Passive Vestibulo-ocular Reflex Research Articles

Human Vestibulo-Ocular Reflex Adaptation Reduces when Training Demand Variability Increases.

One component of vestibular rehabilitation in patients with vestibulo-ocular reflex (VOR) hypofunction is gaze-stabilizing exercises that seek to increase (adapt) the VOR response. These prescribed home-based exercises are performed by the patient and thus their use/training is inherently variable. We sought to determine whether this variability affected VOR adaptation in ten healthy controls (× 2 training only) and ten patients with unilateral vestibular hypofunction (× 1 and × 2 training). During × 1 training, patients actively (self-generated, predictable) move their head sinusoidally while viewing a stationary fixation target; for × 2 training, they moved their outstretched hand anti-phase with their head rotation while attempting to view a handheld target. We defined the latter as manual × 2 training because the subject manually controls the target. In this study, head rotation frequency during training incrementally increased 0.5-2Hz over 20min. Active and passive (imposed, unpredictable) sinusoidal (1.3-Hz rotations) and head impulse VOR gains were measured before and after training. We show that for controls, manual × 2 training resulted in significant sinusoidal and impulse VOR adaptation of ~ 6% and ~ 3%, respectively, though this was ~two-thirds lower than increases after computer-controlled × 2 training (non-variable) reported in a prior study. In contrast, for patients, there was an increase in impulse but not sinusoidal VOR response after a single session of manual × 2 training. Patients had more than double the variability in VOR demand during manual × 2 training compared to controls, which could explain why adaptation was not significant in patients. Our data suggest that the clinical × 1 gaze-stabilizing exercise is a weak stimulus for VOR adaptation.

The instantaneous training demand drives vestibulo-ocular reflex adaptation.

The vestibulo-ocular reflex (VOR) maintains stable vision during rapid head rotations by rotating the eyes in the opposite direction to the head. The latency between onset of the head rotation and onset of the eye rotation is 5-8ms in healthy humans. However, VOR latency can be 3-4 times larger in patients treated with intra-tympanic gentamicin. A prior study showed that latency can be trained with head rotations at 0.2Hz. We sought to determine how the VOR is affected when a delay between vestibular and visual stimuli is added during adaptation training with high-frequency head rotations (impulses), where the VOR is the main vision-stabilizing system. Using a variant of the incremental VOR adaptation technique, the delay between head rotation onset and movement onset of a visual target was gradually increased. With this training, the instantaneous VOR gain demand (= target/head velocity) varied from less than unity to greater than unity during each head impulse, albeit in a consistent and repeatable way. We measured the active and passive VOR gain and latency before and after VOR adaptation training in healthy normal subjects. There was no significant change in VOR latency across subjects; however, there was a significant decrease in VOR gain of - 6.0 ± 4.5%. These data suggest that during high-frequency head rotations delay/latency is interpreted as a changing instantaneous VOR gain demand. Although the gain demand in this study had a complex trajectory, adaptation was evident with the VOR seeming to use an average of the instantaneous gain demand.

Convergence Vestibulo-ocular Reflex in Unilateral Vestibular Hypofunction: Behavioral Evidence in Support of a Novel Gaze Stability Exercise

Convergence of the eyes during head rotation increases the gain (eye velocity/head velocity) of the vestibulo-ocular reflex (VOR). We sought to know whether convergence would increase the VOR gain (mean + SD) in unilateral vestibular hypofunction (UVH). Vestibulo-ocular reflex gain during ipsi- and contralesional horizontal head rotation at near (15 cm) and far (150 cm) targets was measured in 22 subjects with UVH and 12 healthy controls. Retinal slip was estimated (retinal slip index [RSI]) as the difference between ideal VOR gain (no retinal slip) and the actual VOR gain. Convergence did not significantly enhance VOR gain for ipsilesional rotation (mean difference, 0.04; 95% confidence interval [CI], -0.01 to 0.09), near viewing (0.77 ± 0.34) versus far viewing (0.72 ± 0.29), yet the VOR gain during contralesional rotation was greater for near viewing (1.20 ± 0.23) than for far viewing (0.97 ± 0.21; mean difference, 0.23; 95% CI, 0.13-0.32). In the 36% of subjects with recovery of their ipsilesional VOR gain, the vergence effect trended to recover (far VOR gain: 1.06 ± 0.17 vs near VOR gain 1.16 ± 0.21; mean difference, 0.10; 95% CI, -0.02 to 0.22). Ipsilesional head rotation induced greater retinal slip for near (RSI = 0.90 ± 0.34) targets than for far targets (RSI = 0.35 ± 0.29; mean difference, 0.56; 95% CI, 0.51-0.61). The convergence-mediated VOR gain enhancement is preserved during contralesional but impaired during ipsilesional head rotation. Recovery of ipsilesional passive VOR gain does not equate to restored convergence enhancement, although it did increase ∼10%. These data suggest head motion viewing near targets will increase retinal slip, which warrants consideration as a gaze stability exercise for subjects with UVH.Video Abstract available for more insights from the authors (see Video, Supplemental Digital Content 1, available at: http://links.lww.com/JNPT/A325).

Incremental Vestibulo-ocular Reflex Adaptation Training Dynamically Tailored for Each Individual.

Unilateral incremental vestibulo-ocular reflex (VOR) adaptation (IVA) increases the VOR gain (= eye/head velocity) for head rotations to one side by ∼10%. Prior IVA studies involved setting the initial VOR training gain demand at the subject's starting value (= 1 in a healthy subject), with the gain preset to increment by 0.1 every 90 seconds over 15 minutes, defined as Static IVA. We determined whether a dynamically calculated gain demand (= "actual gain" + 0.1) would result in greater adaptation, defined as Dynamic IVA. Using a hybrid video-oculography and StableEyes training system, we measured the active (self-generated head impulse) and passive (imposed, unpredictable head impulse) VOR gain in 8 healthy subjects before and after 15 minutes of Static (ie, preset) and Dynamic IVA training consisting of active, leftward and rightward, horizontal head impulses (peak amplitude 15°, peak velocity 150°/s, and peak acceleration 3000°/s). We also measured the active VOR gain during training. The VOR gain increase toward the adapting side was ∼5% larger after Dynamic compared with Static IVA training (Dynamic: 13.9% ± 5.2%, Static: 9.4% ± 7.3%; P < 0.05). Our data suggest that 17°/s retinal image slip (due to the 0.1 gain difference between demand and actual gain) is sufficient to drive robust VOR adaptation. The implications for vestibular rehabilitation are that Dynamic IVA training not only produces better VOR adaptation but also allows more flexible training, for example, training can be spread over several smaller time blocks, without undoing prior adaptation.

Human Vestibulo-Ocular Reflex Adaptation Training: Time Beats Quantity.

The vestibulo-ocular reflex (VOR) is the main gaze stabilising system during rapid head movements. The VOR is highly plastic and its gain (eye/head velocity) can be increased via training that induces an incrementally increasing retinal image slip error signal to drive VOR adaptation. Using the unilateral incremental VOR adaptation technique and horizontal active head impulses as the vestibular stimulus, we sought to determine the factors important for VOR adaptation including: the total training time, ratio and number of head impulses to each side (adapting and non-adapting sides; the adapting side was pseudo-randomised left or right) and exposure time to the visual target during each head impulse. We tested 11 normal subjects, each over 5 separate sessions and training protocols. The basic training protocol (protocol one) consisted of unilateral incremental VOR adaptation training lasting 15min with the ratio of head impulses to each side 1:1. Each protocol varied from the basic. For protocol two, the ratio of impulses were in favour of the adapting side by 2:1. For protocol three, all head impulses were towards the adapting side and the training only lasted 7.5min. For protocol four, all impulses were towards the adapting side and lasted 15min. For protocol five, all head impulses were to the adapting side and the exposure time to the visual target during each impulse was doubled. We measured the active and passive VOR gains before and after the training. Albeit with small sample size, our data suggest that the total training time and the visual target exposure time for each head impulse affected adaptation, whereas the total number and repetition rate of head impulses did not. These data have implications for vestibular rehabilitation, suggesting that quality and duration of VOR adaptation exercises are more important than rapid repetition of exercises.

Human Vestibulo-Ocular Reflex Adaptation: Consolidation Time Between Repeated Training Blocks Improves Retention.

We sought to determine if separating vestibulo-ocular reflex (VOR) adaptation training into training blocks with a consolidation (rest) period in between repetitions would result in improved VOR adaptation and retention. Consolidation of motor learning refers to the brain benefitting from a rest period after prior exposure to motor training. The role of consolidation on VOR adaptation is unknown, though clinicians often recommend rest periods as a part of vestibular rehabilitation. The VOR is the main gaze stabilising system during rapid head movements. The VOR is highly plastic and its gain (eye/head velocity) can be increased via training that induces an incrementally increasing retinal image slip error signal to drive VOR adaptation. The unilateral incremental adaptation technique typically consists of one 15-min training block leading to an increase in VOR gain of ~ 10% towards the training side. We tested nine normal subjects, each over six separate sessions/days. Three training protocols/sessions were 5min each (1 × 5-min training) and three training protocols/sessions were 55min each. Each 55-min protocol comprised 5-min training, 20-min rest, 5-min training, 20-min rest, 5-min training (3 × 5-min training). Active and passive VOR gains were measured before and after training. For training with consolidation breaks, VOR gain retention was measured over 1h. The VOR gain increase after 1 × 5-min training was 3.1 ± 2.1% (P < 0.01). One might expect that repeating this training three times would result in × 3 total increase of 9.3%; however, the gain increase after 3 × 5-min training was only 7.1 ± 2.8% (P < 0.001), suggesting that consolidation did not improve VOR adaptation for our protocols. However, retention was improved by the addition of consolidation breaks, i.e. gains did not decrease over 1h (P = 0.43). These data suggest that for optimal retention VOR adaptation exercises should be performed over shorter repeated blocks.

The Effect of Visual Contrast on Human Vestibulo-Ocular Reflex Adaptation.

The vestibulo-ocular reflex (VOR) is the main retinal image stabilising mechanism during rapid head movement. When the VOR does not stabilise the world or target image on the retina, retinal image slip occurs generating an error signal that drives the VOR response to increase or decrease until image slip is minimised, i.e. VOR adaptation occurs. Visual target contrast affects the human smooth pursuit and optokinetic reflex responses. We sought to determine if contrast also affected VOR adaptation. We tested 12 normal subjects, each over 16 separate sessions. For sessions 1-14, the ambient light level (lx) during adaptation training was as follows: dark, 0.1, 0.2, 0.3, 0.5, 0.7, 1, 2, 8, 16, 32, 64, 128 and 255lx (light level for a typical room). For sessions 15-16, the laser target power (related to brightness) was halved with ambient light at 0 and 0.1lx. The adaptation training lasted 15min and consisted of left/right active head impulses. The VOR gain was challenged to increment, starting at unity, by 0.1 every 90s for rotations to the designated adapting side and fixed at unity towards the non-adapting side. We measured active and passive VOR gains before and after adaptation training. We found that for both the active and passive VOR, there was a significant increase in gain only towards the adapting side due to training at contrast level 1.5k and above (2lx and below). At contrast level 261 and below (16lx and above), adaptation training resulted in no difference between adapting and non-adapting side gains. Our modelling suggests that a contrast threshold of ~1000, which is 60 times higher than that provided by typical room lighting, must be surpassed for robust active and passive VOR adaptation. Our findings suggest contrast is an important factor for adaptation, which has implication for rehabilitation programs.

The effect of retinal image error update rate on human vestibulo-ocular reflex gain adaptation.

The primary function of the angular vestibulo-ocular reflex (VOR) is to stabilise images on the retina during head movements. Retinal image movement is the likely feedback signal that drives VOR modification/adaptation for different viewing contexts. However, it is not clear whether a retinal image position or velocity error is used primarily as the feedback signal. Recent studies examining this signal are limited because they used near viewing to modify the VOR. However, it is not known whether near viewing drives VOR adaptation or is a pre-programmed contextual cue that modifies the VOR. Our study is based on analysis of the VOR evoked by horizontal head impulses during an established adaptation task. Fourteen human subjects underwent incremental unilateral VOR adaptation training and were tested using the scleral search coil technique over three separate sessions. The update rate of the laser target position (source of the retinal image error signal) used to drive VOR adaptation was different for each session [50 (once every 20 ms), 20 and 15/35 Hz]. Our results show unilateral VOR adaptation occurred at 50 and 20 Hz for both the active (23.0 ± 9.6 and 11.9 ± 9.1% increase on adapting side, respectively) and passive VOR (13.5 ± 14.9, 10.4 ± 12.2%). At 15 Hz, unilateral adaptation no longer occurred in the subject group for both the active and passive VOR, whereas individually, 4/9 subjects tested at 15 Hz had significant adaptation. Our findings suggest that 1-2 retinal image position error signals every 100 ms (i.e. target position update rate 15-20 Hz) are sufficient to drive VOR adaptation.

Pilot study of a new rehabilitation tool: improved unilateral short-term adaptation of the human angular vestibulo-ocular reflex.

Unilateral vestibulo-ocular reflex (VOR) short-term adaptation training causes some increase toward the nonadapting side (~30% of increase on adapting side). We conducted a pilot study to determine if the increase could be reduced by providing a visual stimulus during rotations to the nonadapting side. Unilateral vestibular short-term adaptation is a technique that could increase the ipsilesional VOR response of vestibular patients with unilateral hypofunction. However, this technique results in the VOR response increasing for rotations toward the nonadapting (normal) side, which is undesirable because the VOR will be overcompensatory (causing nonstable vision) during head rotations toward the normal side. We built a portable helmet device that sensed horizontal angular head velocity to generate a visual target that required a preset VOR gain (eye velocity/head velocity) for optimal image stabilization that could be set differently for leftward and rightward head rotations. We tested 10 subjects (six controls and four patients with vestibular hypofunction). We measured the active and passive VOR gain during high-peak-acceleration, unilateral, transient head rotations (head impulses) before and after unilateral VOR adaptation training. In control subjects, for rotations toward the adapting side (target gain = 1.5), the VOR gain increased because of training by 26.1% ± 23.4% during active head impulses and by 14.6% ± 13.0% during passive head impulses. In contrast, for rotations toward the nonadapting side, there were no statistically significant increases. A visual stimulus driving the VOR gain to unity toward the nonadapting side aids unilateral adaptation more so than no visual stimulus.

Unilateral Adaptation of the Human Angular Vestibulo-Ocular Reflex

A recent study showed that the angular vestibulo-ocular reflex (VOR) can be better adaptively increased using an incremental retinal image velocity error signal compared with a conventional constant large velocity-gain demand (×2). This finding has important implications for vestibular rehabilitation that seeks to improve the VOR response after injury. However, a large portion of vestibular patients have unilateral vestibular hypofunction, and training that raises their VOR response during rotations to both the ipsilesional and contralesional side is not usually ideal. We sought to determine if the vestibular response to one side could selectively be increased without affecting the contralateral response. We tested nine subjects with normal vestibular function. Using the scleral search coil and head impulse techniques, we measured the active and passive VOR gain (eye velocity / head velocity) before and after unilateral incremental VOR adaptation training, consisting of self-generated (active) head impulses, which lasted ≈ 15 min. The head impulses consisted of rapid, horizontal head rotations with peak-amplitude 15°, peak-velocity 150°/s and peak-acceleration 3,000°/s(2). The VOR gain towards the adapting side increased after training from 0.92 ± 0.18 to 1.11 ± 0.22 (+22.7 ± 20.2 %) during active head impulses and from 0.91 ± 0.15 to 1.01 ± 0.17 (+11.3 ± 7.5 %) during passive head impulses. During active impulses, the VOR gain towards the non-adapting side also increased by ≈ 8 %, though this increase was ≈ 70 % less than to the adapting side. A similar increase did not occur during passive impulses. This study shows that unilateral vestibular adaptation is possible in humans with a normal VOR; unilateral incremental VOR adaptation may have a role in vestibular rehabilitation. The increase in passive VOR gain after active head impulse adaptation suggests that the training effect is robust.

False-Positive Head-Impulse Test in Cerebellar Ataxia

The objective of this study was to compare the findings of the bedside head-impulse test (HIT), passive head rotation gain, and caloric irrigation in patients with cerebellar ataxia (CA). In 16 patients with CA and bilaterally pathological bedside HIT, vestibuloocular reflex (VOR) gains were measured during HIT and passive head rotation by scleral search coil technique. Eight of the patients had pathologically reduced caloric responsiveness, while the other eight had normal caloric responses. Those with normal calorics showed a slightly reduced HIT gain (mean ± SD: 0.73 ± 0.15). In those with pathological calorics, gains 80 and 100 ms after the HIT as well as the passive rotation VOR gains were significantly lower. The corrective saccade after head turn occurred earlier in patients with pathological calorics (111 ± 62 ms after onset of the HIT) than in those with normal calorics (191 ± 17 ms, p = 0.0064). We identified two groups of patients with CA: those with an isolated moderate HIT deficit only, probably due to floccular dysfunction, and those with combined HIT, passive rotation, and caloric deficit, probably due to a peripheral vestibular deficit. From a clinical point of view, these results show that the bedside HIT alone can be false-positive for establishing a diagnosis of a bilateral peripheral vestibular deficit in patients with CA.

Effects of eccentric rotation on the human pitch vestibulo-ocular reflex

Conclusion. The pitch plane vestibulo-ocular reflex (VOR) gain and symmetry at low frequencies (≤0.3 Hz) are enhanced by otoliths and/or somatosensory sensory cues during combined angular and linear stimuli. We conclude that neural processing of these linear motion cues is used to improve the VOR when stimulus frequencies are below the optimal range for the canals. Objective. The purpose of this study was to examine the effects of eccentric rotation on the passive pitch VOR responses in humans. Subjects and methods. Eleven subjects were placed on their left sides (90° roll position) and rotated in the pitch plane about an earth-vertical axis at 0.13, 0.3, and 0.56 Hz. The inter-aural axis was either aligned with the axis of rotation (no modulation of linear acceleration) or offset from it by 50 cm (centripetal linear acceleration directed feet-ward). The modulation of pitch VOR responses was measured in the dark with a binocular videography system. Results. The pitch VOR gain was significantly increased and the VOR asymmetry was significantly reduced at the lowest stimulus frequencies during eccentric rotation. There was no effect of eccentric rotation on the pitch gain or asymmetry at the highest frequency tested.

Head unrestrained horizontal gaze shifts after unilateral labyrinthectomy in the rhesus monkey.

Following the orienting saccade of a combined eye-head gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) of near unity, is a manifestation of the vestibulo-ocular reflex (VOR). Acute unilateral labyrinthectomy (UL) causes severe asymmetry in the VOR during passive head rotations that recovers incompletely over time. The purpose of this investigation was to compare the recovery of the counterrotation gain during horizontal gaze shifts with that of the passive VOR after UL. During the 1st week after UL, counterrotation gains were asymmetric, being lower for head movements towards the lesion but nearly normal for head movements towards the intact side. Whereas this asymmetry in the counterrotation gain resolved within a week after UL, asymmetries in the passive VOR persisted. During the 1st week after UL, behavioral performance was generally poor, with a high incidence of inaccurate gaze shifts and larger latencies. In addition, animals used slower head movements such that peak head amplitude during the eye saccade was significantly lower during the 1st week after UL as compared to control values. Bilateral labyrinthectomy (BL) resulted in larger but symmetric deficits in counterrotation, which, contrary to the passive VOR, exhibited significant recovery over time. It is hypothesized that recovery of counterrotation gain after UL has contributions from multiple sources, including the contralateral intact labyrinth and an efference copy of the head movement.

Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization.

Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization. To study the contribution of the vestibular system to the coordinated eye and head movements of a gaze shift, we plugged the lumens of just the horizontal (n = 2) or all six semicircular canals (n = 1) in monkeys trained to make horizontal head-unrestrained gaze shifts to visual targets. After the initial eye saccade of a gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) near one has been attributed to the vestibuloocular reflex (VOR). One day after horizontal canal plugging, the gain of the passive horizontal VOR at frequencies between 0.1 and 1.0 Hz was <0.10 in the horizontal-canal-plugged animals and zero in the all-canal-plugged animal. One day after surgery, counterrotation gain was approximately 0.3 in the animals with horizontal canals plugged and absent in the animal with all canals plugged. As the time after plugging increased, so too did counterrotation gain. In all three animals, counterrotation gain recovered to between 0.56 and 0.75 within 80-100 days. The initial loss of compensatory counterrotation after plugging resulted in a gaze shift that ended long after the eye saccade and just before the end of the head movement. With recovery, the length of time between the end of the eye saccade and the end of the gaze movement decreased. This shortening of the duration of reduced gain counterrotation occurred both because head movements ended sooner and counterrotation gain returned to 1.0 more rapidly relative to the end of the eye saccade. Eye counterrotation was not due to activation of pursuit eye movements as it persisted when gaze shifts were executed to extinguished targets. Also counterrotation was not due simply to activation of neck receptors because counterrotation persisted after head movements were arrested in midflight. We suggest that the neural signal that is used to cause counterrotation in the absence of vestibular input is an internal copy of the intended head movement.

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

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.