectively. The latency of the adaptive increase in linear VOR gain was approximately 50 ms for the peak head acceleration of 2,800 degrees /s(2), and 100 ms for the peak head acceleration of 1,000 degrees /s(2). Thus VOR gain changes and latency were consistent with modification in the angular VOR in most subjects, and additionally in the linear VOR in a minority of subjects.

Effects of limb proprioception on human linear VOR and pursuit eye movements

Effects of limb proprioception on human linear VOR and pursuit eye movements

Effect of viewing distance on the generation of vertical eye movements during locomotion.

Vertical head and eye coordination was studied as a function of viewing distance during locomotion. Vertical head translation and pitch movements were measured using a video motion analysis system (Optotrak 3020). Vertical eye movements were recorded using a video-based pupil tracker (Iscan). Subjects (five) walked on a linear treadmill at a speed of 1.67 m/s (6 km/h) while viewing a target screen placed at distances ranging from 0.25 to 2.0 m at 0. 25-m intervals. The predominant frequency of vertical head movement was 2 Hz. In accordance with previous studies, there was a small head pitch rotation, which was compensatory for vertical head translation. The magnitude of the vertical head movements and the phase relationship between head translation and pitch were little affected by viewing distance, and tended to orient the naso-occipital axis of the head at a point approximately 1 m in front of the subject (the head fixation distance or HFD). In contrast, eye velocity was significantly affected by viewing distance. When viewing a far (2-m) target, vertical eye velocity was 180 degrees out of phase with head pitch velocity, with a gain of 0. 8. This indicated that the angular vestibulo-ocular reflex (aVOR) was generating the eye movement response. The major finding was that, at a close viewing distance (0.25 m), eye velocity was in phase with head pitch and compensatory for vertical head translation, suggesting that activation of the linear vestibulo-ocular reflex (lVOR) was contributing to the eye movement response. There was also a threefold increase in the magnitude of eye velocity when viewing near targets, which was consistent with the goal of maintaining gaze on target. The required vertical lVOR sensitivity to cancel an unmodified aVOR response and generate the observed eye velocity magnitude for near targets was almost 3 times that previously measured. Supplementary experiments were performed utilizing body-fixed active head pitch rotations at 1 and 2 Hz while viewing a head-fixed target. Results indicated that the interaction of smooth pursuit and the aVOR during visual suppression could modify both the gain and phase characteristics of the aVOR at frequencies encountered during locomotion. When walking, targets located closer than the HFD (1.0 m) would appear to move in the same direction as the head pitch, resulting in suppression of the aVOR. The results of the head-fixed target experiment suggest that phase modification of the aVOR during visual suppression could play a role in generating eye movements consistent with the goal of maintaining gaze on targets closer than the HFD, which would augment the lVOR response.

Horizontal linear vestibulo-ocular reflex testing in patients with peripheral vestibular disorders.

Horizontal eye movements in response to lateral head translation [linear vestibulo-ocular reflex (LVOR)] in normal subjects and in patients with bilateral vestibular failure (n = 14), unilateral vestibular nerve section (n = 9), and benign positional vertigo (n = 14), were studied. LVORs were elicited in darkness by step acceleration (0.24 g) of the whole body along the interaural axis. (1) In patients with bilateral vestibular failure, LVORs were either absent or abnormal with asymmetries, diminished velocities, and prolonged latencies. Measurements of dynamic visual acuity during linear self-motion showed decreased performance in patients at 1.0 and 1.5 Hz, which correlated with absent or delayed LVORs. These findings demonstrate the functional role of LVORs for dynamic visual acuity. (2) Early after vestibular nerve section, LVORs were diminished or absent with head acceleration toward the operated ear and normal in the opposite direction. After 6-10 weeks, responses were symmetrical again. Thus, a single utricle appears to be polarized with respect to the LVOR early after unilateral vestibular loss generating mostly contraversive responses. (3) Patients with benign positional vertigo showed mostly normal LVORs, which can be explained by minor utricular damage or central compensation of a chronic unilateral deficit.

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation.

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal-related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal's head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3-1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement-related units were significantly affected by viewing distance. The viewing distance-related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)-related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance-related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal-related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR.

Characteristics of the VOR in response to linear acceleration.

The primate linear VOR (LVOR) includes two forms. First, eye-movement responses to translation [e.g., horizontal responses to interaural (i.a.) motion] help maintain binocular fixation on targets, and therefore a stable bifoveal image. The translational LVOR is strongly modulated by fixation distance, and operates with high-pass dynamics (> 1 Hz). Second, other LVOR responses occur that cannot be compensatory for translation and instead seem compensatory for head tilt. This reflects an otolith response ambiguity--that is, an inability to distinguish head translation from head tilt relative to gravity. Thus, ocular torsion is appropriately compensatory for head roll-tilt, but also occurs during IA translation, since both stimuli entail IA acceleration. Unlike the IA-horizontal response, IA torsion behaves with low-pass dynamics (with respect to "tilt"), and is uninfluenced by fixation distance. Interestingly, roll-tilt, like IA translation, also produces both horizontal (a translational reflex) and torsional (a tilt reflex) responses, further emphasizing the ambiguity problem. Early data from subjects following unilateral labyrinthectomy, which demonstrates a general immediate decline in translational LVOR responses, are also presented, followed by only modest recovery over several months. Interestingly, the usual high-pass dynamics of these reflexes shift to an even higher cutoff. Both eyes respond roughly equally, suggesting that unilateral otolith input generates a binocularly symmetric LVOR.

Signal Processing Related to the Vestibulo‐Ocular Reflex during Combined Angular Rotation and Linear Translation of the Head

The contributions of vestibular nerve afferents and central vestibular pathways to the angular (AVOR) and linear (LVOR) vestibulo-ocular reflex were studied in squirrel monkeys during fixation of near and far targets. Irregular vestibular afferents did not appear to be necessary for the LVOR, since when they were selectively silenced with galvanic currents the LVOR was essentially unaffected during both far- and near-target viewing. The linear translation signals generated by secondary AVOR neurons in the vestibular nuclei were, on average, in phase with head velocity, inversely related to viewing distance, and were nearly as strong as AVOR-related signals. We suggest that spatial-temporal transformation of linear head translation signals to angular eye velocity commands is accomplished primarily by the addition of viewing distance multiplied, centrally integrated, otolith regular afferent signals to angular VOR pathways.

Adaptive plasticity in the naso-occipital linear vestibulo-ocular reflex.

The linear vestibulo-ocular reflex (LVOR) during motion along the naso-occipital (NO) axis is governed by eye position and viewing distance. These influences are necessary for the LVOR to maintain stable foveal images during head translation. The response to NO translation must be large when eye position is eccentric from the axis of head motion (i.e., during lateral gaze) and must diminish as eye position approaches straight-ahead, eventually reaching zero when the eye is aligned with the NO axis of motion (the "null point"). As eye position crosses to the opposite side, the LVOR response must reappear, but in the opposite direction, and must grow in magnitude as eccentricity increases. To determine whether the NO-LVOR is subject to adaptive plastic mechanisms, squirrel monkeys were conditioned during NO translation while they binocularly viewed a rich visual field through parallel base-right or base-left wedge prisms. This optical method effectively shifted the visual world 9 degrees leftward or rightward, respectively, thus inducing a mismatch between vision and the NO-LVOR during head movements. To restore compensatory function, the relationship between LVOR sensitivity and horizontal eye position must shift by 9 degrees in the same direction as the visual image shift, effectively shifting the null point. After 2 h of adaptive conditioning, all monkeys exhibited an adaptive shift in the appropriate direction by an average of 3.0 degrees (range 0.7-5.0 degrees), corresponding to 33% of the geometrically required adaptation.