Unidirectional Vertical Vestibuloocular Reflex Adaptation in Humans Using 1D and 2D Scenes.

HYPOTHESIS: The vertical vestibuloocular reflex (VOR) in response to pitch head impulses can be optimally trained to increase in one direction using a two-dimensional (2D) visual training target with minimal effect on the horizontal VOR. BACKGROUND: We modified the incremental VOR adaptation (IVA) technique, shown to increase the horizontal VOR in patients with vestibular hypofunction, to drive vertical VOR adaptation in healthy control subjects. METHODS: We measured the horizontal and vertical active (self-generated) and passive (imposed) head impulse VOR gains (eye velocity/head velocity) before and after 15 minutes of unidirectional downward IVA training. IVA training consisted of two sessions, one using a single-dot one-dimensional (1D) target, the other a grid-of-dots 2D target. RESULTS: The downward head impulse VOR gain significantly increased because of training by 13.3%, whereas the upward VOR gain did not change. The addition of extraretinal (2D) feedback did not result in greater adaptation, i.e., 1D and 2D gain increases were 15.5% and 10.6%, respectively. The vertical VOR gain increase resulted in a 3.2% decrease in horizontal VOR gain. CONCLUSION: This preliminary study is the first to show that physiologically relevant (high frequency) unidirectional increases in vertical VOR gain are possible with just 15 minutes of training. This study sets the basis for future clinical trials examining vertical IVA training in patients, which may provide the first practical rehabilitation treatment to functionally improve the vertical VOR.

Comparison of Incremental Vestibulo-ocular Reflex Adaptation Training Versus x1 Training in Patients With Chronic Peripheral Vestibular Hypofunction: A Two-Year Randomized Controlled Trial.

BACKGROUND AND PURPOSE: A crossover, double-blinded randomized controlled trial to investigate once-daily incremental vestibulo-ocular reflex (VOR) adaptation (IVA) training over 2 years in people with stable and chronic peripheral vestibular hypofunction. METHODS: Twenty-one patients with peripheral vestibular hypofunction were randomly assigned to intervention-then-control (n = 12) or control-then-intervention (n = 9) groups. The task consisted of either x1 (control) or IVA training, once daily every day for 15 minutes over 6-months, followed by a 6-month washout, then repeated for arm 2 of the crossover. Primary outcome: vestibulo-ocular reflex gain. Secondary outcomes: compensatory saccades, dynamic visual acuity, static balance, gait, and subjective symptoms. Multiple imputation was used for missing data. Between-group differences were analyzed using a linear mixed model with repeated measures. RESULTS: On average patients trained once daily 4 days per week. IVA training resulted in significantly larger VOR gain increase (active: 20.6% ± 12.08%, P = 0.006; passive: 30.6% ± 25.45%, P = 0.016) compared with x1 training (active: -2.4% ± 12.88%, P = 0.99; passive: -0.6% ± 15.31%, P = 0.68) (P < 0.001). The increased IVA gain did not significantly reduce with approximately 27% persisting over the washout period. x1 training resulted in greater reduction of compensatory saccade latency (P = 0.04) and increase in amplitude (P = 0.02) compared with IVA training. There was no difference between groups in gait and balance measures; however, only the IVA group had improved total Dizziness Handicap Inventory (P = 0.006). DISCUSSION AND CONCLUSIONS: Our results suggest IVA improves VOR gain and reduces perception of disability more than conventional x1 training. We suggest at least 4 weeks of once-daily 4 days-per-week IVA training should be part of a comprehensive vestibular rehabilitation program.Video Abstract available for more insights from the authors (see the Video, Supplemental Digital Content 1, available at: http://links.lww.com/JNPT/A356).

Once-Daily Incremental Vestibular-Ocular Reflex Adaptation Training in Patients With Chronic Peripheral Vestibular Hypofunction: A 1-Week Randomized Controlled Study.

BACKGROUND AND PURPOSE: This was a double-blinded randomized controlled study to investigate the effects of once-daily incremental vestibulo-ocular reflex (VOR) training over 1 week in people with chronic peripheral vestibular hypofunction. METHODS: A total of 24 patients with peripheral vestibular hypofunction were randomly assigned to intervention (n = 13) or control (n = 11) groups. Training consisted of either x1 (control) or incremental VOR adaptation exercises, delivered once daily for 15 minutes over 4 days in 1 week. Primary outcome: VOR gain with video-oculography. Secondary outcomes: Compensatory saccades measured using scleral search coils, dynamic visual acuity, static balance, gait, and subjective symptoms. Between-group differences were analyzed with a linear mixed-model with repeated measures. RESULTS: There was a difference in the VOR gain increase between groups (P < 0.05). The incremental training group gain increased during active (13.4% ± 16.3%) and passive (12.1% ± 19.9%) head impulse testing (P < 0.02), whereas it did not for the control group (P = 0.59). The control group had reduced compensatory saccade latency (P < 0.02). Both groups had similarly improved dynamic visual acuity scores (P < 0.05). Both groups had improved dynamic gait index scores (P < 0.002); however, only the incremental group had improved scores for the 2 walks involving head oscillations at approximately 2 Hz (horizontal: P < 0.05; vertical: P < 0.02), increased gait speed (P < 0.02), and step length (P < 0.01) during normal gait, and improved total Dizziness Handicap Inventory (P < 0.05). CONCLUSIONS: Our results suggest incremental VOR adaptation significantly improves gain, gait with head rotation, balance during gait, and symptoms in patients with chronic peripheral vestibular hypofunction more so than conventional x1 gaze-stabilizing exercises.Video Abstract available for more insights from the authors (see the Video, Supplemental Digital Content 1, available at: http://links.lww.com/JNPT/A336).

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 0.5-2 Hz over 20 min. 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 5-8 ms 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 0.2 Hz. 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.

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.

Improved Oculomotor Physiology and Behavior After Unilateral Incremental Adaptation Training in a Person With Chronic Vestibular Hypofunction: A Case Report.

BACKGROUND AND PURPOSE: Traditional vestibular rehabilitation therapies are effective in reducing vestibular hypofunction symptoms, but changes to the vestibulo-ocular reflex (VOR) are minimal. This controlled case report describes an increase in VOR after 6 months of incremental VOR adaptation (IVA) training in a person with chronic unilateral vestibular hypofunction. CASE DESCRIPTION: The participant was a 58-year-old female with a confirmed (Neurologist P.D.C.) left vestibular lesion stable for 2 years prior to entering a clinical trial examining the effects of daily IVA training. She was evaluated monthly for self-reported symptoms (dizziness handicap inventory), VOR function (video head impulse test), and VOR behavior (Dynamic Visual Acuity test). Intervention consisted of 6 months of 15 minutes per day unassisted training using the IVA training regime with a device developed in our laboratory. The take-home device enables the VOR response to gradually normalize on the ipsilesional side via visual-vestibular mismatch training. The intervention was followed by a 6-month wash-out and 3-month control period. The control condition used the same training device set to function like standard VOR training indistinguishable to the participant. OUTCOMES: After the intervention, ipsilesional VOR function improved substantially. The VOR adapted both via a 52% increase in slow-phase response and via 43% earlier onset compensatory saccades for passive head movements. In addition, the participant reported fewer symptoms and increased participation in sports and daily activities. DISCUSSION: Here, a participant with chronic vestibular hypofunction showing improved oculomotor performance atypical for traditional vestibular rehabilitation therapies, subsequent to using the newly developed IVA technique, is presented. It is the first time to our knowledge an improvement of this magnitude has been demonstrated as well as sustained over an extended period of time.