Clinical Neurophysiology xxx (2015) xxx–xxx
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Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth Jennifer C. Parker-George ⇑, Steven L. Bell, Michael J. Griffin Institute of Sound and Vibration Research, University of Southampton, United Kingdom
a r t i c l e
i n f o
Article history: Accepted 17 February 2015 Available online xxxx Keywords: Vestibular Otolith Vestibular evoked potentials OVEMP Vibration
h i g h l i g h t s This study investigates if applying stimulation directly to the teeth improves measurement of the
vibration-induced oVEMP. Applying 100-Hz vibration tone pips directly to the teeth via a customised bite-bar elicits clearer
oVEMP responses than direct application to the head. The quality and amplitude of vibration-induced oVEMPs is dependent on stimulus characteristics.
a b s t r a c t Objectives: This study investigated whether the method for eliciting vibration-induced oVEMPs could be improved by applying vibration directly to the teeth, and how vibration-induced oVEMP responses depend on the duration of the applied vibration. Methods: In 10 participants, a hand-held shaker was used to present 100-Hz vibration tone pips to the teeth via a customised bite-bar or to other parts of the head. oVEMP potentials were recorded in response to vibration in three orthogonal directions and five stimulus durations (10–180 ms). The oVEMP responses were analysed in terms of the peak latency onset, peak-to-peak amplitude, and the quality of the trace. Results: Vibration applied to the teeth via the bite-bar produced oVEMPs that were more consistent, of higher quality and of greater amplitude than those evoked by vibration applied to the head. Results: Longer duration stimuli produced longer duration oVEMP responses. Results: One cycle duration stimuli produced responses that were smaller in amplitude and lower quality than the longer stimulus durations. Conclusions: Application of vibration via the teeth using a bite-bar is an effective means of producing oVEMPs. Conclusions: A 1-cycle stimulus is not optimal to evoke an oVEMP because it produces less robust responses than those of longer stimulus duration. Conclusions: A positive relationship between the duration of the stimulus and the response is consistent with the notion that the vibration-induced oVEMP is an oscillatory response to the motion of the head, rather than being a simple reflex response that occurs when the stimulus exceeds a threshold level of stimulation. Significance: Applying acceleration to the teeth through a bite-bar elicits clearer oVEMP responses than direct application to other parts of the head and has potential to improve clinical measurements. A 100-Hz 1-cycle stimulus produces less robust oVEMP responses than longer 100-Hz stimuli. Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction
⇑ Corresponding author at: 22 Cinderhill Way, Ruardean, Gloucestershire, GL17 9TQ, United Kingdom. Tel.: +44 7974481896. E-mail address: [email protected] (J.C. Parker-George).
Vestibular evoked myogenic potentials (VEMPs) are thought to be a measure of reflexive changes in muscle tone in response to the activation of the vestibular system. VEMPs are most commonly
http://dx.doi.org/10.1016/j.clinph.2015.02.007 1388-2457/Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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elicited using a high level acoustic stimulus, with the acoustic sensitivity of the vestibular system first described by Tulio (1929). VEMPs are thought to be of otolith origin. Evidence supporting this view was given by Sheykholeslami and Kaga (2002) who showed that VEMP responses were present in subjects with normal otolith organs but absent in those with genetic pathologies that affected both the cochlear and the semi-circular canals. It is possible to record VEMPs from the cervical muscles (cVEMPs) or the ocular muscles (oVEMPs). Both oVEMPs and cVEMPs can also be elicited by non acoustic stimulation, including bone conduction vibration and electrical stimulation. Vestibular end organs respond to air conducted sound and vibration stimuli with different patterns, and may indicate the integrity of different parts of the vestibular system and different neural pathways. The utricle is particularly sensitive to bone conduction vibration (BCV), as demonstrated by Curthoys et al. (2006) who observed that utricular irregular neurons are sensitive to BCV at low levels. Since the first studies of cVEMPs by Colebatch and Halmagyi (1992), there have been numerous developments in the understanding and knowledge of VEMPs resulting in the development of the methodology for VEMPs elicited by air conduction (AC) stimuli. In contrast, protocols for measuring VEMPs evoked by BCV are less well established. Halmagyi (2010) suggested that the lack of understanding of the ideal stimulus for VEMPs evoked by BCV is problematic since the application, location, and characteristics of the stimulus affect the measured properties of the VEMP, such as latency and amplitude. Bone conduction stimuli for eliciting VEMPs include skull taps, conventional bone oscillators, and electro-mechanical vibration from small vibrators (or mini-shakers). It has been observed that using skull taps can present difficulties controlling the stimulus intensity (Brantberg et al., 2008; Iwasaki et al., 2008), as well as producing problems with ringing of the skull, linked to the resonance and anti-resonance properties of the skull. Furthermore, clinical bone oscillators, such as the B71 have been found to provide inadequate stimulation to elicit reliable VEMP responses (Iwasaki et al., 2008). A hand-held shaker is currently the preferred method of providing BCV stimuli, since it can provide more precise and directionally specific accelerations of the head with minimal ringing in comparison to its earlier counterparts (Todd et al., 2008a). The characteristics of bone conducted vibration stimuli, including the direction of excitation (Rosengren et al., 2009) and the frequency of excitation (Todd et al., 2008a,b, 2009a,b), affect the VEMP waveform. The oVEMP response also depends on the properties of the skin where the stimulus is applied, as demonstrated by Jombik et al. (2011). They found that oVEMP amplitudes were greater when stimuli were applied at the hairline than when stimuli were applied at the inion. This may be because the skin has different compliance at different locations. The influence of tissue compliance at the location of contact with vibration can be eliminated by presenting vibration stimuli to the teeth. A method of measuring head vibration has been developed using a bite-bar (Griffin, 1975) and is used to quantify the transmission of vibration from seat to the head in studies of biodynamic responses to whole-body vibration (e.g., Kitazaki and Griffin, 1998; Matsumoto and Griffin, 1998). A bite-bar may also provide improved coupling between a shaker and the skull. Application of vibration to the teeth may involve less attenuation of the vibration by soft tissue before it reaches the skull and the vestibular end organs and so improve the oVEMP response. To our knowledge, the process of applying vibration to the teeth to elicit oVEMPs has not previously been investigated. The skull has a complex response to acceleration, moving in both translation and rotation when vibration is applied at a single location. The primary direction of head acceleration may
correspond to the direction of movement of the vibratory stimulus (Jombik et al., 2011), but acceleration in other axes may contribute to the oVEMP response. Applying vibration directly to the teeth in the midsagittal plane may help to control motion of the skull. One aspect of vibration-induced VEMPs that has received limited attention is the effect of the duration of the stimulus on the response. Todd et al. (2009a) found that the oVEMP appears to act to oppose the vibration acceleration applied by a shaker. Such a compensatory response differs from a reflex response that occurs above a reflex threshold, such as the cVEMP, where the characteristics of the response do not reflect the stimulus applied but are primarily an onset response. The cVEMP response does not mirror the properties of the stimulation applied, but the oVEMP does appear to mirror (oppose) the applied acceleration. If this is the case then the oVEMP response duration should increase with increasing stimulus duration. In this study we explore the effect of stimulus duration on response duration. A one cycle stimulus, as used in some previous studies, will have poor frequency specificity because it contains frequencies above and below the nominal frequency (i.e., spectral splatter), whereas a longer stimulus with a greater concentration of motion at a single frequency may improve ability to target the vestibular end organs with specific frequencies of vibration. This experimental study was designed to investigate how the characteristics of vibration stimuli affect oVEMP responses. We aimed to answer the following questions: (i) Can the method of stimulus application for vibration elicited oVEMPs be improved by applying stimulation to the teeth? (ii) How does more direct application of the stimulus affect the morphology of the recorded oVEMP responses? (iii) What are the effects of stimulus duration on the recorded oVEMP response? 2. Methods 2.1. Subjects Ten subjects were recruited via opportunistic sampling yielding 6 females and 4 males. The mean subject age was 27 years (range = 22–53, SD = 9.42). Inclusion criteria specified that the participants must be aged 18–60 years with self-reported normal balance function and no dental prosthetics, history of vestibular conditions, eye conditions, or eye surgery. All subjects completed the testing within one session. The study was approved by the Institute of Sound and Vibration Research Human Experimentation Safety and Ethics Committee. 2.2. Electrophysiological measurement of oVEMPs A single channel electrically isolated biological amplifier (Cambridge Electronic Design [CED] 1902) was employed to record electrophysiological signals, with the recording electrodes connected to the amplifier via a battery-powered four-channel headstage electrode adaptor box (CED, 1902-10). The amplifier was set with a band-pass filter (30–3000 Hz), with a 50 Hz notch filter, and a gain of 1000. A laboratory host interface (CED, Micro 1401) was used to receive input from the biological amplifier and also to provide output to the Vibrotactile Perception Meter (VPM) via an external attenuator. The attenuator (Hatfield, attenuator type 687/ E) could be manually adjusted by the experimenter to adjust the gain of the signal going to the VPM and hence the applied acceleration. Standard clinical electrodes were attached to the skin using a bipolar electrode montage; the ground electrode was applied to the forehead, the inverting electrode was located 1 cm inferior to centre of the eye and non-inverting electrode was placed 2 cm below the inverting electrode on the cheek. All recordings were single channel. The electrical impedance relative to the ground electrode
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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was checked prior to commencing measurements and at the halfway point during a comfort break, to ensure they did not exceed 6 kO. The recording side (right or left eye) was alternated between participants to avoid bias, hence five subjects underwent right sided recordings, and five subjects underwent left sided recordings. 2.3. Application of acceleration Vibration tone burst stimuli were generated in Matlab and exported to the CED ‘signal’ software for presentation. Stimuli were presented using the applicator of an HVLab Vibrotactile Perception Meter containing an electrodynamic shaker (Gearing and Watson). The VPM is well suited to oVEMP measurement as it provides monitoring of the force level applied to the head. For the measurements reported here the application force was maintained at 10 N. The VPM also gives a measurement of the acceleration at the application point, so the drive voltage could be adjusted to give the desired head acceleration. Two HVLab applicators were employed in the study (see Fig. 1). One was set up for the application of vibration to the head and was adjusted so that the application probe and force plate were slightly raised to assist precise placement of the vibrating probe on the skin. The second applicator was customised to apply vibration to the teeth. The top of the applicator and central plastic application probe were removed, so that a metal bar could be attached to the vibrator, with an aluminium bite-bar attached to this metal bar. The bite-bar was designed so it could be rotated so as to apply vibration to the teeth in different directions. For participant comfort and hygiene, the bite-bar was covered with dental compound moulded for each participant. Within both applicators there were accelerometers (PCB model 355B03) that allowed control of the level of vibration applied to the head or the teeth. The convention used for the direction of applied acceleration was: x-axis (front– back relative to the subject’s head), y-axis (side-to-side), and z-axis (up down). Head positions (Fz and Cz) are described using the 10:20 convention (Da Silva and Niedernever, 2012). 2.4. Stimuli The stimuli consisted of 100-Hz tone bursts generated with a sample rate of 10 kHz and a repetition rate of 5 per second. This was based on previous findings that 100 Hz elicits strong vibration
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induced oVEMPs (Todd et al., 2008b). For each measurement, 150 epochs were recorded. Five different stimulus durations were used to elicit oVEMP responses, consisting of 1, 4, 6, 10, and 18 cycles. The shortest one-cycle duration (10 ms) was identical to that used in previous oVEMP small shaker studies (Todd et al., 2008a, 2008b). The additional durations are configurations of tone bursts with 1cycle linear onset and offset ramps and with a binary increase in plateau times (1:2:1, 1:4:1, etc.). A 3.92 ms 2 r.m.s. (0.4 g) sinusoidal acceleration was applied to the head and teeth using the shakers, except the sideward teeth application was reduced by the attenuator to 0.2 g (see below). The amplitude of the acceleration was monitored in CED ‘signal’ software, and the attenuation was increased or decreased as necessary to obtain the target acceleration. 2.5. Pilot study During piloting it was established that repeatable oVEMP responses could be evoked in all three axes to 0.4 g acceleration. However, it was noted that whilst application of 0.4 g acceleration in upwards (z-axis) and frontal (x-axis) directions was acceptable to subjects, this magnitude in the sideways (y-axis) direction resulted in some discomfort; hence the acceleration was reduced for the sideways applications from 0.4 to 0.2 g. Accelerometers were used to measure the head motion. Due to the complex nature of the skull, it is difficult to measure accurately the direction and magnitude of acceleration caused by the stimuli. It was decided that the best location for measuring the response with the external accelerometer was at the teeth; whilst this was possible for the head applications, it would not be achievable when using the minishaker at the teeth since the external accelerometer would merely measure the input stimulus rather than the response of the skull. Consequently, when stimuli were applied to the head, the external accelerometer was attached to the teeth using a standard bite-bar, and when applying the stimuli at the teeth via the bite-bar, the external accelerometer was taped onto the participant’s forehead. Pilot results were not always consistent with a simple relationship between the direction of acceleration applied to the head and the resultant head motion. Shaker locations at Cz and the inion resulted in maximum head accelerations in the z-axis. Application of the shaker at Fz and the mastoid resulted in maximum acceleration in the x-axis. We chose not to use the mastoid condition in the main study as the resulting head motion appeared to be complex, although this contrasts with the findings of Todd et al. (2008a) who report that application of a shaker at the mastoid produces primarily y-axis motion. For bite-bar application of vibration, sideways acceleration caused maximum motion in the lateral, y-axis. Upwards and frontal acceleration both caused greatest motion in the z-axis. 2.6. Test conditions A repeated measures design was chosen. The experimental conditions are shown in Table 1. In total 16 conditions were tested:
Fig. 1. The two mini-shakers. The applicator on the right is the conventional minishaker used for head applications. The raised black application probe and force plate can be seen on the lid of the mini-shaker. Whilst, the applicator on the left is the customised mini-shaker for use with teeth applications. Shown here in the bitebar up position, however the screws in the metal block could be removed to change the orientation of the aluminium bite-bar for the front and side applications.
(a) To explore the effect of stimulus duration, oVEMP responses were measured using 1-, 4-, 6-, 10- and 18-cycle stimulus durations at two positions: (i) x-axis vibration applied at Fz (forehead) on the head and (ii) z-axis acceleration applied to the teeth via the bite-bar. All measurements were made with eyes elevated. (b) To check the responses were of physiological origin, the two 6-cycle conditions in (a) were repeated with eyes looking forward (not elevated).
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Table 1 Summary of the experimental conditions used for the study. Applicator type
Position/direction
Subject condition
Gaze direction
Number of measurements
Stimulus duration (cycles)
Handheld Bitebar Handheld Handheld Bitebar Bitebar Handheld Bitebar
Fz Upwards (z) Cz Inion Sideways (y) Frontal (x) Fz Upwards (z)
Supine at 30° Sitting Sitting Leaning forwards Sitting Sitting Supine at 30° Sitting
Upwards Upwards Upwards Upwards Upwards Upwards Frontal Frontal
6 1 1 1 6 1 1 1
1, 4, 6, 10, 18 1, 4, 6, 10, 18 6 6 6 6 6 6
shaker on head shaker on head shaker on head
shaker on head
elevate their gaze by 20° by staring at the target. The inclusion of a control condition of eyes straight ahead in two conditions was to confirm that the responses had a physiological origin as it is know that the oVEMP increases with gaze elevation (Rosengren et al., 2010). A Latin square was used for randomisation of the measurement conditions. When applying vibration directly to the head, the VPM was hand-held and applied by the experimenter. For application to each of the three head positions, subjects were positioned so that gravity would aid the application force; this approach was employed after pilot studies found that different positions worked well to ensure that the appropriate force was applied throughout the measurements. This meant that for vibration applied at Fz, participants lay supine on a medical couch raised by 30°. For vibration applied at Cz, participants sat comfortably in a chair looking straight ahead, and for vibration applied at the inion they sat in the chair but leant forward so their forehead rested on their arms placed on a desk. When applying vibration with the bite-bar, the VPM applicator was held by participants who were instructed to bite into the dental compound while holding the applicator so that there was no downward or upward force on the metal rod that attached the bite-bar to the shaker.
2.7. Response analysis
Fig. 2. Diagram of location of mini-shaker positioning for teeth applications. The mini-shaker was applied at the teeth using the customised bite-bar in three orientations, up, front and side. These positions are illustrated in (a, b and c) respectively. The blue rectangle represents the customised bite-bar and dental compound, whilst the red arrow represents the motion of the metal rod to which the bite-bar was attached, and thus denotes the way in which acceleration was applied to the teeth. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
(c) To explore the effect of stimulus direction and minishaker location on the responses, the 6-cycle stimulus was additionally applied to the head via the hand-held shaker at the vertex (Cz) and the inion, and to the teeth via the bite-bar in both frontal and sideways directions (Fig. 2). Hence, in total [including the 6-cycle conditions from part (a)], the 6-cycle stimulation was applied in three different directions on both the head and teeth. These measurements were made with eyes elevated. During all measurements, subjects were advised to relax as much as possible. A target for visual fixation was placed approximately 1.5 m in front of the participants and 20° above the horizontal. In all but two control conditions, subjects were asked to
All oVEMP responses were analysed to determine the latency of the first three peaks, the peak-to-peak amplitude of the second peak and the total duration of the response. The experimenter identified the first three peaks and troughs of the oVEMP response so that the latency of each peak could be read. The peak-to-peak amplitude value was calculated from the difference between the positive peak following the first negative trough, to the following negative trough; this second peak was used as it was consistently the largest of the first three peaks. To calculate the duration of the response, the oVEMP was marked at the first and final peak and these two values used to calculate the total duration of the response. The quality of responses was determined using the F value at a single point [Fsp] quality metric (Elberling and Don, 1984). The Fsp quality metric compares the variance (power) of the averaged response to an estimate of the noise derived from single point variation across epochs to give a value that increases as the signal-to-noise ratio increases. The Fsp values were calculated in MATLAB, with an analysis time window 30–50 ms post stimulus and a single point set at 40 ms (see Elberling and Don, 1984 for a definition of the method). Repeated measures analysis of variance (ANOVA) with post hoc analysis or repeated measures t-tests were used for most statistical analysis, with Pearson’s r correlation coefficient to identify relationships between data. For non-parametric data, Friedman’s ANOVA and post hoc Wilcoxon tests were used.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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3. Results Example waveforms recorded from one subject using a six cycle stimulus are shown in Fig. 3. In general, the vibration stimulus was well tolerated, although one subject withdrew in the very early stages of the experiment as they did not like the sensation of vibration on their teeth, so another participant was recruited as a replacement. All participants experienced all 16 conditions in the planned order, but some individual measurements required a repeat, such as when a constant force was not maintained or the applicator slipped, or there was no observable oVEMP response. If the physiological response was not seen in the trace following the repeat it was recorded that no oVEMP was measurable. Three of the participants had no measurable oVEMP responses in one or more condition, all when the vibration was applied directly to the head with the hand-held shaker. In each part of the analysis, subjects with missing data were excluded. One subject did not have any measurable responses with the hand-held shaker. Two further subjects had no Fz response for either the 1or 10-cycle stimuli. This meant that nine subjects were included in the analysis of stimulus position and seven subjects in the analysis of the effect of stimulus duration.
4. Amplitude of oVEMP responses: effects of stimulus location and stimulus duration Fig. 4 shows mean peak to peak amplitudes of responses to the 6-cycle stimulus presented directly to the head at three positions and via the bite-bar in each of the three directions. Repeated measures analysis of variance (RMANOVA) with one within subject factor of position (with six different levels for each minishaker position) was used to compare the head and bite-bar positions for the 6-cycle stimulus duration. A one-tailed test was used as it was hypothesized that the bite-bar would increase the response amplitude due to better coupling of the vibration to the head. The main analysis identified that the type of stimulation had a significant effect on the amplitude of the response (p < 0.001 onetailed). In post-hoc t-tests, the peak to peak amplitudes measurements from the bite-bar conditions were not significantly different from each other and the measurements from the hand held shaker positions were not significantly different from each other. The three measurements from the bite-bar and the three measurements from the hand-held shaker were combined and averaged for a further analysis. By doing this, the t-test only compared two means (combined head applications to combined teeth applications) rather than several, thus preventing the need to adjust for multiple comparisons. The mean peak to peak amplitude data for bite-bar and hand-held shaker stimulation are shown in Table 2. In a dependant t-test the mean response amplitude was significantly smaller for application on the head than for application to the teeth p < 0.01 (one-tailed), with amplitude approximately double with tooth application. Fig. 5 shows mean peak-to-peak amplitude of responses as a function of both stimulus duration and type of stimulation (either Fz with the hand-held shaker or vertical acceleration applied via the bite-bar). A RMANOVA applied with factors of stimulus duration and type of stimulation showed that the location of the minishaker had a significant effect on the response amplitude (p < 0.05). Overall stimulus duration did not have a significant effect on the response amplitude. However, on inspection it appeared that the effect of duration on responses was different for the hand-held shaker than the bite-bar. Therefore separate RMANOVAs were conducted that showed a significant effect of
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duration using the hand-held shaker (p < 0.001), but no significant effect of duration for the bite-bar data. The effect of duration for the hand-held shaker can be explained from the low amplitude of the response to the 1 cycle stimulus. Dependent paired t-tests were used to compare the response to the 1-cycle stimulus duration with the other four stimulus durations in both positions. Bonferroni adjustments for multiple comparisons meant that the significance level was adjusted to p < 0.0125. For applications of vibration at Fz, the 1-cycle stimulus had a significantly smaller mean amplitude response compared to all other stimulus durations. In comparison, for applications of vibration at the teeth, no significant differences were found between the 1-cycle stimulus duration and the other conditions.
5. Onset latency of oVEMP responses: effects of stimulus location The location of application of vibration had a significant effect on the onset latency of the oVEMP response (p < 0.01). Examples of changes in response onset can be seen in Fig. 3. For example the onset latency of the bite bar response to x stimulation (lower right) is earlier than that to y stimulation (lower middle). This may represent a change in the phase of otolith stimulation as position and type of stimulation varies. Post hoc pair-wise comparisons with Bonferroni adjustments for multiple comparisons, revealed that the mean latencies of peak one at Fz (M = 0.023, S.E = 0.002) and at Cz (M = 0.022, S.E = 0.00) were both significantly greater (p < 0.05 two tailed) than the latency of peak one at the bite-bar with sideways (y-axis) application (M = 0.016, S.E = 0.001).
6. Duration of oVEMP response: effect of stimulus duration Fig. 6 shows the effect of stimulus duration on responses from one subject for two stimulations (x-axis at Fz and z-axis with the bite-bar). Clearly response duration increases with stimulus length. To investigate the association between the stimulus duration and the response duration, the data from two stimulations (x-axis at Fz and z-axis with the bite-bar) were grouped together. The response durations from all subjects, where a measurable response was able to be recorded, were averaged to give one mean value for response duration (at each stimulus duration) for the two positions. The analysis time window was not long enough to allow the final peak of the response to be measured for the 18-cycle stimuli. The mean duration of the response had a strong positive association with the duration of the stimulus (R2 = 0.9766), Pearson correlation coefficient r = 0.98, p < 0.01 (one tailed).
7. Quality of the oVEMP responses: effect of eye position, stimulus duration, and location of application of vibration Quality values from an Fsp analysis (Elberling and Don, 1984) were calculated for each oVEMP measurement in order to analyse the effect of minishaker location and stimulus duration on the quality of the oVEMP trace. The majority the data was non-parametric, so separate non-parametric Friedman’s ANOVA analysis were applied. The Fsp values varied significantly for the two independent variables of position and duration, (p < 0.001). With the application of vibration at Fz, Fsp values for both the 10-cycle (p < 0.005) and 18-cycle (p < 0.005) stimulus durations were found to be significantly greater than Fsp values recorded with the 1-cycle stimulus duration. No significant differences were identified between the Fsp values for different durations with the application of vibration at the teeth.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Fig. 3. Examples of oVEMP responses from one subject in response to the 6 cycle stimulus duration applied using the minishaker at the head in the Fz, Cz and Inion positions and at the teeth in the bitebar up, front and side positions. The x axis shows time in seconds. The y axis denotes amplitude of the response in microvolts (y axis range varies in the figures). In all responses the stimulus was introduced at 0.01 s.
Fig. 4. Mean amplitude of oVEMP responses in microvolts as a function of the minishaker position in six different positions on the head and teeth using the 6 cycle stimulus duration. The error bar represents ±1 standard error of the mean. Fz, Cz and Inion conditions indicate application of the minishaker on the head, whilst the other conditions used the bitebar.
Table 2 Mean amplitude of measured oVEMPs and mean FSP values as a function of minishaker application for combined responses from the head (Fz, Cz and Inion) and teeth (bite-bar in the up, front and side positions) locations using the 6 cycle stimulus duration.
Combined head applications Combined teeth applications
Mean quality (Fsp)
Mean amplitude (lV)
34.92 145.92
74.5 185
Fig. 5. Amplitude of oVEMP responses as a function of stimulus duration for application at the head and teeth. The error bar represents ±1 standard error of the mean. The lighter grey circles represent application of the minishaker at the head in the Fz positions, whilst the black circles signify application of the vibration at the teeth in the bitebar up position.
To compare response quality (Fsp) for vibration applied at the head to that applied via the teeth, mean Fsp values for the head application and teeth application were calculated by finding the collective mean of all three head locations and all three teeth locations. This approach meant the comparison of only two means (Fsp mean for all of the head applications versus Fsp mean for all of the teeth applications) rather than several, thus preventing the need to adjust for multiple comparisons. Mean quality (Fsp) for head and bite-bar stimulation are shown in Table 2. Using Wilcoxon paired
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Fig. 6. Example oVEMP responses from one subject to various stimulus durations applied using the hand help shaker at the head in the Fz position and using bitebar upwards stimulation. The x axis denotes time in seconds with stimulus onset at 0.01 s. The y axis denotes response amplitude in microvolts.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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comparisons, Fsp values were significantly greater (p < 0.05) for responses evoked using application at the teeth than those evoked using application at the head. Using Wilcoxon matched-paired comparisons, Fsp values were found to be significantly greater with eyes in the elevated position than straight ahead in both the Fz position (p < 0.025) and with vibration applied at the teeth in the upwards (z-axis) direction (p < 0.025), as shown in Fig. 7. 8. Discussion The location of application of vibration to the head or teeth and the direction of applied vibration has a significant effect on the amplitude, latency, and quality of the oVEMP response. The amplitude and the quality of responses to vibration applied to the teeth were considerably greater than for vibration applied at the head. Response quality measured using Fsp was significantly greater for responses evoked using vibration application at the teeth than those evoked using application of vibration to the head. This is consistent with the concept that better coupling of the vibration stimulus to the head via the teeth would results in greater stimulation of the otoliths and evoke greater responses of greater magnitude. Jombik and colleagues (2011) found that when oVEMP responses were elicited by vibration applied to the head with a hand-held shaker, the responses varied with site of stimulation. They suggest that one explanation could be that the compliance of the skin varies over the head. Applying vibration to the teeth overcomes this variation in compliance. For the current study we excluded any subjects with dental prostheses. Such a prosthesis may well be a contraindication measurements of this type. A limitation of the current study is that it only used suprathreshold stimuli. Todd et al. (2008b) explored threshold measurements using vibration-induced oVEMPs and demonstrated high sensitivity of the vestibular system to vibration. It appears that the vestibular system may be more sensitive than the auditory system to vibration at 100 Hz. It would be interesting to extend the current study to explore oVEMP thresholds using bite-bar stimulation. This study focused on the use 100-Hz tone bursts, based on previous findings that this is the best frequency for eliciting vibrationinduced oVEMPs (Todd et al., 2008b). It is also thought that at 100 Hz the head will move as a whole without compression.
Fig. 7. Mean FSP values of oVEMP responses as a function of eye position using the 6 cycle stimulus duration at Fz and at the teeth in bitebar up position. The error bar represents ±1 standard error of the mean.
Todd et al. (2009b) and Jombik et al. (2011) have similarly employed this frequency for bone conduction vibration studies. However, a number of minishaker studies have employed 500 Hz stimuli and caution should be exhibited when comparing the findings of this study to those with different frequencies (e.g. Lin and Young, 2014). In the current study, amplitude measurements were obtained by measuring the peak-to-peak amplitude of the second peak: the first positive peak following a negative trough. This approach was employed as it was consistently the largest and clearest peak to mark, reducing measurement error. However this is not the approach most commonly used in clinical work, where often only the n10 peak is measured. The amplitudes of the oVEMP responses measured in the current study are larger than those reported in similar papers using the n10 peak, which may be due to this measurement approach. It is important to note that the origin of later peaks is not fully understood, but may reflect both peripheral and central mechanisms, as suggested by Todd et al. (2009b). Recently, Gurkov and Kantner (2013) identified that there is a significant relationship between head position and amplitudes of oVEMP elicited using air conduction sound stimuli. Given that posture has been shown to influence oVEMP results (Jerin and Gurkov, 2014), this has to be taken into account as a limitation of the current study when comparing the oVEMP results for stimulation at the head to those using the bite bar (as the subject was in different positions for the two measurements). However, a doubling in response amplitude between head and bite-bar stimulation is unlikely to be explained only by posture effects. As air conduction sound and bone conduction vibration are thought to stimulate the otolith organs in different ways and may be selective for different end organs (Todd et al., 2009a), further exploration of the effects of position on BCV oVEMP measurements is required. A not unexpected issue identified from pilot work for this study is that there is a complex relationship between the acceleration applied to the head and the motion of the head. This is also an area for further study. Few previous studies have explored the effects of stimulus type on BCV oVEMPs. The current study investigated how oVEMP responses were affected by stimulus duration and shows that stimulus duration affects not only the magnitude and the latency of responses, but also the duration of oVEMP responses. The shortest stimulus used in this experiment, one cycle (10-ms duration), was based on stimuli that had previously been used in other studies. However, a one-cycle stimulus has poor frequency specificity compared to a longer stimulus. With application to the head with the hand-held shaker, the one-cycle stimulus produced significantly smaller response amplitudes than the longer stimulus durations. Furthermore, the Fsp values of the oVEMP response to the one-cycle stimulus were significantly lower than for the two longest durations (10 and 18 cycles), thus confirming that stimulus duration affects the signal-to-noise ratio of the recorded response. The effect of stimulus duration has been described previously by Lim et al. (2013) who found that increased stimulus duration resulted in no significant increase in amplitude of responses for both BCV oVEMPs and cVEMPs. Their experiment was different to ours in that it utilised a 500 Hz tone burst and included BCV stimulus durations varying from 2 to 10 ms, which are notably shorter than the durations we employed for our study. Interestingly, Lim et al. (2013) suggest that there is no advantage of using BCV stimuli longer than 2 ms. However, in contrast we identified that longer durations are more robust stimuli for BCV oVEMPs. The one-cycle (10 ms) stimulus duration does not appear to be a robust stimulus to elicit vibration-induced oVEMPs when a hand-held shaker is applied to the head, since responses to longer stimulus durations are greater in amplitude and have higher signal-to-noise ratios.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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In total, a third of the responses to the 1-cycle stimulus duration at Fz were not measurable. This suggests that shorter stimulus durations applied using vibration applied directly to the head are less suited to elicit the oVEMP than longer stimulus durations. The oVEMP was measurable in response to application of vibration to the teeth in all participants, but was only measurable in response to application at Fz in 70%, Cz in 90%, and the inion in 90% of participants. It is clear that application of vibration to the teeth can be a more robust and consistent method of stimuli presentation. There is a strong positive correlation between the duration of the vibration stimulus and the duration of the OVEMP response. This suggests the oVEMP is fundamentally different from the cVEMP, and may be a compensatory response to motion of the head, rather than being a simple reflex response that occurs to a stimulus, but does not depend on stimulus waveform. This is consistent with the findings of Todd et al. (2009a), who suggest that oVEMP responses to low frequency BCV stimuli oppose the applied acceleration. A possible origin of the reflex could be the linear Vestibular Occular Reflex. In the present study, the mean response durations exceeded the mean stimulus duration for most. A possible explanation for this is anatomical ringing following stimulation. When a response mirrors the applied stimulation (as seen in Fig. 6), a non-physiological artefact such as electromagnetic coupling from the stimulator to the electrodes could be misinterpreted as a response. However response quality increased with eye eccentricity, as previously observed for the oVEMP and consistent with a response of physiological origin. 9. Conclusions The application of vibration to the teeth using a customised bite-bar resulted in oVEMP responses of greater amplitude and better quality than those evoked using the conventional application of vibration to the skin of the head. It appears that the bitebar method provides improved coupling of vibration to the skull. There has been limited exploration of the desirable stimulus characteristics for eliciting vibration-induced oVEMPs. This study suggests that a 100 Hz 1-cycle tone pip may be a poor stimulus choice for vibration-induced oVEMPs, since it evokes smaller amplitude and noisier oVEMP responses than longer 100 Hz stimulus durations. A linear relationship between the duration of the stimulus and the duration of the recorded response is consistent with the oVEMP response differing from the reflex response evident in the cVEMP. Conflict of interest
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References Brantberg K, Löfqvist L, Westin M, Tribukait A. Skull tap induced vestibular evoked myogenic potentials: an ipsilateral vibration response and a bilateral head acceleration response? Clin Neurophysiol 2008;119:2363–9. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation J Neurol 1992;42:1635–6. Curthoys I, Kim J, McPhedran S, Camp A. Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig. Exp Brain Res 2006;175:256–67. Elberling C, Don M. Quality estimation of averaged auditory brainstem responses. Scand Audiol 1984;13:219–28. Griffin MJ. Vertical vibration of seated subjects: effects of posture, vibration level and frequency. Aviat Space Environ Med 1975;46:269–76. Gurkov R, Kantner C. Modulation of oVEMP amplitudes by lateral head tilts. Clin Neurophysiol 2013;124:1911–21. Halmagyi G. Vestibular evoked myogenic potentials – we live in interesting times. Clin Neurophysiol 2010;121:631–3. Iwasaki S, Smulders Y, Burgess A, McGarvie L, MacDougall H, Halmagyi G, et al. Ocular vestibular evoked myogenic potentials to bone conducted vibration of the midline forehead at Fz in healthy subjects. Clin Neurophysiol 2008;119:2135–47. Jerin C, Gurkov R. Posture-induced changes of ocular vestibular evoked myogenic potentials suggest a modulation by intracranial pressure. Exp Brain Res 2014;232:2273–9. Jombik P, Spodniak P, Bahyl V. Direction-dependent excitatory and inhibitory ocular vestibular-evoked myogenic potentials (oVEMPs) produced by oppositely directed accelerations along the midsagittal axis of the head. Exp Brain Res 2011;211:251–63. Kitazaki S, Griffin MJ. Resonance behaviour of the seated human body and effects of posture. J Biomech 1998;31:143–9. Lim L, Dennis D, Govender S, Colebatch J. Differential effects of duration for ocular and cervical vestibular evoked myogenic potentials evoked by air- and boneconducted stimuli. Exp Brain Res 2013;224:437–45. Lin KY, Young YH. Role of ocular VEMP test in assessing the occurrence of vertigo in otosclerosis patients. Clin Neurophysiol 2014. pii:S1388-2457(14)00188-6. Lopes Da Silva F Lopes, Niedernever E. Electroencephalography: basic principles, clinical applications, and related fields. 5th ed. Philadelphia: Lippincott Williams & Wilkins; 2012. Matsumoto Y, Griffin MJ. Movement of the upper-body of seated subjects exposed to vertical whole-body vibration at the principal resonance. J Sound Vib 1998;215:743–62. Rosengren S, Todd N, Colebatch J. Vestibular evoked myogenic potentials evoked by brief interaural head acceleration: properties and possible origin. J Appl Physiol 2009;107:841–52. Rosengren S, Welgampola M, Colebatch J. Vestibular evoked myogenic potentials: past, present and future. Clin Neurophysiol 2010;121:636–51. Sheykholeslami K, Kaga K. The otolithic organ as a receptor of vestibular hearing revealed by vestibular-evoked myogenic potentials in patients with inner ear anomalies. Hear Res 2002;165:62–7. Todd N, Rosengren S, Colebatch J. Ocular vestibular evoked myogenic potentials (oVEMPs) produced by impulsive transmastoid accelerations. Clin Neurophysiol 2008a;119:1638–51. Todd N, Rosengren S, Colebatch J. Tuning and sensitivity of the human vestibular system to low-frequency vibration Neurosci Lett 2008b;444:36–41. Todd N, Rosengren S, Colebatch J. A utricular origin of frequency tuning to lowfrequency vibration in the human vestibular system? Neurosci Lett 2009a;451:175–80. Todd N, Rosengren S, Govender S, Colebatch J. Low-frequency tuning in the human vestibular–ocular projection is determined by both peripheral and central mechanisms. Neurosci Lett 2009b;458:43–7. Tulio P. Das Ohr und die Entstehung der Sprache und Schrift. Munchen: Urban and Schwarzenberg; 1929.
None.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth Jennifer C. Parker-George ⇑, Steven L. Bell, Michael J. Griffin Institute of Sound and Vibration Research, University of Southampton, United Kingdom
a r t i c l e
i n f o
Article history: Accepted 17 February 2015 Available online xxxx Keywords: Vestibular Otolith Vestibular evoked potentials OVEMP Vibration
h i g h l i g h t s This study investigates if applying stimulation directly to the teeth improves measurement of the
vibration-induced oVEMP. Applying 100-Hz vibration tone pips directly to the teeth via a customised bite-bar elicits clearer
oVEMP responses than direct application to the head. The quality and amplitude of vibration-induced oVEMPs is dependent on stimulus characteristics.
a b s t r a c t Objectives: This study investigated whether the method for eliciting vibration-induced oVEMPs could be improved by applying vibration directly to the teeth, and how vibration-induced oVEMP responses depend on the duration of the applied vibration. Methods: In 10 participants, a hand-held shaker was used to present 100-Hz vibration tone pips to the teeth via a customised bite-bar or to other parts of the head. oVEMP potentials were recorded in response to vibration in three orthogonal directions and five stimulus durations (10–180 ms). The oVEMP responses were analysed in terms of the peak latency onset, peak-to-peak amplitude, and the quality of the trace. Results: Vibration applied to the teeth via the bite-bar produced oVEMPs that were more consistent, of higher quality and of greater amplitude than those evoked by vibration applied to the head. Results: Longer duration stimuli produced longer duration oVEMP responses. Results: One cycle duration stimuli produced responses that were smaller in amplitude and lower quality than the longer stimulus durations. Conclusions: Application of vibration via the teeth using a bite-bar is an effective means of producing oVEMPs. Conclusions: A 1-cycle stimulus is not optimal to evoke an oVEMP because it produces less robust responses than those of longer stimulus duration. Conclusions: A positive relationship between the duration of the stimulus and the response is consistent with the notion that the vibration-induced oVEMP is an oscillatory response to the motion of the head, rather than being a simple reflex response that occurs when the stimulus exceeds a threshold level of stimulation. Significance: Applying acceleration to the teeth through a bite-bar elicits clearer oVEMP responses than direct application to other parts of the head and has potential to improve clinical measurements. A 100-Hz 1-cycle stimulus produces less robust oVEMP responses than longer 100-Hz stimuli. Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction
⇑ Corresponding author at: 22 Cinderhill Way, Ruardean, Gloucestershire, GL17 9TQ, United Kingdom. Tel.: +44 7974481896. E-mail address: [email protected] (J.C. Parker-George).
Vestibular evoked myogenic potentials (VEMPs) are thought to be a measure of reflexive changes in muscle tone in response to the activation of the vestibular system. VEMPs are most commonly
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Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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elicited using a high level acoustic stimulus, with the acoustic sensitivity of the vestibular system first described by Tulio (1929). VEMPs are thought to be of otolith origin. Evidence supporting this view was given by Sheykholeslami and Kaga (2002) who showed that VEMP responses were present in subjects with normal otolith organs but absent in those with genetic pathologies that affected both the cochlear and the semi-circular canals. It is possible to record VEMPs from the cervical muscles (cVEMPs) or the ocular muscles (oVEMPs). Both oVEMPs and cVEMPs can also be elicited by non acoustic stimulation, including bone conduction vibration and electrical stimulation. Vestibular end organs respond to air conducted sound and vibration stimuli with different patterns, and may indicate the integrity of different parts of the vestibular system and different neural pathways. The utricle is particularly sensitive to bone conduction vibration (BCV), as demonstrated by Curthoys et al. (2006) who observed that utricular irregular neurons are sensitive to BCV at low levels. Since the first studies of cVEMPs by Colebatch and Halmagyi (1992), there have been numerous developments in the understanding and knowledge of VEMPs resulting in the development of the methodology for VEMPs elicited by air conduction (AC) stimuli. In contrast, protocols for measuring VEMPs evoked by BCV are less well established. Halmagyi (2010) suggested that the lack of understanding of the ideal stimulus for VEMPs evoked by BCV is problematic since the application, location, and characteristics of the stimulus affect the measured properties of the VEMP, such as latency and amplitude. Bone conduction stimuli for eliciting VEMPs include skull taps, conventional bone oscillators, and electro-mechanical vibration from small vibrators (or mini-shakers). It has been observed that using skull taps can present difficulties controlling the stimulus intensity (Brantberg et al., 2008; Iwasaki et al., 2008), as well as producing problems with ringing of the skull, linked to the resonance and anti-resonance properties of the skull. Furthermore, clinical bone oscillators, such as the B71 have been found to provide inadequate stimulation to elicit reliable VEMP responses (Iwasaki et al., 2008). A hand-held shaker is currently the preferred method of providing BCV stimuli, since it can provide more precise and directionally specific accelerations of the head with minimal ringing in comparison to its earlier counterparts (Todd et al., 2008a). The characteristics of bone conducted vibration stimuli, including the direction of excitation (Rosengren et al., 2009) and the frequency of excitation (Todd et al., 2008a,b, 2009a,b), affect the VEMP waveform. The oVEMP response also depends on the properties of the skin where the stimulus is applied, as demonstrated by Jombik et al. (2011). They found that oVEMP amplitudes were greater when stimuli were applied at the hairline than when stimuli were applied at the inion. This may be because the skin has different compliance at different locations. The influence of tissue compliance at the location of contact with vibration can be eliminated by presenting vibration stimuli to the teeth. A method of measuring head vibration has been developed using a bite-bar (Griffin, 1975) and is used to quantify the transmission of vibration from seat to the head in studies of biodynamic responses to whole-body vibration (e.g., Kitazaki and Griffin, 1998; Matsumoto and Griffin, 1998). A bite-bar may also provide improved coupling between a shaker and the skull. Application of vibration to the teeth may involve less attenuation of the vibration by soft tissue before it reaches the skull and the vestibular end organs and so improve the oVEMP response. To our knowledge, the process of applying vibration to the teeth to elicit oVEMPs has not previously been investigated. The skull has a complex response to acceleration, moving in both translation and rotation when vibration is applied at a single location. The primary direction of head acceleration may
correspond to the direction of movement of the vibratory stimulus (Jombik et al., 2011), but acceleration in other axes may contribute to the oVEMP response. Applying vibration directly to the teeth in the midsagittal plane may help to control motion of the skull. One aspect of vibration-induced VEMPs that has received limited attention is the effect of the duration of the stimulus on the response. Todd et al. (2009a) found that the oVEMP appears to act to oppose the vibration acceleration applied by a shaker. Such a compensatory response differs from a reflex response that occurs above a reflex threshold, such as the cVEMP, where the characteristics of the response do not reflect the stimulus applied but are primarily an onset response. The cVEMP response does not mirror the properties of the stimulation applied, but the oVEMP does appear to mirror (oppose) the applied acceleration. If this is the case then the oVEMP response duration should increase with increasing stimulus duration. In this study we explore the effect of stimulus duration on response duration. A one cycle stimulus, as used in some previous studies, will have poor frequency specificity because it contains frequencies above and below the nominal frequency (i.e., spectral splatter), whereas a longer stimulus with a greater concentration of motion at a single frequency may improve ability to target the vestibular end organs with specific frequencies of vibration. This experimental study was designed to investigate how the characteristics of vibration stimuli affect oVEMP responses. We aimed to answer the following questions: (i) Can the method of stimulus application for vibration elicited oVEMPs be improved by applying stimulation to the teeth? (ii) How does more direct application of the stimulus affect the morphology of the recorded oVEMP responses? (iii) What are the effects of stimulus duration on the recorded oVEMP response? 2. Methods 2.1. Subjects Ten subjects were recruited via opportunistic sampling yielding 6 females and 4 males. The mean subject age was 27 years (range = 22–53, SD = 9.42). Inclusion criteria specified that the participants must be aged 18–60 years with self-reported normal balance function and no dental prosthetics, history of vestibular conditions, eye conditions, or eye surgery. All subjects completed the testing within one session. The study was approved by the Institute of Sound and Vibration Research Human Experimentation Safety and Ethics Committee. 2.2. Electrophysiological measurement of oVEMPs A single channel electrically isolated biological amplifier (Cambridge Electronic Design [CED] 1902) was employed to record electrophysiological signals, with the recording electrodes connected to the amplifier via a battery-powered four-channel headstage electrode adaptor box (CED, 1902-10). The amplifier was set with a band-pass filter (30–3000 Hz), with a 50 Hz notch filter, and a gain of 1000. A laboratory host interface (CED, Micro 1401) was used to receive input from the biological amplifier and also to provide output to the Vibrotactile Perception Meter (VPM) via an external attenuator. The attenuator (Hatfield, attenuator type 687/ E) could be manually adjusted by the experimenter to adjust the gain of the signal going to the VPM and hence the applied acceleration. Standard clinical electrodes were attached to the skin using a bipolar electrode montage; the ground electrode was applied to the forehead, the inverting electrode was located 1 cm inferior to centre of the eye and non-inverting electrode was placed 2 cm below the inverting electrode on the cheek. All recordings were single channel. The electrical impedance relative to the ground electrode
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was checked prior to commencing measurements and at the halfway point during a comfort break, to ensure they did not exceed 6 kO. The recording side (right or left eye) was alternated between participants to avoid bias, hence five subjects underwent right sided recordings, and five subjects underwent left sided recordings. 2.3. Application of acceleration Vibration tone burst stimuli were generated in Matlab and exported to the CED ‘signal’ software for presentation. Stimuli were presented using the applicator of an HVLab Vibrotactile Perception Meter containing an electrodynamic shaker (Gearing and Watson). The VPM is well suited to oVEMP measurement as it provides monitoring of the force level applied to the head. For the measurements reported here the application force was maintained at 10 N. The VPM also gives a measurement of the acceleration at the application point, so the drive voltage could be adjusted to give the desired head acceleration. Two HVLab applicators were employed in the study (see Fig. 1). One was set up for the application of vibration to the head and was adjusted so that the application probe and force plate were slightly raised to assist precise placement of the vibrating probe on the skin. The second applicator was customised to apply vibration to the teeth. The top of the applicator and central plastic application probe were removed, so that a metal bar could be attached to the vibrator, with an aluminium bite-bar attached to this metal bar. The bite-bar was designed so it could be rotated so as to apply vibration to the teeth in different directions. For participant comfort and hygiene, the bite-bar was covered with dental compound moulded for each participant. Within both applicators there were accelerometers (PCB model 355B03) that allowed control of the level of vibration applied to the head or the teeth. The convention used for the direction of applied acceleration was: x-axis (front– back relative to the subject’s head), y-axis (side-to-side), and z-axis (up down). Head positions (Fz and Cz) are described using the 10:20 convention (Da Silva and Niedernever, 2012). 2.4. Stimuli The stimuli consisted of 100-Hz tone bursts generated with a sample rate of 10 kHz and a repetition rate of 5 per second. This was based on previous findings that 100 Hz elicits strong vibration
3
induced oVEMPs (Todd et al., 2008b). For each measurement, 150 epochs were recorded. Five different stimulus durations were used to elicit oVEMP responses, consisting of 1, 4, 6, 10, and 18 cycles. The shortest one-cycle duration (10 ms) was identical to that used in previous oVEMP small shaker studies (Todd et al., 2008a, 2008b). The additional durations are configurations of tone bursts with 1cycle linear onset and offset ramps and with a binary increase in plateau times (1:2:1, 1:4:1, etc.). A 3.92 ms 2 r.m.s. (0.4 g) sinusoidal acceleration was applied to the head and teeth using the shakers, except the sideward teeth application was reduced by the attenuator to 0.2 g (see below). The amplitude of the acceleration was monitored in CED ‘signal’ software, and the attenuation was increased or decreased as necessary to obtain the target acceleration. 2.5. Pilot study During piloting it was established that repeatable oVEMP responses could be evoked in all three axes to 0.4 g acceleration. However, it was noted that whilst application of 0.4 g acceleration in upwards (z-axis) and frontal (x-axis) directions was acceptable to subjects, this magnitude in the sideways (y-axis) direction resulted in some discomfort; hence the acceleration was reduced for the sideways applications from 0.4 to 0.2 g. Accelerometers were used to measure the head motion. Due to the complex nature of the skull, it is difficult to measure accurately the direction and magnitude of acceleration caused by the stimuli. It was decided that the best location for measuring the response with the external accelerometer was at the teeth; whilst this was possible for the head applications, it would not be achievable when using the minishaker at the teeth since the external accelerometer would merely measure the input stimulus rather than the response of the skull. Consequently, when stimuli were applied to the head, the external accelerometer was attached to the teeth using a standard bite-bar, and when applying the stimuli at the teeth via the bite-bar, the external accelerometer was taped onto the participant’s forehead. Pilot results were not always consistent with a simple relationship between the direction of acceleration applied to the head and the resultant head motion. Shaker locations at Cz and the inion resulted in maximum head accelerations in the z-axis. Application of the shaker at Fz and the mastoid resulted in maximum acceleration in the x-axis. We chose not to use the mastoid condition in the main study as the resulting head motion appeared to be complex, although this contrasts with the findings of Todd et al. (2008a) who report that application of a shaker at the mastoid produces primarily y-axis motion. For bite-bar application of vibration, sideways acceleration caused maximum motion in the lateral, y-axis. Upwards and frontal acceleration both caused greatest motion in the z-axis. 2.6. Test conditions A repeated measures design was chosen. The experimental conditions are shown in Table 1. In total 16 conditions were tested:
Fig. 1. The two mini-shakers. The applicator on the right is the conventional minishaker used for head applications. The raised black application probe and force plate can be seen on the lid of the mini-shaker. Whilst, the applicator on the left is the customised mini-shaker for use with teeth applications. Shown here in the bitebar up position, however the screws in the metal block could be removed to change the orientation of the aluminium bite-bar for the front and side applications.
(a) To explore the effect of stimulus duration, oVEMP responses were measured using 1-, 4-, 6-, 10- and 18-cycle stimulus durations at two positions: (i) x-axis vibration applied at Fz (forehead) on the head and (ii) z-axis acceleration applied to the teeth via the bite-bar. All measurements were made with eyes elevated. (b) To check the responses were of physiological origin, the two 6-cycle conditions in (a) were repeated with eyes looking forward (not elevated).
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Table 1 Summary of the experimental conditions used for the study. Applicator type
Position/direction
Subject condition
Gaze direction
Number of measurements
Stimulus duration (cycles)
Handheld Bitebar Handheld Handheld Bitebar Bitebar Handheld Bitebar
Fz Upwards (z) Cz Inion Sideways (y) Frontal (x) Fz Upwards (z)
Supine at 30° Sitting Sitting Leaning forwards Sitting Sitting Supine at 30° Sitting
Upwards Upwards Upwards Upwards Upwards Upwards Frontal Frontal
6 1 1 1 6 1 1 1
1, 4, 6, 10, 18 1, 4, 6, 10, 18 6 6 6 6 6 6
shaker on head shaker on head shaker on head
shaker on head
elevate their gaze by 20° by staring at the target. The inclusion of a control condition of eyes straight ahead in two conditions was to confirm that the responses had a physiological origin as it is know that the oVEMP increases with gaze elevation (Rosengren et al., 2010). A Latin square was used for randomisation of the measurement conditions. When applying vibration directly to the head, the VPM was hand-held and applied by the experimenter. For application to each of the three head positions, subjects were positioned so that gravity would aid the application force; this approach was employed after pilot studies found that different positions worked well to ensure that the appropriate force was applied throughout the measurements. This meant that for vibration applied at Fz, participants lay supine on a medical couch raised by 30°. For vibration applied at Cz, participants sat comfortably in a chair looking straight ahead, and for vibration applied at the inion they sat in the chair but leant forward so their forehead rested on their arms placed on a desk. When applying vibration with the bite-bar, the VPM applicator was held by participants who were instructed to bite into the dental compound while holding the applicator so that there was no downward or upward force on the metal rod that attached the bite-bar to the shaker.
2.7. Response analysis
Fig. 2. Diagram of location of mini-shaker positioning for teeth applications. The mini-shaker was applied at the teeth using the customised bite-bar in three orientations, up, front and side. These positions are illustrated in (a, b and c) respectively. The blue rectangle represents the customised bite-bar and dental compound, whilst the red arrow represents the motion of the metal rod to which the bite-bar was attached, and thus denotes the way in which acceleration was applied to the teeth. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
(c) To explore the effect of stimulus direction and minishaker location on the responses, the 6-cycle stimulus was additionally applied to the head via the hand-held shaker at the vertex (Cz) and the inion, and to the teeth via the bite-bar in both frontal and sideways directions (Fig. 2). Hence, in total [including the 6-cycle conditions from part (a)], the 6-cycle stimulation was applied in three different directions on both the head and teeth. These measurements were made with eyes elevated. During all measurements, subjects were advised to relax as much as possible. A target for visual fixation was placed approximately 1.5 m in front of the participants and 20° above the horizontal. In all but two control conditions, subjects were asked to
All oVEMP responses were analysed to determine the latency of the first three peaks, the peak-to-peak amplitude of the second peak and the total duration of the response. The experimenter identified the first three peaks and troughs of the oVEMP response so that the latency of each peak could be read. The peak-to-peak amplitude value was calculated from the difference between the positive peak following the first negative trough, to the following negative trough; this second peak was used as it was consistently the largest of the first three peaks. To calculate the duration of the response, the oVEMP was marked at the first and final peak and these two values used to calculate the total duration of the response. The quality of responses was determined using the F value at a single point [Fsp] quality metric (Elberling and Don, 1984). The Fsp quality metric compares the variance (power) of the averaged response to an estimate of the noise derived from single point variation across epochs to give a value that increases as the signal-to-noise ratio increases. The Fsp values were calculated in MATLAB, with an analysis time window 30–50 ms post stimulus and a single point set at 40 ms (see Elberling and Don, 1984 for a definition of the method). Repeated measures analysis of variance (ANOVA) with post hoc analysis or repeated measures t-tests were used for most statistical analysis, with Pearson’s r correlation coefficient to identify relationships between data. For non-parametric data, Friedman’s ANOVA and post hoc Wilcoxon tests were used.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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3. Results Example waveforms recorded from one subject using a six cycle stimulus are shown in Fig. 3. In general, the vibration stimulus was well tolerated, although one subject withdrew in the very early stages of the experiment as they did not like the sensation of vibration on their teeth, so another participant was recruited as a replacement. All participants experienced all 16 conditions in the planned order, but some individual measurements required a repeat, such as when a constant force was not maintained or the applicator slipped, or there was no observable oVEMP response. If the physiological response was not seen in the trace following the repeat it was recorded that no oVEMP was measurable. Three of the participants had no measurable oVEMP responses in one or more condition, all when the vibration was applied directly to the head with the hand-held shaker. In each part of the analysis, subjects with missing data were excluded. One subject did not have any measurable responses with the hand-held shaker. Two further subjects had no Fz response for either the 1or 10-cycle stimuli. This meant that nine subjects were included in the analysis of stimulus position and seven subjects in the analysis of the effect of stimulus duration.
4. Amplitude of oVEMP responses: effects of stimulus location and stimulus duration Fig. 4 shows mean peak to peak amplitudes of responses to the 6-cycle stimulus presented directly to the head at three positions and via the bite-bar in each of the three directions. Repeated measures analysis of variance (RMANOVA) with one within subject factor of position (with six different levels for each minishaker position) was used to compare the head and bite-bar positions for the 6-cycle stimulus duration. A one-tailed test was used as it was hypothesized that the bite-bar would increase the response amplitude due to better coupling of the vibration to the head. The main analysis identified that the type of stimulation had a significant effect on the amplitude of the response (p < 0.001 onetailed). In post-hoc t-tests, the peak to peak amplitudes measurements from the bite-bar conditions were not significantly different from each other and the measurements from the hand held shaker positions were not significantly different from each other. The three measurements from the bite-bar and the three measurements from the hand-held shaker were combined and averaged for a further analysis. By doing this, the t-test only compared two means (combined head applications to combined teeth applications) rather than several, thus preventing the need to adjust for multiple comparisons. The mean peak to peak amplitude data for bite-bar and hand-held shaker stimulation are shown in Table 2. In a dependant t-test the mean response amplitude was significantly smaller for application on the head than for application to the teeth p < 0.01 (one-tailed), with amplitude approximately double with tooth application. Fig. 5 shows mean peak-to-peak amplitude of responses as a function of both stimulus duration and type of stimulation (either Fz with the hand-held shaker or vertical acceleration applied via the bite-bar). A RMANOVA applied with factors of stimulus duration and type of stimulation showed that the location of the minishaker had a significant effect on the response amplitude (p < 0.05). Overall stimulus duration did not have a significant effect on the response amplitude. However, on inspection it appeared that the effect of duration on responses was different for the hand-held shaker than the bite-bar. Therefore separate RMANOVAs were conducted that showed a significant effect of
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duration using the hand-held shaker (p < 0.001), but no significant effect of duration for the bite-bar data. The effect of duration for the hand-held shaker can be explained from the low amplitude of the response to the 1 cycle stimulus. Dependent paired t-tests were used to compare the response to the 1-cycle stimulus duration with the other four stimulus durations in both positions. Bonferroni adjustments for multiple comparisons meant that the significance level was adjusted to p < 0.0125. For applications of vibration at Fz, the 1-cycle stimulus had a significantly smaller mean amplitude response compared to all other stimulus durations. In comparison, for applications of vibration at the teeth, no significant differences were found between the 1-cycle stimulus duration and the other conditions.
5. Onset latency of oVEMP responses: effects of stimulus location The location of application of vibration had a significant effect on the onset latency of the oVEMP response (p < 0.01). Examples of changes in response onset can be seen in Fig. 3. For example the onset latency of the bite bar response to x stimulation (lower right) is earlier than that to y stimulation (lower middle). This may represent a change in the phase of otolith stimulation as position and type of stimulation varies. Post hoc pair-wise comparisons with Bonferroni adjustments for multiple comparisons, revealed that the mean latencies of peak one at Fz (M = 0.023, S.E = 0.002) and at Cz (M = 0.022, S.E = 0.00) were both significantly greater (p < 0.05 two tailed) than the latency of peak one at the bite-bar with sideways (y-axis) application (M = 0.016, S.E = 0.001).
6. Duration of oVEMP response: effect of stimulus duration Fig. 6 shows the effect of stimulus duration on responses from one subject for two stimulations (x-axis at Fz and z-axis with the bite-bar). Clearly response duration increases with stimulus length. To investigate the association between the stimulus duration and the response duration, the data from two stimulations (x-axis at Fz and z-axis with the bite-bar) were grouped together. The response durations from all subjects, where a measurable response was able to be recorded, were averaged to give one mean value for response duration (at each stimulus duration) for the two positions. The analysis time window was not long enough to allow the final peak of the response to be measured for the 18-cycle stimuli. The mean duration of the response had a strong positive association with the duration of the stimulus (R2 = 0.9766), Pearson correlation coefficient r = 0.98, p < 0.01 (one tailed).
7. Quality of the oVEMP responses: effect of eye position, stimulus duration, and location of application of vibration Quality values from an Fsp analysis (Elberling and Don, 1984) were calculated for each oVEMP measurement in order to analyse the effect of minishaker location and stimulus duration on the quality of the oVEMP trace. The majority the data was non-parametric, so separate non-parametric Friedman’s ANOVA analysis were applied. The Fsp values varied significantly for the two independent variables of position and duration, (p < 0.001). With the application of vibration at Fz, Fsp values for both the 10-cycle (p < 0.005) and 18-cycle (p < 0.005) stimulus durations were found to be significantly greater than Fsp values recorded with the 1-cycle stimulus duration. No significant differences were identified between the Fsp values for different durations with the application of vibration at the teeth.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Fig. 3. Examples of oVEMP responses from one subject in response to the 6 cycle stimulus duration applied using the minishaker at the head in the Fz, Cz and Inion positions and at the teeth in the bitebar up, front and side positions. The x axis shows time in seconds. The y axis denotes amplitude of the response in microvolts (y axis range varies in the figures). In all responses the stimulus was introduced at 0.01 s.
Fig. 4. Mean amplitude of oVEMP responses in microvolts as a function of the minishaker position in six different positions on the head and teeth using the 6 cycle stimulus duration. The error bar represents ±1 standard error of the mean. Fz, Cz and Inion conditions indicate application of the minishaker on the head, whilst the other conditions used the bitebar.
Table 2 Mean amplitude of measured oVEMPs and mean FSP values as a function of minishaker application for combined responses from the head (Fz, Cz and Inion) and teeth (bite-bar in the up, front and side positions) locations using the 6 cycle stimulus duration.
Combined head applications Combined teeth applications
Mean quality (Fsp)
Mean amplitude (lV)
34.92 145.92
74.5 185
Fig. 5. Amplitude of oVEMP responses as a function of stimulus duration for application at the head and teeth. The error bar represents ±1 standard error of the mean. The lighter grey circles represent application of the minishaker at the head in the Fz positions, whilst the black circles signify application of the vibration at the teeth in the bitebar up position.
To compare response quality (Fsp) for vibration applied at the head to that applied via the teeth, mean Fsp values for the head application and teeth application were calculated by finding the collective mean of all three head locations and all three teeth locations. This approach meant the comparison of only two means (Fsp mean for all of the head applications versus Fsp mean for all of the teeth applications) rather than several, thus preventing the need to adjust for multiple comparisons. Mean quality (Fsp) for head and bite-bar stimulation are shown in Table 2. Using Wilcoxon paired
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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Fig. 6. Example oVEMP responses from one subject to various stimulus durations applied using the hand help shaker at the head in the Fz position and using bitebar upwards stimulation. The x axis denotes time in seconds with stimulus onset at 0.01 s. The y axis denotes response amplitude in microvolts.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
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comparisons, Fsp values were significantly greater (p < 0.05) for responses evoked using application at the teeth than those evoked using application at the head. Using Wilcoxon matched-paired comparisons, Fsp values were found to be significantly greater with eyes in the elevated position than straight ahead in both the Fz position (p < 0.025) and with vibration applied at the teeth in the upwards (z-axis) direction (p < 0.025), as shown in Fig. 7. 8. Discussion The location of application of vibration to the head or teeth and the direction of applied vibration has a significant effect on the amplitude, latency, and quality of the oVEMP response. The amplitude and the quality of responses to vibration applied to the teeth were considerably greater than for vibration applied at the head. Response quality measured using Fsp was significantly greater for responses evoked using vibration application at the teeth than those evoked using application of vibration to the head. This is consistent with the concept that better coupling of the vibration stimulus to the head via the teeth would results in greater stimulation of the otoliths and evoke greater responses of greater magnitude. Jombik and colleagues (2011) found that when oVEMP responses were elicited by vibration applied to the head with a hand-held shaker, the responses varied with site of stimulation. They suggest that one explanation could be that the compliance of the skin varies over the head. Applying vibration to the teeth overcomes this variation in compliance. For the current study we excluded any subjects with dental prostheses. Such a prosthesis may well be a contraindication measurements of this type. A limitation of the current study is that it only used suprathreshold stimuli. Todd et al. (2008b) explored threshold measurements using vibration-induced oVEMPs and demonstrated high sensitivity of the vestibular system to vibration. It appears that the vestibular system may be more sensitive than the auditory system to vibration at 100 Hz. It would be interesting to extend the current study to explore oVEMP thresholds using bite-bar stimulation. This study focused on the use 100-Hz tone bursts, based on previous findings that this is the best frequency for eliciting vibrationinduced oVEMPs (Todd et al., 2008b). It is also thought that at 100 Hz the head will move as a whole without compression.
Fig. 7. Mean FSP values of oVEMP responses as a function of eye position using the 6 cycle stimulus duration at Fz and at the teeth in bitebar up position. The error bar represents ±1 standard error of the mean.
Todd et al. (2009b) and Jombik et al. (2011) have similarly employed this frequency for bone conduction vibration studies. However, a number of minishaker studies have employed 500 Hz stimuli and caution should be exhibited when comparing the findings of this study to those with different frequencies (e.g. Lin and Young, 2014). In the current study, amplitude measurements were obtained by measuring the peak-to-peak amplitude of the second peak: the first positive peak following a negative trough. This approach was employed as it was consistently the largest and clearest peak to mark, reducing measurement error. However this is not the approach most commonly used in clinical work, where often only the n10 peak is measured. The amplitudes of the oVEMP responses measured in the current study are larger than those reported in similar papers using the n10 peak, which may be due to this measurement approach. It is important to note that the origin of later peaks is not fully understood, but may reflect both peripheral and central mechanisms, as suggested by Todd et al. (2009b). Recently, Gurkov and Kantner (2013) identified that there is a significant relationship between head position and amplitudes of oVEMP elicited using air conduction sound stimuli. Given that posture has been shown to influence oVEMP results (Jerin and Gurkov, 2014), this has to be taken into account as a limitation of the current study when comparing the oVEMP results for stimulation at the head to those using the bite bar (as the subject was in different positions for the two measurements). However, a doubling in response amplitude between head and bite-bar stimulation is unlikely to be explained only by posture effects. As air conduction sound and bone conduction vibration are thought to stimulate the otolith organs in different ways and may be selective for different end organs (Todd et al., 2009a), further exploration of the effects of position on BCV oVEMP measurements is required. A not unexpected issue identified from pilot work for this study is that there is a complex relationship between the acceleration applied to the head and the motion of the head. This is also an area for further study. Few previous studies have explored the effects of stimulus type on BCV oVEMPs. The current study investigated how oVEMP responses were affected by stimulus duration and shows that stimulus duration affects not only the magnitude and the latency of responses, but also the duration of oVEMP responses. The shortest stimulus used in this experiment, one cycle (10-ms duration), was based on stimuli that had previously been used in other studies. However, a one-cycle stimulus has poor frequency specificity compared to a longer stimulus. With application to the head with the hand-held shaker, the one-cycle stimulus produced significantly smaller response amplitudes than the longer stimulus durations. Furthermore, the Fsp values of the oVEMP response to the one-cycle stimulus were significantly lower than for the two longest durations (10 and 18 cycles), thus confirming that stimulus duration affects the signal-to-noise ratio of the recorded response. The effect of stimulus duration has been described previously by Lim et al. (2013) who found that increased stimulus duration resulted in no significant increase in amplitude of responses for both BCV oVEMPs and cVEMPs. Their experiment was different to ours in that it utilised a 500 Hz tone burst and included BCV stimulus durations varying from 2 to 10 ms, which are notably shorter than the durations we employed for our study. Interestingly, Lim et al. (2013) suggest that there is no advantage of using BCV stimuli longer than 2 ms. However, in contrast we identified that longer durations are more robust stimuli for BCV oVEMPs. The one-cycle (10 ms) stimulus duration does not appear to be a robust stimulus to elicit vibration-induced oVEMPs when a hand-held shaker is applied to the head, since responses to longer stimulus durations are greater in amplitude and have higher signal-to-noise ratios.
Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
J.C. Parker-George et al. / Clinical Neurophysiology xxx (2015) xxx–xxx
In total, a third of the responses to the 1-cycle stimulus duration at Fz were not measurable. This suggests that shorter stimulus durations applied using vibration applied directly to the head are less suited to elicit the oVEMP than longer stimulus durations. The oVEMP was measurable in response to application of vibration to the teeth in all participants, but was only measurable in response to application at Fz in 70%, Cz in 90%, and the inion in 90% of participants. It is clear that application of vibration to the teeth can be a more robust and consistent method of stimuli presentation. There is a strong positive correlation between the duration of the vibration stimulus and the duration of the OVEMP response. This suggests the oVEMP is fundamentally different from the cVEMP, and may be a compensatory response to motion of the head, rather than being a simple reflex response that occurs to a stimulus, but does not depend on stimulus waveform. This is consistent with the findings of Todd et al. (2009a), who suggest that oVEMP responses to low frequency BCV stimuli oppose the applied acceleration. A possible origin of the reflex could be the linear Vestibular Occular Reflex. In the present study, the mean response durations exceeded the mean stimulus duration for most. A possible explanation for this is anatomical ringing following stimulation. When a response mirrors the applied stimulation (as seen in Fig. 6), a non-physiological artefact such as electromagnetic coupling from the stimulator to the electrodes could be misinterpreted as a response. However response quality increased with eye eccentricity, as previously observed for the oVEMP and consistent with a response of physiological origin. 9. Conclusions The application of vibration to the teeth using a customised bite-bar resulted in oVEMP responses of greater amplitude and better quality than those evoked using the conventional application of vibration to the skin of the head. It appears that the bitebar method provides improved coupling of vibration to the skull. There has been limited exploration of the desirable stimulus characteristics for eliciting vibration-induced oVEMPs. This study suggests that a 100 Hz 1-cycle tone pip may be a poor stimulus choice for vibration-induced oVEMPs, since it evokes smaller amplitude and noisier oVEMP responses than longer 100 Hz stimulus durations. A linear relationship between the duration of the stimulus and the duration of the recorded response is consistent with the oVEMP response differing from the reflex response evident in the cVEMP. Conflict of interest
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References Brantberg K, Löfqvist L, Westin M, Tribukait A. Skull tap induced vestibular evoked myogenic potentials: an ipsilateral vibration response and a bilateral head acceleration response? Clin Neurophysiol 2008;119:2363–9. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation J Neurol 1992;42:1635–6. Curthoys I, Kim J, McPhedran S, Camp A. Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig. Exp Brain Res 2006;175:256–67. Elberling C, Don M. Quality estimation of averaged auditory brainstem responses. Scand Audiol 1984;13:219–28. Griffin MJ. Vertical vibration of seated subjects: effects of posture, vibration level and frequency. Aviat Space Environ Med 1975;46:269–76. Gurkov R, Kantner C. Modulation of oVEMP amplitudes by lateral head tilts. Clin Neurophysiol 2013;124:1911–21. Halmagyi G. Vestibular evoked myogenic potentials – we live in interesting times. Clin Neurophysiol 2010;121:631–3. Iwasaki S, Smulders Y, Burgess A, McGarvie L, MacDougall H, Halmagyi G, et al. Ocular vestibular evoked myogenic potentials to bone conducted vibration of the midline forehead at Fz in healthy subjects. Clin Neurophysiol 2008;119:2135–47. Jerin C, Gurkov R. Posture-induced changes of ocular vestibular evoked myogenic potentials suggest a modulation by intracranial pressure. Exp Brain Res 2014;232:2273–9. Jombik P, Spodniak P, Bahyl V. Direction-dependent excitatory and inhibitory ocular vestibular-evoked myogenic potentials (oVEMPs) produced by oppositely directed accelerations along the midsagittal axis of the head. Exp Brain Res 2011;211:251–63. Kitazaki S, Griffin MJ. Resonance behaviour of the seated human body and effects of posture. J Biomech 1998;31:143–9. Lim L, Dennis D, Govender S, Colebatch J. Differential effects of duration for ocular and cervical vestibular evoked myogenic potentials evoked by air- and boneconducted stimuli. Exp Brain Res 2013;224:437–45. Lin KY, Young YH. Role of ocular VEMP test in assessing the occurrence of vertigo in otosclerosis patients. Clin Neurophysiol 2014. pii:S1388-2457(14)00188-6. Lopes Da Silva F Lopes, Niedernever E. Electroencephalography: basic principles, clinical applications, and related fields. 5th ed. Philadelphia: Lippincott Williams & Wilkins; 2012. Matsumoto Y, Griffin MJ. Movement of the upper-body of seated subjects exposed to vertical whole-body vibration at the principal resonance. J Sound Vib 1998;215:743–62. Rosengren S, Todd N, Colebatch J. Vestibular evoked myogenic potentials evoked by brief interaural head acceleration: properties and possible origin. J Appl Physiol 2009;107:841–52. Rosengren S, Welgampola M, Colebatch J. Vestibular evoked myogenic potentials: past, present and future. Clin Neurophysiol 2010;121:636–51. Sheykholeslami K, Kaga K. The otolithic organ as a receptor of vestibular hearing revealed by vestibular-evoked myogenic potentials in patients with inner ear anomalies. Hear Res 2002;165:62–7. Todd N, Rosengren S, Colebatch J. Ocular vestibular evoked myogenic potentials (oVEMPs) produced by impulsive transmastoid accelerations. Clin Neurophysiol 2008a;119:1638–51. Todd N, Rosengren S, Colebatch J. Tuning and sensitivity of the human vestibular system to low-frequency vibration Neurosci Lett 2008b;444:36–41. Todd N, Rosengren S, Colebatch J. A utricular origin of frequency tuning to lowfrequency vibration in the human vestibular system? Neurosci Lett 2009a;451:175–80. Todd N, Rosengren S, Govender S, Colebatch J. Low-frequency tuning in the human vestibular–ocular projection is determined by both peripheral and central mechanisms. Neurosci Lett 2009b;458:43–7. Tulio P. Das Ohr und die Entstehung der Sprache und Schrift. Munchen: Urban and Schwarzenberg; 1929.
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Please cite this article in press as: Parker-George JC et al. Ocular vestibular evoked myogenic potentials elicited with vibration applied to the teeth. Clin Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.02.007
