Insight into postural control in unilateral sensorineural hearing loss and vestibular hypofunction

This pilot study aimed to identify postural strategies in response to sensory perturbations (visual, auditory, somatosensory) in adults with and without sensory loss. We tested people with unilateral peripheral vestibular hypofunction (N = 12, mean age 62 range 23–78), or with Unilateral Sensorineural Hearing Loss (USNHL, N = 9, 48, 22–82), or healthy controls (N = 21, 52, 28–80). Postural sway and head kinematics parameters (Directional Path in the anterior-posterior and medio-lateral directions (sway & head); pitch, yaw and roll (head) were analyzed in response to 2 levels of auditory (none, rhythmic sounds via headphones), visual (static, dynamic) and somatosensory cues (floor, foam) within a simulated, virtual 3-wall display of stars. We found no differences with the rhythmic auditory cues. The effect of foam was magnified in the vestibular group compared with controls for anterior-posterior and medio-lateral postural sway, and all head direction except for medio-lateral. The vestibular group had significantly larger anterior-posterior and medio-lateral postural sway and head movement on the static scene compared with controls. Differences in pitch, yaw and roll emerged between vestibular and controls only with sensory perturbations. The USNHL group did not increase their postural sway and head movement with the increased visual load as much as controls did, particularly when standing on the foam. They did not increase their medio-lateral sway with the foam as much as controls did. These findings suggest that individuals with USNHL employ a compensatory strategy of conscious control of balance, the functional implications of which need to be tested in future research.

Introduction horizontal canal paresis > 25% if caloric testing was available [28]. USNHL was defined as normal hearing (<26 dB 4 frequency (0.5, 1, 2 and 4 kHz) pure tone average) in one ear and at least moderate (> 41 dB 4 frequency PTA) SNHL in the affected ear [29]. Control participants were recruited from the community. All participants were screened for normal or corrected to normal vision, normal protective sensation at the bottom of their feet and reported no neurological conditions. No participants used a cane or walker. Control participants self-reported normal hearing and no vestibular symptoms. No participants in this study wore any kind of amplification, including traditional hearing aids, CROS (contralateral routing of signals) or Bi-CROS aids. Participants in the USNHL were excluded for mixed or conductive hearing loss.

Testing protocol
Postural sway and head kinematics parameters were analyzed in response to 2 levels of auditory, visual and somatosensory cues within a virtual stars scene as detailed in Table 1. The visual protocol is well-established [26,27] and we added an auditory layer of a rhythmic sound to match the oscillating visual perturbations (see S1 Video) in a district frequency, both comfortable frequencies for human standing postural control (0.2 or 0.3 Hz) [30,31].
This study was approved by the Institutional Review Board of the Icahn School of Medicine at Mount Sinai (#STUDY-18-00431) and New York University Committee on Activities Involving Research Subjects (#IRB-FY2016-155). The individual in this manuscript has given written informed consent (as outlined in PLOS consent form) to publish these case details ( Fig  1). All participants first signed a written informed consent. Then their vision was screened using the standard EDTRS chart in ambient room light. The acceptable standard for driving as our measure for adequate vision was applied at a visual acuity of 20/60. Participants could wear glasses for testing, so long as they were worn for the postural assessment as well. Normal protective sensation at the bottom of the feet was confirmed by the ability to perceive a 5.07 (10 gram) monofilament [32]. The participant's height and forehead length were measured to ensure that the visual scene would be projected at their eye height. Participants completed the Simulator Sickness Questionnaire [33] at baseline, during breaks and at the end of the session. This 16-item scale asks participants to rate symptoms such as dizziness, blurred vision or fatigue on a scale of 0 (none) to 3 (severe). For the virtual reality (VR) protocol, participants stood hip-width apart on a stable force-platform (Kistler 5233A, Winterthur, Switzerland) wearing the Vive Pro Eye headset (HTC Corporation, Taoyuan City, Taiwan). Participants were asked to look straight ahead and do whatever felt natural to them to maintain their balance. There were 4 possible combinations of visuals / sounds: static visual / no sound; static visual / rhythmic white noise; moving visuals / no sound; moving visuals/ rhythmic white noise. Each trial lasted 60 seconds and was repeated 3 times on each surface for a total of 24 conditions: 12 standing directly on the stable force-platform embedded in the floor and 12 standing on Airex memory foam placed on top of the force-platform. The order of the conditions was randomized per block meaning that the same randomized order was performed on floor or foam (Table 1 and S1 Video). For safety reasons, the floor block was always presented first. Participants were guarded by either a licensed or student physical therapist. Two quad

PLOS ONE
Sensory loss: Postural responses canes were placed on either side of the force-platform for safety and to help with stepping on and off the force-platform, particularly with the foam (See Fig 1). A rest break was provided after 12 trials but offered as needed. During the break, participants completed several questionnaires: The Dizziness Handicap Inventory (DHI) [34,35]; The Activities-Specific Balance Confidence (ABC) [35]; and the Speech, Spatial and Quality of Hearing 12-item Scale [SSQ12] [36]. The SSQ12 was only administered to those in the USNHL group (see Table 2).  [34] and the remaining 7 participants reported 0.
The DHI was designed to identify difficulties that a patient may be experiencing because of their dizziness. The ABC scale is a subjective measure of confidence in performing various ambulatory activities without falling or feeling 'unsteady'. The SSQ12 is valid and provides insight into the day-to-day impact of hearing loss. https://doi.org/10.1371/journal.pone.0276251.t002

System
Visuals were implemented in C# language using standard Unity Engine version 2019.4.16f1 (64-bit) (©Unity Technologies, San Francisco, CA, USA). The scenes (visuals and sounds) were delivered via an HTC Vive Pro Eye headset (HTC Corporation, Taoyuan City, Taiwan) controlled by a Dell Alienware laptop 15 R3 (Round Rock, TX, USA). The participants observed a display of randomly distributed white spheres (diameter 0.02 meters [m]) on a black background. The display is viewed as 1.63 m away from the participant and appears to have a room arrangement with one front and two side walls, each 6.16 m by 3.2 m. A clear central area of occlusion of 0.46 m in diameter was created to suppress the visibility of "sampling artifacts" or aliasing effects, which are most likely to occur in the foveal region [37]. Height was calibrated using Steam VR standing paradigm setup.
To generate the auditory cues, we used Matlab to develop white noise in an envelope generator. We then modulated the sonic amplitude cycle from quieter to louder at 0.3 Hz. The intensity was defined as the difference between the lowest and loudest part of the oscillation. The sounds mimicked a wave where the mid-point of the cycle has the loudest point. In order to render the white noise in the Unity scenes to join the visuals, the generated audio files were further processed with Wwise which was integrated into Unity. Sounds were presented binaurally between 65-71 dB at the highest level that was comfortable to the participant. The sound level in the testing environment (for the 'no sound' scene) was measured to be between 42 dB (no air-conditioning on) to 55 dB (both ACs on). Nine participants chose 90% (67 to 70 dB): 1 USNHL, 4 controls, 4 vestibular. Five participants chose 100% (69 to 71 dB): 3 controls, 2 vestibular. All other participants listened to the sounds at 80% intensity (65 to 68 dB).

Data reduction and outcome measures
Postural sway was recorded at 100 Hz by Qualisys software. Head kinematics at 90 Hz was recorded by custom-made software written for the HTC Vive headset [38]. The last 55 seconds (of the total 60 seconds) were used for analysis. Data processed and analyzed in Matlab R2021a (Mathworks, Natick, MA). We applied a low-pass 4 th order Butterworth filter with a conservative cutoff frequency at 10 Hz [30]. Directional Path (DP) is a valid and reliable measure of postural steadiness and is used as an indication of how much static balance is perturbed with a sensory manipulation [39]. DP [40] was calculated as the total path length of the position curve in the medio-lateral and anterior-posterior directions for center-of-pressure data (cm) and in medio-lateral, anterior-posterior (cm) and pitch, yaw, and roll (radians) for the head data. Test-retest reliability of postural sway DP within a similar protocol without the sounds has been previously demonstrated [41]. Criterion validity of the HTC Vive to detect head kinematics in postural tasks in a comparable way to a Qualisys motion capture system has been demonstrated as well [38]. Head kinematics has been shown to be more sensitive to vestibular hypofunction than postural sway metrics [42].

Data analysis
We ran descriptive statistics, plots and inspection of model assumptions for all outcome and descriptive measures. We conducted a visual inspection of the data to determine whether the distributions differed by sensory perturbations and observed no difference between sound conditions. To confirm this observation, we fit two linear mixed effects models for each outcome. The first included a 4-way interaction of sound by surface, visual and group. The second included only the 3-way interaction surface by visual by group. We then compared the AIC values between these models for each outcome. In all cases, AIC was lower for the model that did not include sound (See S1 Table). Therefore, sound was not included as a variable in any of the other models. In addition, an initial inspection of the residuals from the linear mixed effects models indicated heteroskedasticity. Therefore, we log-transformed all DP data in the final models to ameliorate this issue. Following transformation all model assumptions were met.
For each of the measures of interest (DP center-of-pressure: anterior-posterior, medio-lateral. DP Head: anterior-posterior, medio-lateral, pitch, yaw, roll) we fit a linear mixed effects model. Each model included the main effects of group, visual condition, and surface condition, and their two-and three-way interactions. Group comparisons were conducted for the vestibular group vs. controls and USNHL group vs. controls. This model maximizes the information we can obtain from the data by accounting for the inherent multi-level study design (person, conditions, repetitions). That is, since each person completes various trials for each condition, the linear mixed effects model accounts for these sources of variability [43]. P-values for the fixed effects were calculated through the Satterthwaite approximation for the degrees of freedom for the T-distribution [44].
We report the P value derived from the logarithmic model and difference in means (DIM) as well as 95% confidence intervals per condition, per group in the units of measurement through the calculation of the estimated marginal means. The DIM provides an indication of the magnitude of the difference both between and within groups and conditions. We investigate 3 types of DIMs: within-group (e.g., for controls the DIMs indicate differences within the group across conditions); between-group (e.g., for the vestibular or USNHL group the comparison to controls on the static visual/floor condition); and DIMs that represent the interaction terms-meaning how much the differences due to conditions (visual, surface) differ between groups.

Sample
For a detailed description of the sample and results of the Simulator Sickness Questionnaire see Tables 2 and 3. The sample included 21 healthy controls, 12 participants with unilateral vestibular hypofunction and 9 individuals with USNHL. All participants in the control group reported no hearing impairment and no vestibular symptoms (all scored 0 on the DHI, average ABC 97%., Table 2) but it was not formally tested. All participants in the USNHL group reported no vestibular complaints (average 5 on the DHI vs. 43 for the vestibular group and 96% ABC vs. 66% for the vestibular group, Table 2) but was not submitted to vestibular tests. Two patients with vestibular hypofunction were not able to stand on foam without support hence only completed the floor segment of the protocol. All other participants completed all trials.

Center-of-pressure (COP) (see Figs 2 and 3 and S2 Table)
With the addition on the foam to a static visual scene, controls significantly increased their medio-lateral sway (DIM = 38. The vestibular group had significantly greater postural sway than the controls for the static visual scene on the floor: medio-lateral (between-group DIM = 9.7cm, P = 0.005); anterior-posterior (between-group DIM = 13.5cm, P = 0.03). The effect of foam, but not of visual load, was magnified in the vestibular group compared to controls. The vestibular group increased on average by 60.8 cm with the foam vs. floor which is 22 cm more than the control group increased (medio-lateral, P = 0.03 for group by surface interaction); and by 92 cm which is on average 46.6 cm more than controls did (anterior-posterior, P<0.001).
The USNHL group did not differ from the controls for the static scene on the floor. For medio-lateral sway, the effect of foam was different between the USNHL and controls (interaction P = 0.003). With the addition of foam, the USNHL group increased on average by 34 cm which is 4.8 cm less than controls did. For anterior-posterior sway, the effect of visual load was different between the USNHL and controls (P = 0.005 for interaction USNHL by visual on foam). With dynamic visuals, the USNHL group increased on average by 26.8 cm on foam which is 17 cm less than the change in controls. See Fig 3 for individual changes with the visual load when participants are standing on foam.

Head (see Figs 2 and 4 and S2 Table)
With the addition of foam to a static visual scene, the controls significantly  for visuals on foam = 21.1cm, 15.5 cm greater change than on floor, interaction visual by surface P<0.001; pitch DIM = 0.14 rad, 0.11 rad greater change than on floor, interaction visual by surface P = 0.003 respectively). The effect of increased visual load was significant only when  Head movement of the USNHL group did not differ from controls on the static scene on the floor. Neither did USNHL differ from the controls in pitch, yaw or roll on any condition. For medio-lateral and anterior-posterior head movements, the effect of visual load was different between the USNHL and controls when standing on foam. The USNHL group increased their medio-lateral head movements on average by 0.2 cm which is 22.2 cm less than the change with visuals on foam in controls (interaction P = 0.04). The USNHL group increased their anterior-posterior head movements on average by 16.3 cm which is 4.8 cm less than the change with visuals on foam in controls (interaction P = 0.03).

Discussion
Prior studies of sensory integration have demonstrated that when healthy individuals perform balance tasks in complex sensory environments, they respond to sensory perturbations (e.g., moving visual environments) with increased postural sway [18][19][20]. Postural control of participants in the present study mimicked published results and provided context for postural responses in those with unilateral hearing or vestibular loss. Given that balance problems related to vestibular hypofunction are known to stem from difficulty in sensory integration [45,46], we expected the vestibular group to show more postural sway with magnified differences from the other groups in the most challenging task. Indeed, differences in postural sway between controls and participants with vestibular hypofunction were magnified as the sensory challenge increased. However, we also observed differences between the vestibular group and controls on the static/ stable scene. These differences are larger than we observed in prior studies [47] possibly because these patients were recruited prior to vestibular rehabilitation.

What did we learn about postural responses in individuals with USNHL?
While our USNHL sample was small, their postural behavior was consistent, and suggests new hypotheses for future research. The USNHL group did not increase their postural sway in the presence of visual perturbations, particularly when standing on a compliant surface. This behavior could suggest that people with USNHL overly rely on somatosensory input and not on vision, consistent with [23] that found increased somatosensory reliance in deaf individuals compared to controls [48]. observed significant gray matter volume increases in the somatosensory and motor systems as well as decreases in the auditory and visual systems in individuals with single-sided hearing loss further supporting this hypothesis It is also possible that people with USNHL have an overall reduced reaction to any perturbation to avoid loss of balance. This hypothesis is supported by the finding that participants with USNHL did not increase their medio-lateral sway as much as controls with the addition of an unstable surface. Studies of standing balance, typically consider increased postural sway as indication of poor balance. However, some increase in sway with visual and somatosensory perturbations is expected in healthy adults as part of an adaptive automatic control of standing balance [49]. Little to no change in sway with sensory perturbations is thought to be related to overly conscious movement processing or attempting to cognitively control a process otherwise considered automatic. Such behaviors have been observed in adults with phobic postural vertigo [50], healthy adults tested on an elevated platform [51], and children with autistic spectrum disorders [52]. This new hypothesis calls for further investigation of balance in people with USNHL.

Why didn't sound matter?
Recent studies suggest that healthy individuals use auditory cues for postural control [21,[53][54][55][56]. The lack of differences in sound conditions in this study should be interpreted in the context of the specific sound stimulus used and may not speak to the overall impact of auditory cues in postural control. To create the auditory stimulus for this study, we used broadband sounds, known to influence postural sway more than pure tones [9]. We designed amplitudemodulated white noise, with a non-spatialized noise source. This rhythmic sound was designed to mimic the well-established [26] visual perturbation but at a distinct, different frequency such that the sounds and visuals were not fully aligned. We expected that auditory perturbations would increase postural sway in healthy controls on the most challenging task and magnify postural sway in vestibular hypofunction in all conditions. It is possible that the cycling white noise was neither moving enough to provide a disturbance nor static enough to provide an auditory anchor. Future studies on ecologically valid sounds may be valuable to better understand how sounds are used for balance.

Limitations
The sample size is small and the results, especially the novel result regarding the USNHL group, need to be interpreted with caution and replicated in a larger study before drawing clinical conclusions. In our sample individuals with USNHL have had the condition for years whereas half of the vestibular group had symptoms for over 3 months but less than 12. This difference in chronicity should be controlled for in future studies. All participants in the control group reported no hearing impairment but it was not formally tested. While it is possible that older controls had age-related high frequency hearing loss, this study focused on significant single sided hearing loss which is highly unlikely to be undiagnosed. Also, no diagnostic vestibular testing was done on participants in the control or USNHL groups. However, neither group reported vestibular complaints, and both had comparable outcomes on standardized self-report assessment of balance (ABC) and vestibular dysfunction (DHI). Although the groups were not significantly different in age, it is still a possibility that age had some influence. We provided estimated differences between groups, but it is currently unknown what a clinically important difference is for postural sway measures.

Conclusions
This pilot study aimed to identify postural strategies in response to sensory perturbations (visual, auditory, somatosensory) in with individuals with USNHL (and no vestibular complaints), individuals with vestibular hypofunction, and age-matched controls. While rhythmic sounds did not appear to make a difference in this specific study, this may relate to the specifics of the sound paradigm tested; as many other studies suggest the importance of sounds to postural control, future studies will further explore other forms of sounds, such as ecologically valid, spatialized moving sounds. Patients with vestibular hypofunction were destabilized by the visual and surface perturbations more than healthy controls and overall had larger postural sway even on the static scene, evident in both center-of-pressure and head movement. Head movement was similar between USNHL and controls, but notably large in the vestibular group, adding to prior data suggesting a specific pattern of head kinematics that is unique to vestibular dysfunction. Future studies should examine whether these patterns change following vestibular rehabilitation and their implications to functional complaints. The USNHL group did not change with sensory perturbations, particularly visual, as much as controls did. It is possible that individuals with USNHL employed a compensatory strategy of conscious control of balance, but these findings need to be replicated in larger studies.