Vestibulo-ocular Reflex Adaptation Training Research Articles

The vergence-mediated gain increase: Physiology and clinical relevance.

During near-viewing, the vestibulo-ocular reflex (VOR) response/gain increases to compensate for the relatively larger translation of the eyes with respect to the target. To review vergence-mediated gain increase (VMGI) testing methods stimuli and responses (latency and amplitude), peripheral/central pathways and clinical relevance. The authors discuss publications listed in PUBMED since 1980 in the light of their own studies. The VMGI can be measured during rotational, linear and combined head accelerations. It has short-latency, non-compensatory amplitude, and relies on irregularly discharging peripheral afferents and their pathways. It is driven by a combination of perception, visual-context and internal modelling. Currently, there are technical barriers that hinder VMGI measurement in the clinic. However, the VMGI may have diagnostic value, especially with regards to measuring otolith function. The VMGI also may have potential value in rehabilitation by providing insight about a patient's lesion and how to best tailor a rehabilitation program for them, that potentially includes VOR adaptation training during near-viewing.

Vestibulo-Ocular Reflex Short-Term Adaptation Is Halved After Compensation for Unilateral Labyrinthectomy.

Several prior studies, including those from this laboratory, have suggested that vestibulo-ocular reflex (VOR) adaptation and compensation are two neurologically related mechanisms. We therefore hypothesised that adaptation would be affected by compensation, depending on the amount of overlap between these two mechanisms. To better understand this overlap, we examined the effect of gain-increase (gain = eye velocity/head velocity) adaptation training on the VOR in compensated mice since both adaptation and compensation mechanisms are presumably driving the gain to increase. We tested 11 cba129 controls and 6 α9-knockout mice, which have a compromised efferent vestibular system (EVS) known to affect both adaptation and compensation mechanisms. Baseline VOR gains across frequencies (0.2 to 10Hz) and velocities (20 to 100°/s) were measured on day 28 after unilateral labyrinthectomy (UL) and post-adaptation gains were measured after gain-increase training on day 31 post-UL. Our findings showed that after chronic compensation gain-increase adaptation, as a percentage of baseline, in both strains of mice (~14%), was about half compared to their previously reported healthy, non-operated counterparts (~32%). Surprisingly, there was no difference in gain-increase adaptation between control and α9-knockout mice. These data support the notion that adaptation and compensation are separate but overlapping processes. They also suggest that half of the original adaptation capacity remained in chronically compensated mice, regardless of EVS compromise associated with α9-knockout mice, and strongly suggest VOR adaptation training is a viable treatment strategy for vestibular rehabilitation therapy and, importantly, augments the compensatory process.

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.

Retinal Image Slip Must Pass the Threshold for Human Vestibulo-Ocular Reflex Adaptation.

We sought to determine whether repeated vestibulo-ocular reflex (VOR) adaptation training to increase the VOR gain (eye/head velocity) had a lasting effect in normal subjects and whether there was a retinal image slip tolerance threshold for VOR adaptation. We used the unilateral incremental VOR adaptation technique and horizontal active (self-generated, predictable) head impulses as the vestibular stimulus. Both active and passive (imposed, unpredictable) head impulse VOR gains were measured before and after unilateral incremental VOR adaptation training. The adapting side was pseudo-randomized for left or right. We tested ten normal subjects over one block (10 sessions over 12days) of VOR adaptation training and testing, immediately followed by a second block (5 sessions over 19days) of testing only without training. Our findings show robust short-term VOR adaptation of ~ 10% immediately after each 15-min training session, but that the daily pre-adaptation gain was most different on days 1 and 2, and for subsequent training days before saturating to ~ 5% greater than the pre-adaptation gain on day 1. This increase was partially retained for 19days after regular training stopped. The data suggest that stable vision in normal subjects is maintained when there is < 5% deviation in VOR gain from the original baseline, which corresponds to < 9°/s retinal image slip. Below this threshold, there is poor adaptive drive to return the gain to its original baseline value.

Human vestibulo-ocular reflex adaptation is frequency selective

The vestibulo-ocular reflex (VOR) is the only system that maintains stable vision during rapid head rotations. The VOR gain (eye/head velocity) can be trained to increase using a vestibular-visual mismatch stimulus. We sought to determine whether low-frequency (sinusoidal) head rotation during training leads to changes in the VOR during high-frequency head rotation testing, where the VOR is more physiologically relevant. We tested eight normal subjects over three sessions. For training protocol 1, subjects performed active sinusoidal head rotations at 1.3 Hz while tracking a laser target, whose velocity incrementally increased relative to head velocity so that the VOR gain required to stabilize the target went from 1.1 to 2 over 15 min. Protocol 2 was the same as protocol 1, except that head rotations were at 0.5 Hz. For protocol 3, head rotation frequency incrementally increased from 0.5 to 2 Hz over 15 min, while the VOR gain required to stabilize the target was kept at 2. We measured the active and passive, sinusoidal (1.3Hz) and head impulse VOR gains before and after each protocol. Sinusoidal and head impulse VOR gains increased in protocols 1 and 3; however, although the sinusoidal VOR gain increase was ~20%, the related head impulse gain increase was only ~10%. Protocol 2 resulted in no-gain adaptation. These data show human VOR adaptation is frequency selective, suggesting that if one seeks to increase the higher-frequency VOR response, i.e., where it is physiologically most relevant, then higher-frequency head movements are required during training, e.g., head impulses.NEW & NOTEWORTHY This study shows that human vestibulo-ocular reflex adaptation is frequency selective at frequencies >0.3 Hz. The VOR in response to mid- (1.3 Hz) and high-frequency (impulse) head rotations were measured before and after mid-frequency sinusoidal VOR adaptation training, revealing that the mid-frequency gain change was higher than high-frequency gain change. Thus, if one seeks to increase the higher-frequency VOR response, where it is physiologically most relevant, then higher-frequency head movements are required during training.

New advances regarding adaptation of the vestibulo-ocular reflex.

This is a review summarizing the development of vestibulo-ocular reflex (VOR) adaptation behavior with relevance to rehabilitation over the last 10 years and examines VOR adaptation using head-on-body rotations, specifically the influence of training target contrast, position and velocity error signal, active vs. passive head rotations, and sinusoidal vs. head impulse rotations. This review discusses optimization of the single VOR adaptation training session, consolidation between repeated training sessions, and dynamic incremental VOR adaptation. Also considered are the effects of aging and the roles of the efferent vestibular system, cerebellum, and otoliths on angular VOR adaptation. Finally, this review examines VOR adaptation findings in studies using whole body rotations.

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.

Aging reduces the high-frequency and short-term adaptation of the vestibulo-ocular reflex in mice

Prevailing evidence indicates a relatively late life decline in human vestibulo-ocular reflex (VOR) function. Although mice are commonly used in mechanistic studies of vestibular function, it remains unclear whether aging produces a corresponding decline in VOR function in mice. We sought to determine how the baseline VOR and its short-term adaptation were affected by aging. We tested 8 young (3-month old) and 8 aged (30-month old–equivalent to a ∼80-year old human) C57BL/6 mice. We measured their VOR response to whole-body static tilts and during 0.1–10 Hz whole-body sinusoidal and transient rotations before and after VOR adaptation training. Our data revealed minimal differences in static counter-tilt response between young and aged mice, but a significant deficit in baseline VOR gain in aged mice during transient rotations. Moreover, aged mice had a significant decrease in short-term VOR adaptation, particularly for training that sought to decrease the VOR response.

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.