Can vestibular-evoked myogenic potentials be used in the assessment of reflex habituation? A preliminary report

Feray Gulec Uyaroglu; Roza Ucar Sariteke; Nese Celebisoy

doi:10.4103/nsn.nsn_149_22

ORIGINAL ARTICLE

Year : 2023 | Volume : 40 | Issue : 1 | Page : 43-47

Can vestibular-evoked myogenic potentials be used in the assessment of reflex habituation? A preliminary report

Feray Gulec Uyaroglu¹, Roza Ucar Sariteke¹, Nese Celebisoy²
¹ Department of Neurology, Izmir Tepecik Education and Research Hospital, Izmir, Turkey
² Department of Neurology and Clinical Neurophysiology, Ege University Medical School, Izmir, Turkey

Date of Submission	16-Aug-2022
Date of Decision	01-Sep-2022
Date of Acceptance	02-Sep-2022
Date of Web Publication	29-Mar-2023

Correspondence Address:
Feray Gulec Uyaroglu
Department of Neurology, Izmir Tepecik Education and Research Hospital, Konak, Izmir
Turkey

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/nsn.nsn_149_22

Abstract

Background: Vestibular-evoked myogenic potentials (VEMPs) provide an electrophysiological evaluation of vestibular reflexes. The aim of the study was to search for the habituation of ocular and cervical VEMPs (cVEMPs). Materials and Methods: A total of 20 healthy volunteers (10 men and 10 women), with a mean age of 32.4 years (range: 25–45 years) were included in the study. cVEMP and ocular VEMP (oVEMP) tests were performed using “click stimuli.” In cVEMP and oVEMP tests, the latency and amplitude of the responses recorded with 100 and 250 stimulus sequences were compared. Results: When the traces recorded with 100 repetitions for both tests were compared with the traces obtained with 250 repetitions, it was observed that the latencies increased while the amplitudes decreased with increasing number of stimuli, which was statistically significant. Conclusion: Our results showed that an increase in the number of stimuli in oVEMP and cVEMP tests in healthy individuals led to a decrease in amplitude and an increase in latency. As noninvasive, short, and inexpensive evaluation methods, VEMP tests may be used in evaluating the “habituation response” and may find new areas of investigation.

Keywords: Cervical vestibular-evoked myogenic potential, habituation, ocular vestibular-evoked myogenic potential, vestibular reflex

How to cite this article:
Uyaroglu FG, Sariteke RU, Celebisoy N. Can vestibular-evoked myogenic potentials be used in the assessment of reflex habituation? A preliminary report. Neurol Sci Neurophysiol 2023;40:43-7

How to cite this URL:
Uyaroglu FG, Sariteke RU, Celebisoy N. Can vestibular-evoked myogenic potentials be used in the assessment of reflex habituation? A preliminary report. Neurol Sci Neurophysiol [serial online] 2023 [cited 2023 Jun 10];40:43-7. Available from: http://www.nsnjournal.org/text.asp?2023/40/1/43/372783

Introduction

Vestibular-evoked myogenic potentials (VEMPs), used in the examination of vestibular function, evaluate projections of otolithic organs to the extraocular and cervical muscles.^[1],[2],[3] Myogenic responses recorded from the sternocleidomastoid muscle (SCM) with saccular stimulation are called cervical VEMPs (cVEMPs) and responses recorded from the extraocular muscles with utricular stimulation are called ocular VEMPs (oVEMPs). During the tests, vestibular afferents are nonphysiologically stimulated by sound, and responses are recorded from target muscles with superficial electrodes. The noninvasive, low-cost, and practical nature of these tests provide a wide range of investigation.^[3],[4],[5]

In “evoked potential” tests such as visual-evoked potentials or brainstem auditory-evoked potentials, neural potentials are recorded. In VEMP tests, potentials are recorded from the muscles and generated by averaging repetitive stimulus sequences.^[6] In other words, VEMP traces are formed by averaged printing of reflex myogenic responses produced by repetitive stimulation.

In healthy people, the amplitude of the reflex responses recorded by repeated stimuli is expected to decrease (habituation). In cases such as Parkinson's disease (PD), this cannot be achieved (Myerson's sign). Evaluation of the number of stimulus repetitions in VEMPs may enable these tests to gain use in neurological pathologies associated with the concept of habituation. Evaluation of the oVEMP test in myasthenia gravis or studies that can be performed in diseases such as PD characterized by Myerson's sign is important in this respect.^[7],[8]

In this study, we focused on evaluating habituation in cVEMP and oVEMP tests and aimed to search for the latency and amplitude differences recorded by changing the given number of stimuli. Evaluation of VEMPs obtained with repetitive stimulus sequences in terms of habituation may enable these noninvasive and practical laboratory tests to find different uses.

Materials and Methods

Ten male and female volunteers with a mean age of 34.8 years (range: 25–45 years) were included in the study. Volunteers included in the study were selected among health-care professionals working in our hospital. Those with a history of ear disease, hearing loss, or drug use were excluded from the study. General systemic evaluation and neurological examination of all volunteers were performed and health system records were reviewed. All participants gave their informed written consent before their inclusion in the study. The study protocol was approved by the Local Ethics Committee (reference number 4–1/2018) and was performed in accordance with the ethical standards outlined in the Declaration of Helsinki. Tests were performed with a Synergy (Medelec; Oxford Instruments Medical Inc., UK) device.

Muscle activity was recorded by placing the superficial recording electrode on the outer half of the lower eyelid for oVEMP and the upper 1/3 of the SCM for the cVEMP. The reference electrode was placed 2 cm directly below the recording electrode for oVEMP and on the upper third of the sternum for the cVEMP. A bracelet electrode worn on the right wrist was used as the ground electrode. EMG activity was recorded using a 10–1000 Hz filter and 100 ms interval.

The tests were performed with the individuals sitting. The acoustic stimuli were clicks at an intensity of 110 dBnHL (normal hearing level) of 0.1-ms duration, delivered at a frequency of 5 Hz through a headphone unilaterally to the ear tested for cVEMP and contralaterally for oVEMP. For the cVEMP, the volunteers were asked to turn their heads to the opposite direction of the stimulus, and for oVEMP, they were asked to look at the target 2 m away and 45° above the horizontal plane. For each side, first 100 stimulus repeat sequences, then 250 stimulus repeat sequences were recorded and a 5-min recovery period was left between these stimulus sequences.

The first wave that caused a deviation from the isoelectric line in the oVEMP test was named n10/p15 and in the cVEMP test as p13/n23, and the latency and peak-to-peak amplitudes of these waves were taken into consideration.

IBM SPSS Statistics 25.0 (IBM Corp., Armonk, New York, USA) software was used for the statistical analysis. The hypothesis was tested at α: 0.05 significance level (P < 0.05 was considered statistically significant). The normality of the continuous variables was evaluated with the Shapiro–Wilk test. Independent sample t-test and Mann–Whitney U-test were used to compare age, latencies, and amplitudes. Pearson's Chi-square test was used for the right/left side comparisons and comparison between genders.

Results

Traces recorded from a total of 20 healthy volunteers (10 women, 10 men) with a mean age of 32.4 years (range: 25–45 years) were evaluated. In the cVEMP and oVEMP tests, responses recorded with 100 and 250 stimulus sequences were compared with each other in terms of latency and amplitude.

In both the cVEMP and oVEMP tests, it was found that the latency and amplitude values for the right and left sides were not significantly different from each other in the traces obtained using 100 and 250 stimulus sequences (P > 0.05 for all) [Table 1] and [Table 2]. Therefore, results recorded from the right and left sides were merged.

Table 1: Comparison of the latency and amplitude values obtained with 100 and 250 stimulus sequences in the cervical vestibular-evoked myogenic potentials test for the right and left sides

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Table 2: Comparison of the latency and amplitude values obtained with 100 and 250 stimulus sequences in the ocular vestibular-evoked myogenic potentials test for the right and left sides

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In cVEMP, mean p13, n23 latencies, and p13/n23 amplitudes obtained from 40 traces (right and left together) using 100 stimuli were 11.99 ± 0.34 (min 11.4–max 12.6) ms, 20.58 ± 0.77 (min 19.7–max 22.1) ms, and 254.79 ± 32.19 (min 193.2–max 366.3) μV, respectively. The results obtained using 250 stimuli were 12.64 ± 0.49 (min 11.7–max 13.5) ms, 22.23 ± 1.49 (min 19.5–max 23.7) ms, and 204.14 ± 42.72 (min 149.20–max 302.4) μV in the same order.

In oVEMP, mean n10, p15 latencies, and n10/p15 amplitudes gathered from 40 traces obtained using 100 stimuli were 8.98 ± 0.80 (min 7.7–max 10.3) ms, 13.07 ± 1.07 (min 11.20–max 15.0) ms, 31.84 ± 7.72 (min 19.70–max 44.60) μV, respectively. When 250 stimuli were given the results were 9.66 ± 0.78 (min 8.1–max 10.9) ms, 13.89 ± 0.90 (min 12.1–max 15.4) ms, and 23.83 ± 3.71 (min 18.2–max 33.6) μV.

When the traces recorded with 100 repetitions for both tests were compared with the traces obtained with 250 repetitions, it was observed that the latencies increased while the amplitudes decreased with increasing repetition, which was statistically significant (P < 0.05 for all) [Table 3] and [Figure 1].

Figure 1: cVEMP and oVEMP traces. In both tests, the traces obtained with 100 repetitions had larger amplitudes and shorter latency compared to the traces obtained with 250 repetitions. cVEMP: Cervical vestibular-evoked myogenic potentials, oVEMP: Ocular vestibular-evoked myogenic potentials

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Table 3: Comparison of latency and amplitude values in cervical vestibular-evoked myogenic potentials and ocular vestibular-evoked myogenic potentials tests, right and left together (for 40 tests of 20 volunteers), 100 and 250 stimulus sequences

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Discussion

In both cVEMP and oVEMP tests, the amplitudes were significantly larger and the latencies were significantly shorter when the number of stimuli given was low. Prolonged latencies and reduced amplitudes were noted with increasing the number of stimuli.

Although myogenic responses that occur with sudden and high decibel sound stimuli have been known for a long time, it was only possible after the 90 s to elucidate their nature and transform them into a model suitable for clinical use.^[9],[10] Bickford (1972) defined the inion responses induced by sound stimuli as “myogenic microreflexes” recorded from the muscle cells.^[11],[12] Capturing these microreflexes produced by single motor unit discharges by an intramuscular electrode is not possible due to their small amplitude and the presence of background noise. The surface activity recorded by a surface electrode and averaged in VEMP tests makes these reflexes visible and provides reliable and consistent potentials.^{[11],[12],[13]}

In the VEMP test, averaging is the main factor that determines the morphological features of the potentials corresponding to activation or inhibition of the muscle activity recorded by the surface electrode.^{[14],[15],[16]} Bone conduction sound and galvanic stimulation inevitably produce bilateral effects on the vestibular structures on either side of the head. Therefore, the air-conducted sound stimulus is preferred in the evaluation of vestibular function on one side. For this reason, cVEMP and oVEMP traces obtained with unilateral click stimulus were evaluated in our study.

Sacculus is more sensitive to movement in the vertical plane, and the utriculus is more sensitive to movement in the horizontal plane. Sacculocollic projections for achieving and maintaining erect posture are evaluated with the cVEMP test, and utriculo-ocular projections for keeping the eyes on target during head movements are evaluated with the oVEMP test.^[13],[16] VEMP tests provide the opportunity to evaluate right/left, sacculus/utriculus, inferior/superior vestibular nerve separately, and creating an advantage in evaluating peripheral vestibular pathologies such as vestibular neuritis, Meniere's disease, benign paroxysmal positional, and superior canal dehiscence syndrome.^{[17],[18],[19]} It has been shown that these tests can provide additional information on neurological diseases such as migraine, multiple sclerosis, and extrapyramidal system diseases that may affect vestibular pathways.^[20],[21] Evaluation of myogenic responses to repetitive stimuli is also important in neuromuscular diseases such as myasthenia gravis.^[7]

In PD, characterized by postural instability, anteflexion posture, and camptocormia, Myerson's sign indicates a loss of the habituation response.^[21],[22] Since repetitive stimuli are used in both cVEMP and oVEMP tests, the “habituation response” recorded in healthy individuals is expected to be impaired in PD. Therefore, first of all, searching for the habituation response in VEMPs in healthy individuals may play a key role to evaluate this phenomenon in other neurological diseases.

Focusing on the electrophysiological features of the vestibular reflexes evaluated in these tests may help to identify different areas of use. In this study, we focused on the reflex habituation response and examined the effect of the number of stimulus repetitions on VEMP traces. Our results showed that an increase in the number of stimuli in oVEMP and cVEMP tests in healthy individuals led to a decrease in amplitude and a prolongation in latency. As noninvasive, short, and inexpensive evaluation methods, VEMP tests may be used in evaluating the “habituation response” and may find new areas of investigation.

The inclusion of only 20 healthy volunteers is the main limitation of our study. Therefore, it was named a preliminary report. Future studies, including a higher number of individuals from different age groups, are needed for more concrete results. The other limitation is the use of air conduction as the only method of stimulation. Bone conduction stimulation must also be studied. Large-scale studies, to overcome the abovementioned limitations may help to broaden our perspective on the use of VEMPs and may provide interesting findings in the field of neurotology.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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