Andrew R. Wagner

Background: The Sensory Organization Test (SOT) was designed to measure changes in postural control in response to unreliable visual and/or proprioceptive feedback. However, secondary to the manipulation of sensory cues in only the sagittal plane, the SOT is capable of only describing postural control in a single direction. The present study aimed to characterize postural responses to a modified SOT designed to concurrently challenge both anteroposterior and mediolateral postural control.Methods: Twenty-one healthy adult volunteers (30.6 ± 10.2 years) completed the standard anteroposterior one-dimensional (1D) SOT, in addition to a modified SOT with the support surface sway-referenced to both anteroposterior and mediolateral postural sway (two-dimensional, 2D). Our primary analysis concerned a comparison of mediolateral, as well as anteroposterior postural sway measured during the standard one-dimensional (i.e., pitch tilt) and the novel two-dimensional (i.e., roll and pitch tilt) sway-referenced paradigms. Here, postural sway was quantified by calculating the root mean square distance (RMSD) of the center of pressure (CoP) during each trial.Results: Our data showed that the 2D sway-referenced conditions yielded a selective increase in mediolateral postural sway relative to the standard 1D conditions for both wide (η² = 0.66) and narrow (η² = 0.78) stance conditions, with anteroposterior postural sway being largely unaffected (η²= 0.001 to 0.103, respectively). The ratio between mediolateral postural sway in the sway-referenced conditions and postural sway in the corresponding stable support surface conditions was greater for the 2D (2.99 to 6.26 times greater) compared to 1D paradigms (1.25 to 1.84 times greater), consistent with a superior degradation of viable proprioceptive feedback in the 2D paradigm.Conclusion: A modified 2D version of the SOT was shown to provide a greater challenge to mediolateral postural control relative to the standard 1D SOT protocol, putatively as a result of a superior capacity to degrade proprioceptive feedback in the mediolateral direction. Given these positive findings, future studies should investigate the clinical utility of this modified SOT as a means by which to better characterize sensory contributions to postural control in the presence of various sensorimotor pathologies, including vestibular hypofunction.

Globally, there are nearly three million people living with multiple sclerosis (PLW-MS). Many PLW-MS experience vertigo and have signs of vestibular dysfunction, e.g., low vestibulo–ocular reflex (VOR) gains or the presence of compensatory saccades (CSs), on video head impulse testing (vHIT). We examined whether the vestibular function and compensatory oculomotor behaviors in PLW-MS differed based on the level of MS-related disability. The VOR gain, CS frequency and latency, and gaze position error (GPE) were calculated from the individual traces obtained during six-canal vHIT for 37 PLW-MS (mean age 53.4 ± 12.4 years-old, 28 females) with vertigo and/or an imbalance. The subjects were grouped by their Expanded Disability Status Scale (EDSS) scores: PLW-min-MS (EDSS = 1.0–2.5, n = 8), PLW-mild-MS (EDSS = 3.0–4.5, n = 23), and PLW-moderate-MS (EDSS = 5.0–6.0, n = 6). The between-group differences were assessed with Kruskal–Wallis tests. The VOR gains for most of the canals were higher for PLW-min-MS compared to PLW-mild- and mod-MS, respectively. CS occurred less often in PLW-min-MS versus PLW-mild- and mod-MS, respectively. No clear trend in CS latency was found. The GPE was often lower for PLW-min-MS compared to PLW-mild- and mod-MS, respectively. Thus, our data demonstrate that worse VOR and compensatory oculomotor functions are associated with a greater MS-related disability. PLW-MS may benefit from personalized vestibular physical therapy.

Compensatory saccades (CSs) are recruited by individuals with unilateral vestibular deafferentation (UVD) to compensate for an impaired vestibulo-ocular reflex (VOR). The effectiveness of CS in multiple sclerosis (MS), a central vestibular impairment, is unknown. We show that in UVD and in MS, covert CSs compensate for reduced VOR gain and minimize gaze position error (GPE), yet in >50% of individuals with MS, overt CS worsened GPE, suggesting unique roles for peripheral and central vestibular inputs.

The present study aimed to determine if a vestibular perceptual learning intervention could improve roll tilt self-motion perception and balance performance. Two intervention groups (n = 10 each) performed 1,300 trials of roll tilt at either 0.5 Hz (2 s/motion) or 0.2 Hz (5 s/motion) distributed over 5 days; each intervention group was provided feedback (correct/incorrect) after each trial. Roll tilt perceptual thresholds, measured using 0.2-, 0.5-, and 1-Hz stimuli, as well as quiet stance postural sway, were measured on day 1 and day 6 of the study. The control group (n = 10) who performed no perceptual training, showed stable 0.2-Hz (+1.48%, P > 0.99), 0.5-Hz (−4.0%, P > 0.99), and 1-Hz (−17.48%, P = 0.20) roll tilt thresholds. The 0.2-Hz training group demonstrated significant improvements in both 0.2-Hz (−23.77%, P = 0.003) and 0.5-Hz (−22.2%, P = 0.03) thresholds. The 0.5-Hz training group showed a significant improvement in 0.2-Hz thresholds (−19.13%, P = 0.029), but not 0.5-Hz thresholds (−17.68%, P = 0.052). Neither training group improved significantly at the untrained 1-Hz frequency (P > 0.05). In addition to improvements in perceptual precision, the 0.5-Hz training group showed a decrease in sway when measured during “eyes open, on foam” (d_z = 0.57, P = 0.032) and “eyes closed, on foam” (d_z = 2.05, P < 0.001) quiet stance balance tasks. These initial data suggest that roll tilt perception can be improved with less than 5 h of training and that vestibular perceptual training may contribute to a reduction in subclinical postural instability. NEW & NOTEWORTHY Roll tilt vestibular perceptual thresholds, an assay of vestibular noise, were recently found to correlate with postural sway. We therefore hypothesized that roll tilt perceptual training would yield improvements in both perceptual precision and balance. Our data show that roll tilt perceptual thresholds and quiet stance postural sway can be significantly improved after less than 5 h of roll tilt perceptual training, supporting the hypothesis that vestibular noise contributes to increased postural sway.

In an effort to characterize the factors influencing the perception of self-motion rotational cues, vestibular self-motion perceptual thresholds were measured in 14 subjects for rotations in the roll and pitch planes, as well as in the planes aligned with the anatomic orientation of the vertical semicircular canals (i.e., left anterior, right posterior; LARP, and right anterior, left posterior; RALP). To determine the multisensory influence of concurrent otolith cues, within each plane of motion, thresholds were measured at four discrete frequencies for rotations about earth-horizontal (i.e., tilts; EH) and earth-vertical axes (i.e., head positioned in the plane of the rotation; EV). We found that the perception of rotations, stimulating primarily the vertical canals, was consistent with the behavior of a high-pass filter for all planes of motion, with velocity thresholds increasing at lower frequencies of rotation. In contrast, tilt (i.e, EH rotation) velocity thresholds, stimulating both the canals and otoliths (i.e., multisensory integration), decreased at lower frequencies and were significantly lower than earth-vertical rotation thresholds at each frequency below 2 Hz. These data suggest that multisensory integration of otolithic gravity cues with semicircular canal rotation cues enhances perceptual precision for tilt motions at frequencies below 2 Hz. We also showed that rotation thresholds, at least partially, were dependent on the orientation of the rotation plane relative to the anatomical alignment of the vertical canals. Collectively these data provide the first comprehensive report of how frequency and axis of rotation influence perception of rotational self-motion cues stimulating the vertical canals.

Roll tilt vestibular perceptual thresholds, an assay of vestibular noise, have recently been shown to be associated with suboptimal balance performance in healthy older adults. However, despite the strength of this correlation, the use of a categorical (i.e., pass/fail) balance assessment limits insight into the impacts of vestibular noise on postural sway. As a result, an explanation for this correlation has yet to be determined. We hypothesized that the correlation between roll tilt vestibular thresholds and postural control reflects a shared influence of sensory noise. To address this hypothesis, we measured roll tilt perceptual thresholds at multiple frequencies (0.2 Hz, 0.5 Hz, 1 Hz) and compared each threshold to quantitative measures of quiet stance postural control in 33 healthy young adults (mean = 24.9 years, SD = 3.67). Our data showed a significant linear association between 0.5 Hz roll tilt thresholds and the root mean square distance (RMSD) of the center of pressure in the mediolateral (ML; β = 5.31, p = 0.002, 95% CI = 2.1–8.5) but not anteroposterior (AP; β = 5.13, p = 0.016, 95% CI = 1.03–9.23) direction (Bonferroni corrected α of 0.006). In contrast, vestibular thresholds measured at 0.2 Hz and 1 Hz did not show a significant correlation with ML or AP RMSD. In a multivariable regression model, controlling for both 0.2 Hz and 1 Hz thresholds, the significant effect of 0.5 Hz roll tilt thresholds persisted (β = 5.44, p = 0.029, CI = 0.60–10.28), suggesting that the effect cannot be explained by elements shared by vestibular thresholds measured at the three frequencies. These data suggest that vestibular noise is significantly associated with the temporospatial control of quiet stance in the mediolateral plane when visual and proprioceptive cues are degraded (i.e., eyes closed, standing on foam). Furthermore, the selective association of quiet-stance sway with 0.5 Hz roll tilt thresholds, but not thresholds measured at lower (0.2 Hz) or higher (1.0 Hz) frequencies, may reflect the influence of noise that results from the temporal integration of noisy canal and otolith cues.

Falls are the leading causes of accidental injury in older adults and directly contribute to more than 600,000 deaths each year worldwide. Although the issue of falls is complex, balance dysfunction is one the principal contributors to the heightened incidence of falls in older adults. A nationally representative survey of older adults in the United States showed that an inability to stand on a foam pad with the eyes closed was associated with more than a six-fold increase in the odds of reporting "difficulty with falls." As stability in the "eyes closed, on foam" condition is reliant upon intact vestibular cues, these data implicate age-related vestibular loss as a potential contributor to falls, yet, the specific causal mechanism explaining the link between age-related vestibular loss and imbalance/falls was not known. Here we review recent data showing that, vestibular perceptual thresholds, an assay of vestibular sensory noise, were found to, (1) account for nearly half of subclinical balance impairment in healthy older adults and (2) correlate with postural sway in healthy young adults. Based upon the identified links between balance dysfunction and vestibular noise in healthy adults, we posit the following causal chain: (a) increased "noise" in vestibular feedback - yielding a reduced signal-to-noise ratio in vestibular feedback-increases sway, (b) excessive sway leads to imbalance, and (c) imbalance contributes to falls. Identifying the "cause" of age-related balance dysfunction will inform the development of interventions tailored to prevent falls, and fall-related injuries, in the growing population of older adults.

Aging is associated with progressive declines in both the vestibular and human balance systems. While vestibular lesions certainly contribute to imbalance, the specific contributions of age-related vestibular declines to age-related balance impairment is poorly understood. This gap in knowledge results from the absence of a standardized method for measuring age-related changes to the vestibular balance pathways. The purpose of this manuscript is to provide an overview of the existing body of literature as it pertains to the methods currently used to infer vestibular contributions to age-related imbalance.

The study objective was to understand how the contralesional labyrinth contributes to gaze and gait stability after unilateral vestibular deafferentation (UVD). Head impulse testing (vHIT) was completed in 37 individuals [22 women (59%); age 52.13 ± 11.59 yr, mean ± SD] with UVD from vestibular schwannoma resection. Compensatory saccades (CS) and vestibulo-ocular reflex (VOR) gain were analyzed for both ipsilesional and contralesional impulses. Gait speed (10-m walk test) and endurance (2-min walk test) were collected for 35 individuals. CS were recruited during contralesional head rotation regardless of VOR gain on either the ipsilesional [ρ = 0.21 (−0.14, 0.57); Spearman rank (95% confidence interval)] or contralesional side [ρ = −0.04 (−0.42, 0.35)]. Additionally, the latency of these CS (151.19 ± 52.41 ms) was similar to that of CS generated during ipsilesional rotation (165.65 ± 21.62 ms; P = 0.159). CS recruited during ipsilesional vHIT were of a higher velocity ( P < 0.001) and greater frequency ( P < 0.001) compared with contralesional CS. VOR gain asymmetry was significantly correlated with gait speed [ρ = −0.37 (−0.73, −0.01)], yet individual VOR gain was not correlated [ipsilesional: ρ = 0.17 (−0.20, 0.55); contralesional: ρ = −0.18 (−0.52, 0.15)]. Our data reveal CS are recruited at similar latencies without correlation to VOR gain or direction of head rotation, and that the central integration of ipsilesional and contralesional vestibular afference correlates with gait. Together, our data suggest the brain considers vestibular afference from both sides when generating related behavioral output after UVD. NEW & NOTEWORTHY After unilateral vestibular deafferentation, compensatory saccades (CS) have similar latencies regardless of the direction of head rotation, and those CS generated during contralesional head rotation are unrelated to extent of vestibular loss. Additionally, the extent of asymmetry in residual vestibular function, not the extent of vestibular loss, correlates with gait speed. Our data suggest a common mechanism is responsible for the generation of CS and restoration of gait speed in vestibular compensation.