Literature DB >> 35418364

Vestibular Co-stimulation in Adults with a Cochlear Implant.

Morgana Sluydts1, Marc Leblans2, Joost Js van Dinther2, Erwin Offeciers2, Robby Vanspauwen1, Floris L Wuyts1, Andrzej Zarowski2.   

Abstract

BACKGROUND: Vestibular co-stimulation is a side effect of cochlear implant stimulation. The electrical currents delivered by the cochlear implant can spread toward the vestibular system and thus stimulate it. The aim of the study is to evaluate whether it is feasible to functionally restore the balance by modifying the vestibular co-stimulation.
METHODS: Four adult patients, who had received a commercially available cochlear implant previously, were enrolled. Counterbalanced biphasic pulses were presented as bursts or as an amplitude-modulated biphasic pulse train (modulation frequencies ranging from 1 to 500 Hz) at the participant's upper comfortable level for electrical stimulation. Subjective sensations and vestibular-mediated eye movements were used for evaluating the possible effects of vestibular co-stimulation.
RESULTS: One participant experienced a cyclic tilting of his head in response to an amplitude-modulated biphasic pulse train with a modulation frequency of 2 and 400 Hz. However, during a follow-up visit, the sensation could not be replicated.
CONCLUSION: Subjective vestibular sensations or vestibular-mediated eye movements could not be electrically evoked with a commercially available cochlear implant in 4 adult patients with almost normal vestibular function. Therefore, customized design of the hard-, firm-, and/or software of the commercially available cochlear implant might be necessary in order to electrically restore vestibular performance.

Entities:  

Mesh:

Year:  2022        PMID: 35418364      PMCID: PMC9450210          DOI: 10.5152/iao.2022.21431

Source DB:  PubMed          Journal:  J Int Adv Otol        ISSN: 1308-7649            Impact factor:   1.316


Introduction

Bilateral vestibulopathy (BVP) is a chronic vestibular syndrome that can have a serious impact on the quality of life. Patients with BVP are at increased risk of falling, which can result in several detrimental and sometimes even fatal consequences (e.g., (hip) fractures, hospital admissions, death).[1,2] Because these patients continuously and consciously have to correct their balance, the cognitive load is often increased as well.[3,4] Participation in social and professional activities may thus become complicated with social isolation as a result.[5,6] There are a couple of treatment options for patients with vestibular loss like vestibular rehabilitation or sensory substitution devices.[7-10] However, these treatment options rely on multisensory integration rather than actual restoration of the vestibular reflexes. Therefore, electrical vestibular stimulation (EVS) has been suggested as an alternative approach for artificially restoring the vestibular input. One example of EVS is vestibular co-stimulation with a commercially available cochlear implant (CI). The underlying mechanism of vestibular co-stimulation is based on the theory of spread of excitation, which implies that the currents delivered by the CI can spread toward the surrounding neural structures and tissues. Multiple reports of vestibular co-stimulation have been made throughout the years. In 1982, Eisenberg et al[11] wanted to investigate the possibly detrimental influence of a single-electrode CI on the vestibular system, but instead, they had to conclude that using a CI can actually improve postural stability. Later, Bance et al[12] were able to evoke a nystagmus beating toward the side of implantation with a multichannel CI, albeit in 1 case only. More recently, Nassif et al[13] concluded that the gain of the video head impulse test (vHIT) increased during CI stimulation in comparison to the gain measured without the CI activated in the same patients. Several other researchers observed improvements in postural stability and gait,[14-17] and perception of verticality.[18] Furthermore, cervical and ocular vestibular-evoked myogenic potentials (c- and oVEMPs, respectively) have been shown to be electrically evocable through CI stimulation.[17,19] The results of the abovementioned studies suggest that the CI is capable of simultaneously stimulating the auditory and vestibular system without requiring additional modifications of the device and/or the surgical technique. In this study, the otolith system is targeted as it is mainly responsible for the prevention of falls and their detrimental consequences.[20] The goal of this study was to evaluate whether it was possible to ­electrically elicit otolith-mediated motion percepts (e.g., head tilt or translations) or otolith-mediated reflexes (translational vestibulo-ocular (tVOR) reflex or ocular counter-rolling) in adult CI patients.

MATERIALS AND Methods

Participants

Four adult CI recipients (2 males and 2 females) were enrolled at least 6 months after the initial activation of their CI. The subjects were implanted at the European Institute for ORL-HNS (Sint-Augustinus, GZA Hospital, Antwerp, Belgium). In order to be able to subjectively perceive the effect of vestibular co-stimulation, it was decided to include only patients with residual or normal vestibular function. The likelihood of detecting a perturbation was expected to be higher in patients without total deprivation of the vestibular afferents. Subject 1 (S1) and subject 4 (S4) were unilaterally implanted with a Nucleus® CI532 (Cochlear™, Sydney, Australia), while S2 and S3 received a Nucleus® CI512 (Cochlear™, Sydney, Australia) (Table 1). All participants had progressively developed bilateral profound sensorineural or combined hearing loss (Table 1). No anatomical anomalies were detected on computed tomography or magnetic resonance imaging at the time of implantation.
Table 1.

Patient Demographics

Subject 1Subject 2Subject 3Subject 4
Age at implantation (years)70377069
Age at time of the study (years)71407269*
PTA (dB HL)RightLeftRightLeftRightLeftRightLeft
65deaf939285856873
Implant sideLeftRightRightRight
Implant typeCI532CI512CI512CI532
Contralateral earHearing aidHearing aidHearing aidUnaided
DiagnosisChronic middle ear disorders (progressive, permanent hearing loss)Idiopathic SNHL with onset at 4 years old (unidentified hereditary component)Idiopathic SNHL (probably due to streptomycin treatment during childhood)Iatrogenic SNHL (streptomycin treatment during childhood)

SNHL, sensorineural hearing loss; CI, cochlear implant; PTA, pure tone audiometry (average of hearing thresholds at 500 Hz, 1000 Hz, and 2000 Hz) before implantation; dB HL, decibel hearing level.

*Six months after initial cochlear implant activation.

Vestibular Function Tests

The vestibular performance was evaluated before and after implantation. Postoperative vestibular testing was performed without CI. The vestibular test battery included the sinusoidal harmonic acceleration (SHA) test, the caloric irrigation test, the horizontal vHIT, the cVEMP test, and the oVEMP test. The SHA test (Minitorque, Difra Instrumentation SA, Eupen, Belgium) was performed at a rotation frequency of 0.05 Hz with a maximum velocity of 50°/s. A gain above 0.29 was considered normal (Table 2). Subsequently, caloric irrigations were performed with cold (30˚C) and warm (44˚C) water (Aquastar, Difra Instrumentation SA, Eupen, Belgium). The caloric response was considered normal when the caloric sum of all irrigations was >48.8°/s and the unilateral weakness parameter was <17.4% (Table 2). Subject 1 did not receive caloric testing after the implantation due to a blind sac closure (Table 2).
Table 2.

Semicircular Canal Function After Cochlear Implantation

Implanted EarUnimplanted EarCaloric Test
SHAT: GainvHIT: GainSHAT: GainvHIT: GainCaloric Sum (°/s)Unilateral Weakness (%)
S10.381.170.641.06Blind sac closureBlind sac closure
S20.280.730.190.9852°/s6% contralateral
S30.550.770.640.95140°/s8% ipsilateral
S40.400.720.360.8157°/s17% contralateral

S, subject; ipsilateral/contralateral, ipsi- or contralateral with regard to the implanted ear; SHAT, sinusoidal harmonic acceleration test; vHIT, video head impulse test.

For the horizontal vHIT (Headstar, Difra Instrumentation SA, Eupen, Belgium), only head impulses with a velocity of approximately 200°/s were accepted. The gain was calculated according to the regression slope of the eye velocity (°/s) in relation to the head velocity (°/s). Gains higher than or equal to 0.61 were considered normal (Table 2). Subject 4 had a normal gain in combination with overt correction saccades in the unimplanted ear (left). None of the other subjects had overt or covert correction saccades. The cVEMP test was performed with air- or bone-conducted 500-Hz tone bursts of alternating polarity (2-2-2 ms rise/fall and plateau time; repetition rate = 5.1 Hz) (Neurosoft®, NeurAudio®, Ivanovo, Russia). The air-conducted cVEMP was evoked with insert earphones (Tone 3A Insert Earphones, E-A-R Auditory Systems®, Indianapolis, Ind, USA) at a maximum sound level of 135 decibel sound pressure level (dB SPL). The implanted ear of S1 required a blind sac closure due to chronic middle ear disorders. Therefore, bone-conduction cVEMP was performed for assessing the saccular function after the cochlear implantation. A B71 bone vibrator (B71 Bone Transducer Headset, RadioEar®, Middelfart, Denmark) attached to an additional amplifier with a gain of 15 dB (Neurosoft®, NeurAudio®, Ivanovo, Russia) was used for stimulation at the mastoids. The output was 117 dB force level (dB FL). Only cVEMP traces with an average muscle contraction level higher than 100 µV were accepted.[21] The cVEMP was interpreted as normal when the left–right threshold difference was ≤10 dB and when the left–right difference in corrected amplitude was ≤1.7 (Table 3).
Table 3.

Otolith Function After Cochlear Implantation

Implanted EarUnimplanted Ear
cVEMPoVEMPcVEMPoVEMP
Threshold (dB SPL)Corrected Amplitude* Amplitude (µV)Threshold (dB SPL)Corrected Amplitude* Amplitude (µV)
S1Absent AbsentAbsent1301.0Absent
S21151.221.01201.717.3
S3AbsentAbsent14.8AbsentAbsent13.3
S41350.49.71251.45.7

S, subject; c/oVEMP, cervical/ocular vestibular-evoked myogenic potential; dB SPL, decibel sound pressure level.

*Measured at the highest level of stimulation.

A hand-held bone-conduction vibrator (Mini Shaker type 4810, amplifier model 2718, Brüel & Kjaer®, Nærum, Denmark) was placed at Fz, that is, the midline of the forehead near the hairline, for evoking the oVEMP (Neurosoft®, NeurAudio®, Ivanovo, Russia) (Table 3). The Mini Shaker delivered 500-Hz square wave jerks with an alternating polarity at a 5-Hz stimulation rate. The stimuli were presented at 121 dB FL. The recording surface electrodes were placed as close as possible underneath the inferior orbital rim. The reference electrodes were placed 2 cm below the recording electrodes and the ground electrode was placed on the sternum. The oVEMP was interpreted as normal when bilaterally present at 121 dB FL with a maximal left–right amplitude difference of 12 µV (Table 3).

Electrical Stimulation and Response Recordings

The eye movements were monitored and recorded through video­nystagmography (Headstar, Difra Instrumentation SA, Eupen, Belgium). Visual suppression of eye movements was prevented by covering the second eye and by dimming the light in the examination room. The subjects were instructed to report any kind of (non-)vestibular sensation and were seated on a stable chair. In order to facilitate communication, contralateral hearing aids were kept activated during the session. A baseline measurement without electrical stimulation was performed first, in order to detect the presence of a spontaneous nystagmus. Subsequently, the stimuli were programmed through the Nucleus Implant Communicator (NIC) software (Cochlear™, Sydney, Australia) and presented by an L34 research processor (Cochlear™, Sydney, Australia). Finally, the already implanted intracochlear electrode array delivered the stimuli to the inner ear. The stimulation patterns were presented for 60 seconds and consisted of counterbalanced biphasic pulses (phase width = 100 µs, interphase gap = 7 µs) presented as bursts or as an amplitude-modulated biphasic pulse train (Figure 1). For the latter, modulation frequencies between 1 and 500 Hz were used.
Figure 1.

The upper waveform represents a pulse train of biphasic pulses that were presented in bursts. The lower waveform is the amplitude-modulated biphasic pulse train.

For each subject, the stimuli were different and dependent on the subject’s reports and the observed results (Tables 4 and 5). An individual dynamic range (i.e., the range between the sound detection threshold and the upper comfortable level (UCL)) was defined for each stimulus in order to avoid overstimulation. Increments of 5 current levels (CL) were used to define the UCL. Once the UCL was determined for a specific stimulus, the stimulation was presented for 60 seconds at that intensity. None of the participants reported pain or discomfort during this study. Before and after every 60 seconds of stimulation, the eye movements were recorded for 30 seconds so that any changes upon activation or deactivation of the stimulation could be detected.
Table 4.

Individual Stimulation Parameters: Biphasic Pulses Presented as Bursts

Subject 1
Intra-Burst Pulse Rate (pps) f burst (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)Np/Burst
4673100E3MP1 + MP21502631
467320E3MP1 + MP21703771
4673300E3MP1 + MP21301831
467310E3MP1 + MP21754131
4673300E3MP1 + MP21301832
4673100E3MP1 + MP21201534
2336300E3MP1 + MP21251674
1558100E3MP1 + MP21402198
4673300E3MP1 + MP21201538
467320E3MP1 + MP215026316
4673100E3MP1 + MP212015324
116820E3MP1 + MP214524024
467310E3MP1 + MP214021948
467320E3MP1 + MP213018396
467310E12MP1 + MP21653451
467310E22MP1 + MP21402191
Subject 2 (First Visit)
Intra-Burst Pulse Rate (pps) f burst (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)Np/burst
46732E3MP1 + MP29597584
46732E3MP1 + MP2100107292
46732E3MP1 + MP21352001
Subject 3
Intra-Burst Pulse Rate (pps)fburst (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)Np/Burst
46732E3MP1 + MP21201531
4673400E3MP1 + MP21402191
4673100E3MP1 + MP21452401
46732E3MP1 + MP2110128584
4673400E3MP1 + MP21301833
4673100E3MP1 + MP212015312
4673100E3MP1 + MP212516712
4673200E3MP1 + MP21301836
467310E3MP1 + MP2130183117
4673400E3MP1 + MP21402193
Subject 4
Intra-Burst Pulse Rate (pps) f burst (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)Np/Burst
46732E3MP1 + MP21603151
46732E3MP1 + MP21603151
4673400E3MP1 + MP21301831
4673100E3MP1 + MP21402191
46732E3MP1 + MP2110128584
4673400E3MP1 + MP21251673
4673100E3MP1 + MP211514012

pps, pulses per second; f burst (Hz), burst frequency (Hertz); E3/12/22, basal/middle/apical electrode contact; MP1, ball reference electrode; MP2, fixed location on the implant; Np/burst, number of biphasic pulses in 1 burst.

Table 5.

Individual Stimulation Parameters: Amplitude-Modulated Pulse Train

Subject 2 (First Visit)
Pulse Rate (pps)Modulation Frequency (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)
46732E3MP1 + MP2105117
4673400E3MP1 + MP2110128
4673100E3MP1 + MP2105117
467320E3MP1 + MP2105117
467310E3MP1 + MP2105117
46732E3MP1 + MP2105117
46732E3MP1 + MP2105117
23362E3MP1 + MP2105117
11682E3MP1 + MP2115140
46732E12MP1 + MP2115140
46732E22MP1 + MP29089
23362E22MP1 + MP29089
Subject 2 (Second Visit)
Pulse Rate (pps)Modulation Frequency (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)
467320E3MP1 + MP2105117
4673400E3MP1 + MP2100128
46732E3MP1 + MP2105117
46731E3MP1 + MP2105117
46735E3MP1 + MP2105117
46732E12MP1 + MP2110117
46732E22MP1 + MP2100117
46731E22MP1 + MP2105117
46732E22MP1105117
46732E22MP2110117
46731E3MP2105117
Subject 3
Pulse Rate (pps)Modulation Frequency (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)
46732E3MP1 + MP29089
4673400E3MP1 + MP2130183
4673100E3MP1 + MP2115140
4673200E3MP1 + MP2130183
467310E3MP1 + MP2125167
Subject 4
Pulse Rate (pps)Modulation Frequency (Hz)Electrode ContactReference ElectrodeCurrent LevelCurrent (µA)
46732E3MP1 + MP2110128
4673400E3MP1 + MP2120153
4673100E3MP1 + MP2120153
46732E22MP1 + MP2115140
4673400E22MP1 + MP2120153
4673100E22MP1 + MP2115140
46732E3MP1125167
4673100E3MP1115140
467310E3MP1115140

pps, pulses per second; MP1, ball reference electrode; MP2, fixed location on the implant; E3/12/22, basal/middle/apical electrode contact.

Monopolar (MP) stimulation was used in all 4 cases. In general, the reference electrode configuration was set as a combination of the ball (MP1) and plate electrode (MP2) but when the conditions allowed for it (based on time, tiredness of subject, …), the effects of MP1 and MP2 were examined separately as well. The stimuli were delivered through a basal (E3) electrode contact of the intracochlear electrode array. One middle electrode contact (E12) and one apical electrode contact (E22) were used for additional measurements (Tables 4 and 5).

Statistics

Statistical analyses could not be performed due to the small sample size (n = 4). This prospective open study was conducted according to the principles of the Declaration of Helsinki, and institutional ethical approval was obtained from the local ethics committee (GZA Hospital, Antwerp; study number: 181111ACADEM). All participants provided written informed consent.

Results

Subject 1

The first subject (S1) had a discrete spontaneous nystagmus to the right. The spontaneous nystagmus was present throughout the entire session and did not change direction or velocity. Regardless of which stimulation configuration was used (Table 4), the subject only perceived auditory percepts (e.g., buzzing, ticking, chirping sound). Electrically evoked eye movements were also absent. At the end of the session, one measurement was performed with electrical stimulation at E12 and one at E22, but besides a change in the auditory percept (i.e., more low-frequent sound percepts with the more apical electrode contacts), no changes in subjective or objective vestibular outcomes were observed.

Subject 2

Subject 2 had a rightward beating spontaneous nystagmus with a discrete downbeat component during his first session. Electrical stimulation with bursts did not evoke vestibular sensations or additional eye movements (Table 4). Stimulation with amplitude-modulated biphasic pulse trains (Table 5) with a modulation frequency of 2 Hz at E3 induced a perception of the head tilting to the left (i.e., away from the stimulation site). The same sensation was evoked with a 400-Hz modulation frequency but not with modulation frequencies 10 Hz, 20 Hz, and 100 Hz. A reduction in the stimulation rate from 4673 pulses per second (pps) to 2336 pps diminished the strength of the tilt sensation. A further reduction of the stimulation rate to 1168 pps led to a stronger perception of the head tilt, as it allowed for higher stimulus intensity. There were no changes observed in the eye movements, regardless of the stimulus used. Due to the obtained results, S2 was invited for a second session. During the baseline measurement, a spontaneous nystagmus to the right with a discrete upbeat component was observed (in contrast to the initial discrete downbeat nystagmus). The characteristics of the spontaneous nystagmus did not change during the experiment. The stimuli that were presented were those that evoked the head tilt during the first session. However, 2 additional modulation frequencies (1 Hz and 5 Hz) were added. Unfortunately, none of the results from the first session could be replicated and the subject clearly indicated that he only experienced auditory percepts (e.g., chirping) during the second session. Changing the reference or stimulation electrode did not change the outcome.

Subject 3

During the baseline measurement of S3, a discrete spontaneous nystagmus to the left was visible with additional sporadic horizontal and vertical flutter-like eye movements. A head tremor with horizontal and vertical components was observed as well. It is unclear whether the flutter-like eye movements were the VOR in response to the head tremor or rather an additional symptom. Imaging did not reveal abnormalities and the patient did not report any symptoms. Both stimulation patterns (amplitude-modulated biphasic pulse trains and bursts) (Table 5) presented at E3 did not evoke vestibular sensations or changes in the eye movements.

Subject 4

The baseline eye recordings of subject 4 showed a leftward beating spontaneous nystagmus. No changes of the eye movements were observed during electrical stimulation, regardless of which type of stimulus (bursts or amplitude-modulated pulse trains) was presented (Tables 4 and 5). The subject did not report any vestibular percepts either. There was no detectable effect of modulation frequency (2 Hz, 10 Hz, 100 Hz, and 400 Hz), stimulation electrode contact (E3 or E22), or reference electrode (MP1 or MP1+2).

Discussion

The goal of this study was to evaluate the feasibility of indirectly stimulating the vestibular nerve by means of the current spreading from a CI. The results show that it is difficult to evoke objective or subjective vestibular responses with the described approach. One of the participants (S2) perceived a head tilt during stimulation but this percept could not be replicated. Moreover, there were no electrically mediated eye movements that coincided with the alleged vestibular sensation. In a recent study, a higher activation threshold was observed for electrically evoked vestibular percepts in comparison to electrically evoked VOR or cVEMPs.[22] Thus, a coexisting eye movement could have been expected during the tilt sensation; however, this was not the case. It is therefore unlikely that the perceived head tilt was electrically mediated. It seems that S2 was biased by the vestibular nature of the study and that he perceived the envelope of the amplitude-modulated pulse train as a wave-like motion or head tilt. Elimination of the auditory component could have prevented this, though it seems difficult to accomplish due to the location of the stimulating electrode inside the cochlea. Furthermore, vestibular co-stimulation is a form of far-field stimulation and is dependent on the total amount of electrical energy delivered by the intracochlear array. Lowering the total amount of energy to avoid the audibility of the signal probably would have reduced the likelihood of evoking a vestibular reflex or percept even further. Most studies that succeeded in evoking or improving vestibular reflexes in CI recipients used audible stimulation at UCL,[11,15,18,19] which is similar to the present study. A possible explanation for the discrepancy in obtained results may be the number of stimulating electrode contacts. In most studies, the participant’s standard CI settings were used, which implies that multiple electrode contacts were activated during stimulation, especially when background noise or music was presented.[11,15] Therefore, the total amount of electrical energy delivered to the inner ear may have been higher than in the present study (as only 1 electrode contact was activated during each measurement). Nonetheless, Gnanasegaram et al[18] and Parkes et al[19] used just 1 electrode contact and they successfully elicited cVEMPs and improved the perception of verticality. The waveforms of the stimuli that were used (i.e., single biphasic pulses or biphasic pulse trains) were quite similar to those used in the present study, but the parameters of the biphasic pulses were slightly different. In their studies, the phase width of the biphasic pulse was much shorter (25 µs with a 7-µs interphase gap) which may explain the higher UCLs that were used. The lowest UCL in the studies of Gnanasegaram and colleagues[18,19] was comparable to the highest UCL in the present study. The phase width was fixed in the present study at 100 µs, but systematic comparison of different phase widths may help to understand the observed discrepancy. In previous studies, the electrically restored auditory (directional) cues have been suggested to contribute to the improved balance,[23] especially when background noise or music is provided.[12,15,17,24] In the present study, the possible beneficial effects of the electrically restored auditory cues were not investigated. The subjects did perceive electrically evoked sounds, but these were artificially mediated by the NIC software (Cochlear™, Sydney, Australia) and were not the environmental sounds contributing to spatial orientation. At the moment, the unwanted audibility of the signal and the absence of reproducible signs of effective vestibular stimulation limit the functional implementation of the described stimulation paradigm as an efficient treatment method. This conclusion is however based on a very small sample size (n = 4) and should be further explored. As the likelihood of detecting a perturbation was expected to be higher in patients without deprived vestibular afferents, only patients with almost normal vestibular function were included. However, such patients may not be the ideal study population as the high amount of residual vestibular function may impede the possible effects of stochastic resonance, even though the oVEMPs and cVEMPs were absent in some of them. Stochastic resonance (SR) is a physiological mechanism that improves the performance of a non-linear system (like the vestibular system) with subthreshold residual function when noise is provided.[25] In case of too much residual function or too much noise (e.g., the electrical stimulus), SR fails to improve the overall performance. Moreover, the long-term goal is to use vestibular co-stimulation as a treatment option for patients with BVP. Even though patients with afferent deprivation should be avoided, future studies should focus on patients with more abnormal vestibular function. As all patients received their CI prior to the study, manipulation of the position of the reference electrode was limited to MP1, MP2, or MP1+MP2. Intra-operative manipulation of the ball electrode (e.g., positioning in the vicinity of the vestibular structures) may revoke this limitation. As a result, the current pathway can be directed toward the vestibular structures, which may increase the likelihood of successful vestibular co-stimulation. The applied changes to the stimulation parameters were also limited, as the goal was to not drastically change the hard-, firm-, or software of the commercially available CI. The present results however suggest that modifications to the design of the CI are warranted.

Conclusion

Subjective vestibular sensations or otolith-mediated eye movements could not be evoked through vestibular co-stimulation with a commercially available CI in 4 adult patients with almost normal vestibular function. Therefore, customized design of the hard-, firm-, and/or software of the commercially available cochlear implant might be necessary in order to electrically restore vestibular performance.
  25 in total

1.  Effects of muscle contraction on cervical vestibular evoked myogenic potentials in normal subjects.

Authors:  Sally M Rosengren
Journal:  Clin Neurophysiol       Date:  2015-01-23       Impact factor: 3.708

Review 2.  The role of sensory augmentation for people with vestibular deficits: Real-time balance aid and/or rehabilitation device?

Authors:  K H Sienko; S L Whitney; W J Carender; C Wall
Journal:  J Vestib Res       Date:  2017       Impact factor: 2.435

3.  Auditory contributions to maintaining balance.

Authors:  Madelyn N Stevens; Dennis L Barbour; Meredith P Gronski; Timothy E Hullar
Journal:  J Vestib Res       Date:  2016       Impact factor: 2.435

4.  Fall-related injuries for three ages groups - Analysis of Swedish registry data 1999-2013.

Authors:  Hans Ekbrand; Robert Ekman; Charlotta Thodelius; Michael Möller
Journal:  J Safety Res       Date:  2020-03-16

Review 5.  The Superiority of the Otolith System.

Authors:  Angel Ramos de Miguel; Andrzej Zarowski; Morgana Sluydts; Angel Ramos Macias; Floris L Wuyts
Journal:  Audiol Neurootol       Date:  2020-01-10       Impact factor: 1.854

6.  Effects of the single-electrode cochlear implant on the vestibular system of the profoundly deaf adult.

Authors:  L S Eisenberg; J R Nelson; W F House
Journal:  Ann Otol Rhinol Laryngol Suppl       Date:  1982 Mar-Apr

7.  Vestibular vertigo and comorbid cognitive and psychiatric impairment: the 2008 National Health Interview Survey.

Authors:  Robin T Bigelow; Yevgeniy R Semenov; Sascha du Lac; Howard J Hoffman; Yuri Agrawal
Journal:  J Neurol Neurosurg Psychiatry       Date:  2015-04-17       Impact factor: 10.154

Review 8.  Stochastic resonance and sensory information processing: a tutorial and review of application.

Authors:  Frank Moss; Lawrence M Ward; Walter G Sannita
Journal:  Clin Neurophysiol       Date:  2004-02       Impact factor: 3.708

9.  Playing Music May Improve the Gait Pattern in Patients with Bilateral Caloric Areflexia Wearing a Cochlear Implant: Results from a Pilot Study.

Authors:  Ann Hallemans; Griet Mertens; Paul Van de Heyning; Vincent Van Rompaey
Journal:  Front Neurol       Date:  2017-08-17       Impact factor: 4.003

10.  Simultaneous activation of multiple vestibular pathways upon electrical stimulation of semicircular canal afferents.

Authors:  Anissa Boutabla; Samuel Cavuscens; Maurizio Ranieri; Céline Crétallaz; Herman Kingma; Raymond van de Berg; Nils Guinand; Angélica Pérez Fornos
Journal:  J Neurol       Date:  2020-08-10       Impact factor: 4.849

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