Effects of the BalanCI on Working Memory and Balance in Children and Young Adults With Cochleovestibular Dysfunction.

OBJECTIVES: This study aimed to: (1) determine the interaction between cognitive load and balance in children and young adults with bilateral cochleovestibular dysfunction who use bilateral cochlear implants (CIs) and (2) determine the effect of an auditory balance prosthesis (the BalanCI) on this interaction. Many (20 to 70%) children with sensorineural hearing loss experience some degree of vestibular loss, leading to poorer balance. Poor balance could have effects on cognitive resource allocation which might be alleviated by the BalanCI as it translates head-referenced cues into electrical pulses delivered through the CI. It is hypothesized that children and young adults with cochleovestibular dysfunction will demonstrate greater dual-task costs than typically-developing children during dual balance-cognition tasks, and that BalanCI use will improve performance on these tasks. DESIGN: Study participants were 15 typically-developing children (control group: mean age ± SD = 13.6 ± 2.75 years, 6 females) and 10 children and young adults who use bilateral CIs and have vestibular dysfunction (CI-V group: mean age ± SD=20.6 ± 5.36 years, 7 females). Participants completed two working memory tasks (backward auditory verbal digit span task and backward visuospatial dot matrix task) during three balance conditions: seated, standing in tandem stance with the BalanCI off, and standing in tandem stance with the BalanCI on. Working memory performance was quantified as total number of correct trials achieved. Postural stability was quantified as translational and rotational path length of motion capture markers worn on the head, upper body, pelvis, and feet, normalized by trial time. RESULTS: Relative to the control group, children and young adults in the CI-V group exhibited poorer overall working memory across all balance conditions ( p = 0.03), poorer translational postural stability (larger translational path length) during both verbal and visuospatial working memory tasks ( p < 0.001), and poorer rotational stability (larger rotational path length) during the verbal working memory task ( p = 0.026). The CI-V group also exhibited poorer translational ( p = 0.004) and rotational ( p < 0.001) postural stability during the backward verbal digit span task than backward visuospatial dot matrix task; BalanCI use reduced this stability difference between verbal and visuospatial working memory tasks for translational stability overall ( p > 0.9), as well as for rotational stability during the maximum working memory span (highest load) participants achieved in each task ( p = 0.91). CONCLUSIONS: Balance and working memory were impaired in the CI-V group compared with the control group. The BalanCI offered subtle improvements in stability in the CI-V group during a backward verbal working memory task, without producing a negative effect on working memory outcomes. This study supports the feasibility of the BalanCI as a balance prosthesis for individuals with cochleovestibular impairments.

Evaluating the use of a balance prosthesis during balance perturbations in children and young adults with cochleovestibular dysfunction.

Study objectives were to: (1) quantify stability in children and young adults using cochlear implants with concurrent cochleovestibular dysfunction (CI-V) during balance perturbations and (2) to assess effects of an auditory head-referencing device (BalanCI) on their stability. The BalanCI provides auditory feedback via cochlear implants to cue posture and potentially avoid falling in children with CI-V. It was hypothesized that children and young adults with CI-V respond with larger movements to floor perturbations than typically-developing peers (controls) and that BalanCI use decreases these movements. Motion in response to treadmill perturbations was captured by markers on the head, torso, and feet in eight CI-V and 15 control participants. Stability (area under the curve of motion displacement) and peak displacement latencies were measured. The CI-V group demonstrated less stability and slower responses than the control group during medium and large backwards perturbations (p's < 0.01). In the CI-V group, BalanCI use improved stability during large backwards perturbations (p < 0.001), but worsened stability during large sideways perturbations (p's < 0.001). Children and young adults with CI-V move more to remain upright during perturbations than typically-developing peers. The BalanCI has potential to aid physical/vestibular therapy in children with CIs who have poor balance.

Exposure to Spoken Communication in Children With Cochlear Implants During the COVID-19 Lockdown.

Importance: The coronavirus disease 2019 (COVID-19) lockdowns in Ontario, Canada in the spring of 2020 created unprecedented changes in the lives of all children, including children with hearing loss. Objective: To quantify how these lockdowns changed the spoken communication environments of children with cochlear implants by comparing the sounds they were exposed to before the Ontario provincial state of emergency in March 2020 and during the resulting closures of schools and nonessential businesses. Design, Setting, and Participants: This experimental cohort study comprised children with hearing loss who used cochlear implants to hear. These children were chosen because (1) their devices monitor and catalog levels and types of sounds during hourly use per day (datalogs), and (2) this group is particularly vulnerable to reduced sound exposure. Children were recruited from the Cochlear Implant Program at a tertiary pediatric hospital in Ontario, Canada. Children whose cochlear implant datalogs were captured between February 1 and March 16, 2020, shortly before lockdown (pre-COVID-19), were identified. Repeated measures were collected in 45 children during initial easing of lockdown restrictions (stages 1-2 of the provincial recovery plan); resulting datalogs encompassed the lockdown period (peri-COVID-19). Main Outcomes and Measures: Hours of sound captured by the Cochlear Nucleus datalogging system (Cochlear Corporation) in 6 categories of input levels (<40, 40-49, 50-59, 60-69, 70-79, ≥80 A-weighted dB sound pressure levels [dBA]) and 6 auditory scene categories (quiet, speech, speech-in-noise, music, noise, and other). Mixed-model regression analyses revealed main effects with post hoc adjustment of confidence intervals using the Satterthwaite method. Results: A total of 45 children (mean [SD] age, 7.7 [5.0] years; 23 girls [51.1%]) participated in this cohort study. Results showed similar daily use of cochlear implants during the pre- and peri-COVID-19 periods (9.80 mean hours pre-COVID-19 and 9.34 mean hours peri-COVID-19). Despite consistent device use, these children experienced significant quieting of input sound levels peri-COVID-19 by 0.49 hour (95% CI, 0.21-0.80 hour) at 60 to 69 dBA and 1.70 hours (95% CI, 1.42-1.99 hours) at 70 to 79 dBA with clear reductions in speech exposure by 0.98 hour (95% CI, 0.49-1.47 hours). This outcome translated into a reduction of speech:quiet from 1.6:1.0 pre-COVID-19 to 0.9:1.0 during lockdowns. The greatest reductions in percentage of daily speech occurred in school-aged children (elementary, 12.32% [95% CI, 7.15%-17.49%]; middle school, 11.76% [95% CI, 5.00%-18.52%]; and high school, 9.60% [95% CI, 3.27%-15.93%]). Increased daily percentage of quiet (7.00% [95% CI, 4.27%-9.74%]) was most prevalent for children who had fewer numbers of people in their household (estimate [SE] = -1.12% [0.50%] per person; Cohen f = 0.31). Conclusions and Relevance: The findings of this cohort study indicate a clear association of COVID-19 lockdowns with a reduction in children's access to spoken communication.

Investigation of light-induced lacrimation and pupillary responses in episodic migraine.

The purpose of this pilot study was to investigate the light-induced pupillary and lacrimation responses mediated by intrinsically photosensitive retinal ganglion cells (ipRGCs) in migraine. Ten participants with episodic migraine and normal tear production, as well as eleven visually normal controls participated in this study. Following an initial baseline trial (no light flash), participants received seven incremental and alternating red and blue light flashes. Pupillometry recording of the left eye and a 1-min anesthetized Schirmer's test of the right eye (using 0.5% proparacaine) were performed simultaneously. Intrinsic and extrinsic ipRGC photoactivities did not differ between migraine participants and controls across all intensities and wavelengths. Migraine participants, however, had significantly lower lacrimation than controls following the highest blue intensity. A positive correlation was found between melanopsin-driven post-illumination pupillary responses and lacrimation following blue stimulation in both groups. Our results show that participants with self-reported photophobia have normal ipRGC-driven responses, suggesting that photophobia and pupillary function may be mediated by distinct ipRGC circuits. The positive correlation between melanopsin-driven pupillary responses and light-induced lacrimation suggests the afferent arm of the light-induced lacrimation reflex is melanopsin-mediated and functions normally in migraine. Lastly, the reduced melanopsin-mediated lacrimation at the highest stimulus suggests the efferent arm of the lacrimation reflex is attenuated under certain conditions, which may be a harbinger of dry eye in migraine.

Binocular Summation in Postillumination Pupil Response Driven by Melanopsin-Containing Retinal Ganglion Cells.

Purpose: To investigate how melanopsin-mediated intrinsically photosensitive retinal ganglion cell (ipRGC) signals are integrated binocularly using chromatic pupillometry. We hypothesized that if the melanopsin system is summative, there will be a greater postillumination pupillary response (PIPR) under binocular conditions after viewing bright blue light. Methods: Pupillary responses in 10 visually normal participants were recorded with an eye tracker following full-field stimulation of red (long wavelength) and blue (short wavelength) light of equal intensity (dim: 0.1 cd [candela]/m2, bright: 60 cd/m2) and duration (400 ms). Individual monocular (left eye) pupil responses were measured first, followed by binocular responses. Each participant repeated the same protocol on 3 separate days, at similar times of day. PIPR was recorded for bright red and blue conditions only, whereas maximum pupillary constriction (MPC) was measured under both bright and dim conditions during red and blue light stimulation. Results: Bright blue light stimulation induced greater PIPR under binocular than monocular viewing conditions (F(1,9) = 79.52, P < 0.001). Bright red light stimulation induced minimal PIPR and showed no significant difference between viewing conditions post Bonferroni correction (F(1,9) = 5.49, P = 0.04). MPC was greater during binocular than monocular viewing conditions for all light stimuli, but was greatest following blue compared to red light stimulation. Conclusions: A larger PIPR was induced using a binocular than a monocular full-field stimulus of equal intensity and duration, demonstrating that melanopsin-mediated ipRGC signals are summated binocularly. This study expands our current understanding of the melanopsin system and may be used as an additional marker to stratify diseases according to their etiologies.

A Novel Visual Psychometric Test for Light-Induced Discomfort Using Red and Blue Light Stimuli Under Binocular and Monocular Viewing Conditions.

Purpose: To develop an objective psychophysical method to quantify light-induced visual discomfort, and to measure the effects of viewing condition and stimulus wavelength. Methods: Eleven visually normal subjects participated in the study. Their pupils were dilated (2.5% phenylephrine) before the experiment. A Ganzfeld system presented either red (1.5, 19.1, 38.2, 57.3, 76.3, 152.7, 305.3 cd/m2) or blue (1.4, 7.1, 14.3, 28.6, 42.9, 57.1, 71.4 cd/m2) randomized light intensities (1 s each) in four blocks. Constant white-light stimuli (3 cd/m2, 4 s duration) were interleaved with the chromatic trials. Participants reported each stimulus as either "uncomfortably bright" or "not uncomfortably bright." The experiment was done binocularly and monocularly in separate sessions, and the order of color/viewing condition sequence was randomized across participants. The proportion of "uncomfortable" responses was used to generate individual psychometric functions, from which 50% discomfort thresholds were calculated. Results: Light-induced discomfort was higher under blue compared with red light stimulation, both during binocular (t(10) = 3.58, P < 0.01) and monocular viewing (t(10) = 3.15, P = 0.01). There was also a significant difference in discomfort between viewing conditions, with binocular viewing inducing more discomfort than monocular viewing for blue (P < 0.001), but not for red light stimulation. Conclusions: The light-induced discomfort characteristics reported here are consistent with features of the melanopsin-containing intrinsically photosensitive retinal ganglion cell light irradiance pathway, which may mediate photophobia, a prominent feature in many clinical disorders. This is the first psychometric assessment designed around melanopsin spectral properties that can be customized further to assess photophobia in different clinical populations.

The Initiation of Smooth Pursuit is Delayed in Anisometropic Amblyopia.

PURPOSE: Several behavioral studies have shown that the reaction times of visually guided movements are slower in people with amblyopia, particularly during amblyopic eye viewing. Here, we tested the hypothesis that the initiation of smooth pursuit eye movements, which are responsible for accurately keeping moving objects on the fovea, is delayed in people with anisometropic amblyopia. METHODS: Eleven participants with anisometropic amblyopia and 14 visually normal observers were asked to track a step-ramp target moving at ±15°/s horizontally as quickly and as accurately as possible. The experiment was conducted under three viewing conditions: amblyopic/nondominant eye, binocular, and fellow/dominant eye viewing. Outcome measures were smooth pursuit latency, open-loop gain, steady state gain, and catch-up saccade frequency. RESULTS: Participants with anisometropic amblyopia initiated smooth pursuit significantly slower during amblyopic eye viewing (206 ± 20 ms) than visually normal observers viewing with their nondominant eye (183 ± 17 ms, P = 0.002). However, mean pursuit latency in the anisometropic amblyopia group during binocular and monocular fellow eye viewing was comparable to the visually normal group. Mean open-loop gain, steady state gain, and catch-up saccade frequency were similar between the two groups, but participants with anisometropic amblyopia exhibited more variable steady state gain (P = 0.045). CONCLUSIONS: This study provides evidence of temporally delayed smooth pursuit initiation in anisometropic amblyopia. After initiation, the smooth pursuit velocity profile in anisometropic amblyopia participants is similar to visually normal controls. This finding differs from what has been observed previously in participants with strabismic amblyopia who exhibit reduced smooth pursuit velocity gains with more catch-up saccades.

Saccadic adaptation in visually normal individuals using saccadic endpoint variability from amblyopia.

PURPOSE: Saccadic adaptation is affected by the spatial variability of the adapting error signal. Recently, we have shown that saccadic adaptation is reduced in anisometropic amblyopia, possibly impacted by spatially imprecise saccades. Here, we tested this idea by quantifying the saccadic endpoint variability difference between people with anisometropic amblyopia and visually normal individuals. We then applied this difference to the second target step distribution during saccadic adaptation in visually normal people to test whether their performance diminished to a similar extent as participants with amblyopia. METHODS: Ten visually normal adults performed a double-step adaptation task (±19°, followed by 4° back-steps) with the nondominant eye under two conditions: "consistent error," using a constant back-step; and "variable error," using a variable (σdiff) back-step determined by subtracting the saccadic endpoint variability in controls from that in anisometropic amblyopia during amblyopic/nondominant eye viewing. Percentage change in saccadic gains, percentage retention, and adaptation time constants were analyzed. RESULTS: Percentage change in saccadic gains decreased significantly during the variable error condition (50% ± 10%) compared to the consistent error condition (69% ± 9%; P = 0.0008). Percentage retention and time constants did not differ between conditions. The adaptation magnitude during the variable error condition was comparable to the previous percentage adaptation in people with anisometropic amblyopia during the consistent error condition with amblyopic eye viewing. CONCLUSIONS: Our findings indicate that adding exogenous spatial noise to the adapting step consistent with the saccadic endpoint variability difference between amblyopic and visually normal groups is sufficient to reduce saccadic adaptation in healthy individuals.

Short-term saccadic adaptation in patients with anisometropic amblyopia.

PURPOSE: Amblyopia is a developmental disorder characterized by impairment of spatiotemporal visual processing that also affects oculomotor and manual motor function. We investigated the effects of amblyopia on short-term visuomotor adaptation using a saccadic adaptation paradigm. METHODS: A total of 8 patients with anisometropic amblyopia and 11 visually-normal controls participated. Saccadic adaptation was induced using a double-step paradigm that displaced a saccadic visual target (at ±19°) back toward central fixation by 4.2° during the ongoing saccade. Three test blocks, preadaptation, adaptation, and postadaptation, were performed sequentially while participants viewed binocularly and monocularly with the amblyopic and fellow eyes (nondominant and dominant eyes in controls) in three separate sessions. The spatial and temporal characteristics of saccadic adaptation were measured. RESULTS: Patients exhibited diminished saccadic gain adaptation. The percentage change in saccadic gain was lower in patients during amblyopic eye and binocular viewing compared to controls. Saccadic latencies were longer, and saccadic gains and latencies were more variable in patients during amblyopic eye viewing. The time constants of adaptation were comparable between controls and patients under all viewing conditions. CONCLUSIONS: The short-term adaptation of saccadic gain was weaker and more variable in patients during amblyopic eye and binocular viewing. Our findings suggest that visual error information necessary for adaptation is imprecise in amblyopia, leading to reduced modulation of saccadic gain, and support the proposal that the error signal driving saccadic adaptation is visual.

Effects of earth-fixed vs head-fixed targets on static ocular counterroll.

OBJECTIVE: To investigate whether static ocular counterroll (OCR) gain is reduced during viewing of an earth-fixed vs a head-fixed target. METHODS: Twelve healthy individuals were recruited. The target consisted of a red fixation cross against a grid pattern at a viewing distance of 33 cm. The target was mounted on a wall (earth fixed) or was coupled to the head (head fixed). Changes in mean torsional eye position were plotted as a function of head position steps (0 degrees +/- 25 degrees in 5 degrees steps), and sigmoidal fits were performed. Mean static OCR gain was calculated by taking the derivative of the fitted functions. RESULTS: Mean static OCR gain was 40% lower with a head-fixed target (-0.084) than with an earth-fixed target (-0.141) (P < .001). CONCLUSION: The reduction in static OCR gain during viewing of a head-fixed target indicates that static OCR is partially negated when a target moves with the head.

Effects of age, viewing distance and target complexity on static ocular counterroll.

The ocular counterroll (OCR) reflex generates partially compensatory torsional eye movements during static head roll tilt. We assessed the influence of age, viewing distance and target complexity on the OCR across the age span (13-63 years; n=47), by recording eye movements during head-on-body roll tilt (0+/-40 degrees in 5 degrees steps) while subjects viewed simple vs. complex targets at 0.33 and 1m. We found that subjects > or = 31 years had lower gains than those < or =30 years, but only for far targets. Consistent with prior reports, far targets elicited higher OCR gains than near targets, and target complexity had no effect on gains, suggesting that visual input is primarily used to maintain vergence during OCR.

The linear vestibulo-ocular reflex in patients with skew deviation.

PURPOSE: The linear vestibulo-ocular reflex (LVOR) is mediated primarily by the otolith organs in the inner ear. Skew deviation is a vertical strabismus believed to be caused by imbalance of otolithic projections to ocular motor neurons (disynaptically through the medial longitudinal fasciculus in the brain stem or polysynaptically through the cerebellum). The authors postulated that if skew deviation is indeed caused by damage to these projections, patients with skew deviation would show abnormal LVOR responses. METHODS: Six patients with skew deviation caused by brain stem or cerebellar lesions and 10 healthy subjects were recruited. All subjects underwent brief, sudden, interaural translations of the head (head heaves) using a head-sled device at an average peak acceleration of 0.42g (range, 0.1-1.1g) while continuously viewing an earth-fixed target monocularly at 15 and 20 cm. LVOR sensitivity (peak rotational eye velocity to peak linear head velocity) and velocity gain (peak actual-to-ideal rotational eye velocities) were calculated for the responses within the first 100 ms after onset of head movements. RESULTS: LVOR sensitivities and velocity gains in patients were decreased by 56% to 62% in both eyes compared with healthy subjects. This binocular reduction in LVOR responses was asymmetric--the magnitude of reduction differed between eyes by 37% to 143% for sensitivities and by 36% to 94% for velocity gains. There were no differences in response between right and left heaves. CONCLUSIONS: The binocular, asymmetric reduction in LVOR sensitivity and velocity gain provides support that imbalance in the otolith-ocular pathway is a mechanism of skew deviation.

The high-frequency/acceleration head heave test in detecting otolith diseases.

OBJECTIVE: To investigate whether transient, high-acceleration interaural head heaves (translational vestibulo-ocular reflex [tVOR]) could aid in the diagnosis of otolith diseases. STUDY DESIGN: Prospective cohort study. SETTING: Tertiary referral center. PATIENTS: Thirteen patients with symptoms suggestive of otolith diseases and 10 age-matched controls. INTERVENTIONS: Patients underwent a clinical otoneurologic examination and standard laboratory audiovestibular evaluation, including audiometry, electronystagmography with bithermal caloric, Halmagyi-Curthoys head thrust test with search coils, and vestibular-evoked myogenic potential. All subjects underwent subjective visual vertical (SVV) and tVOR testings. MAIN OUTCOME MEASURES: Sensitivity (ratio of peak eye to peak head velocities) and velocity gain (ratio of actual to ideal peak eye velocities). RESULTS: Five of 13 patients showed no abnormality in any tests. Of the remaining 8, 3 (38%) had reduced tVOR responses, whereas 1 (13%) had abnormal SVV. Sensitivity and velocity gains were symmetrically reduced in 2 patients, who had symptoms for 8 and 24 months. A third patient, symptomatic for 7 weeks, had asymmetric reduction of tVOR responses and a deviated SVV. CONCLUSION: Both head heave and SVV tests detect acute, asymmetric otolith diseases. Subjective visual vertical test relies on imbalance of utricular tone and may not detect bilateral symmetric diseases or partial diseases with central compensation. Our preliminary data in a small group of patients show that measuring the tVOR in a higher and more physiologic range of frequencies may serve as useful adjunct to detect acute and chronic otolith dysfunction and seems to be superior to the SVV in detecting bilateral symmetric or asymmetric otolith diseases.

The High-Frequency/Acceleration Head Heave Test in Detecting Otolith Diseases.

OBJECTIVE:: To investigate whether transient, high-acceleration interaural head heaves (translational vestibulo-ocular reflex [tVOR]) could aid in the diagnosis of otolith diseases. STUDY DESIGN:: Prospective cohort study. SETTING:: Tertiary referral center. PATIENTS:: Thirteen patients with symptoms suggestive of otolith diseases and 10 age-matched controls. INTERVENTIONS:: Patients underwent a clinical otoneurologic examination and standard laboratory audiovestibular evaluation, including audiometry, electronystagmography with bithermal caloric, Halmagyi-Curthoys head thrust test with search coils, and vestibular-evoked myogenic potential. All subjects underwent subjective visual vertical (SVV) and tVOR testings. MAIN OUTCOME MEASURES:: Sensitivity (ratio of peak eye to peak head velocities) and velocity gain (ratio of actual to ideal peak eye velocities). RESULTS:: Five of 13 patients showed no abnormality in any tests. Of the remaining 8, 3 (38%) had reduced tVOR responses, whereas 1 (13%) had abnormal SVV. Sensitivity and velocity gains were symmetrically reduced in 2 patients, who had symptoms for 8 and 24 months. A third patient, symptomatic for 7 weeks, had asymmetric reduction of tVOR responses and a deviated SVV. CONCLUSION:: Both head heave and SVV tests detect acute, asymmetric otolith diseases. Subjective visual vertical test relies on imbalance of utricular tone and may not detect bilateral symmetric diseases or partial diseases with central compensation. Our preliminary data in a small group of patients show that measuring the tVOR in a higher and more physiologic range of frequencies may serve as useful adjunct to detect acute and chronic otolith dysfunction and seems to be superior to the SVV in detecting bilateral symmetric or asymmetric otolith diseases.