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The effect of electrode positioning on the ocular vestibular evoked myogenic potential to air-conducted sound
Clinical Neurophysiology 124 (2013) 1232–1236
Contents lists available at SciVerse ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
The effect of electrode positioning on the ocular vestibular evoked myogenic potential to air-conducted sound Jaswinder S. Sandhu a,b,⇑, Stefan R. George a, Peter A. Rea b a b
Leicester Medical School, University of Leicester, Leicester LE1 9HN, UK Ear Nose and Throat Department, University Hospitals of Leicester, Leicester LE1 5WW, UK
See Editorial, pages 1051–1052
a r t i c l e
i n f o
Article history: Available online 18 January 2013 Keywords: Ocular vestibular evoked myogenic potential (oVEMP) Air-conducted sound (ACS) Electrode Montage Null-point
h i g h l i g h t s This study demonstrates that the amplitude of the oVEMP is highly sensitive to the relative positions of the active and reference electrodes. Small changes in the active electrode position result in amplitude inversion and exhibit an intermediate null-point where no response is detected. An alternative montage is proposed which avoids the null-point and furthermore enhances the oVEMP response amplitude.
a b s t r a c t Objective: To assess the effect of electrode position on the amplitude and latency of ocular vestibular evoked myogenic potentials (oVEMPs) produced by air-conducted (AC) sound with a view to optimisation of the recording paradigm. Methods: Eight otologically normal subjects (16 ears) were stimulated by 500 Hz AC tone bursts at 95 dBnHL; oVEMP traces were recorded below the eye contralateral to the acoustic stimulation. Five independent oVEMP measurements were recorded with the active electrode in equally spaced positions in the infra-orbital plane relative to a reference electrode positioned 2 cm below the lower lid in the orbital midline. These measurements included the accepted standard-montage in which the electrodes were positioned vertically above and below each other in the orbital midline. A further recording was made using a belly-tendon montage with reference to the inferior oblique muscle. Results: Of the six recording paradigms tested the largest amplitude oVEMP response was found using the belly-tendon montage with an n10 average of 5.67 ± 3.42 lV (sd). This was significantly larger than the amplitude recorded using the standard-montage (p < 0.01). With the reference electrode in the orbital midline, the position of the active electrode in the infra-orbital plane was found to significantly alter the response magnitude. As the active electrode was moved laterally the response reduced in amplitude, however when moved medially the response polarity reversed indicating the existence of a null-point at which no response was present. Conclusions: The location of oVEMP recording electrodes significantly alters the response amplitude. Whilst the standard-montage provides a reasonable method for recording oVEMPs, the belly-tendon montage results in a significantly larger amplitude response. Furthermore medial and lateral variations in the position of the active electrode using the standard-montage significantly affect the magnitude and polarity of the response. Significance: The standard-montage used for recording oVEMPs is sensitive to the placement of the active electrode. Small variations in position result in significant changes in the n10 amplitude and this may account for the variability reported in the literature. Using the belly-tendon montage, larger amplitude responses can be elicited which may improve the robustness with which oVEMPs can be collected. However this enhancement in response amplitude must be balanced against the increased possibility of signal contamination from neighbouring extraocular muscles. Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
⇑ Corresponding author at: Leicester Medical School, University of Leicester, Leicester LE1 9HN, UK. Tel.: +44 (0) 7921189307. E-mail address: [email protected] (J.S. Sandhu). 1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinph.2012.11.019
J.S. Sandhu et al. / Clinical Neurophysiology 124 (2013) 1232–1236
1. Introduction Over the past decade, literature concerning the cervical vestibular evoked myogenic potential (cVEMP) has proliferated and the technique has now become widely accepted as a test of saccule and inferior vestibular nerve integrity (Colebatch and Halmagyi, 1992; Welgampola and Colebatch, 2005). Recently a novel variation of the cVEMP known as the ocular vestibular evoked myogenic potential (oVEMP) has emerged. The oVEMP is a short-latency (10 ms), initially negative potential (n10) that can be recorded from the extraocular muscles in response to air or bone conducted stimulation (Rosengren et al., 2005; Todd et al., 2007; Chihara et al., 2007). The oVEMP is a predominately crossed vestibulo-ocular response. Whilst there remains some debate regarding the end organ involved in the generation of the air-conducted oVEMP, there is increasing evidence that the response is mediated via the superior division of the vestibular nerve (Sandhu et al., 2012; Curthoys et al., 2011, 2012; Murofushi et al., 2010; Manzari et al., 2010). The oVEMP is recorded with upward gaze as this increases the response magnitude (Govender et al., 2009). The oVEMP is thought to result from synchronisation of electromyography (EMG) generated by the inferior oblique extraocular muscles, as these are most active with elevation and extorsion of the eyes (Todd et al., 2007; Leigh and Zee, 1999). More recently direct evidence examining single motor unit activity of the inferior oblique and an inferior rectus muscle has confirmed that the n10 peak originates in the inferior oblique muscle during both vibration and sound evoked oVEMP recordings (Weber et al., 2012). The configuration used most commonly to record the oVEMP response utilises a pair of electrodes positioned just beneath the eye contralateral to the auditory stimulus with the active electrode placed around 2 cm above the reference electrode. A more distant site such as the sternum is used for the ground electrode. The evidence for this electrode montage is based on work by Rosengren et al. (2005) in which bone-conducted oVEMPs responses were recorded from electrodes placed superior, inferior, lateral and medial to the orbit with a reference electrode attached to the earlobe. In all four positions, dominantly negative waveforms were reported with the largest magnitudes obtained on the midline and closest to the eye. This work was further developed by Todd et al. (2007) who used a more selective bipolar montage to exclude more distant electrical activity and thereby showed that the extraocular potentials were not universally negative. Indeed there was a polarity change between the superiorly and inferiorly placed pair of electrodes. A combination of these findings has resulted in the currently favoured montage in which the active electrode is placed inferior to the contralateral eye and the reference electrode is placed directly below it. However, the electrode positions used in these initial studies were limited to the midline of the orbit and therefore lateral and medial variations have not been fully explored. In this paper we aim to investigate the distribution of the amplitude and polarity of the oVEMP response between the lateral and medial canthi in the infra-orbital plane in order to evaluate optimal electrode positioning. Furthermore we aim to investigate the use of a belly-tendon montage in which the reference electrode is placed at the inner canthus and the active just lateral to the orbital midline.
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deficits. Otoscopy was carried out to confirm patency of the external canal and visualisation of the tympanic membranes. Normal hearing (no worse than 20 dBHL at octave frequencies from 250 Hz to 8 kHz) was confirmed by pure tone audiometry and normal middle ear function and pressure confirmed by tympanometry prior to the oVEMP recordings. Informed consent was obtained from all individuals prior to the commencement of the recordings. The local ethics committee provided approval for the study. 2.2. Stimulus design The oVEMP recordings were carried out using an auditory evoked potential system, Navigation Pro, Version 6.1.0 (Bio-logicÒ System Corp, IL, USA). The stimulus was delivered via TDH-39 headphones and consisted of 500 Hz alternating polarity tone bursts with a rise/fall time of 1 cycle and a plateau time of 2 cycles. The stimulation rate was 5.2 Hz. The stimulus amplitude was set to 95 dBnHL. A time-average of 128 tone bursts was recorded for each run with bandpass filtering set to 3–1000 Hz. Two consecutive runs were recorded using AEP version 6.3.0 software package (Bio-logicÒ System Corp, IL, USA). The waveforms were then checked for authenticity by comparing the two runs. Reliable traces were then averaged into a single trace, which was used in the analysis. Amplitudes and latencies were taken at the first peak that occurred around 10 ms. 2.3. Positioning of electrodes and labelling of oVEMP waveforms The oVEMP responses were measured contralateral to the stimulation ear. The skin was prepared using alcohol wipes and six 4 mm silver/silver chloride electrodes were attached using impedance matching gel such that the contact resistances were kept below 10 kX in all cases. Five surface recording electrodes, numbered
2. Materials and methods 2.1. Subjects A total of 16 ears from 8 normal subjects were tested: 5 male and 3 female, age range 22–36 years, average age 26. None of the subjects reported any hearing, vestibular, neurological or visual
Fig. 1. Electrode positions and recording configurations used for oVEMP measurements (left eye shown).
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J.S. Sandhu et al. / Clinical Neurophysiology 124 (2013) 1232–1236
1–5, were placed equally spaced apart inferior to the lower lid margin with electrode 1 adjacent to the medial canthus, electrode 5 close to the lateral canthus, electrode 3 in the midline of the orbit, electrode 2 between electrodes 1 and 3 and electrode 4 between electrodes 3 and 5 (Fig. 1). A reference electrode (r) was placed 2 cm below electrode 3 and a ground electrode was placed on the sternum. In order to avoid ambiguity over the recording configuration used, the following nomenclature was adopted; pa,b, where a and b were the sites of the active and reference electrodes respectively. For example, with the active electrode in position 3 and the reference in position r the corresponding waveform label is p3,r. It is of note that the p3,r electrode configuration is favoured by the majority of investigators in the field and is therefore referred to interchangeably in this paper as the standard-montage. In addition to the five oVEMP recordings p1,r, p2,r, p3,r, p4,r and p5,r a further recording was made with the active electrode in position 4 and the reference electrode in position 1 (p4,1). 2.4. Recording procedure Response variability was minimised by standardising the seating orientation and by using target markers on the examination room ceiling. Subjects were asked to maintain focus upon a marker during oVEMP recordings such that they maximised upward gaze whilst retaining ocular comfort. Subjects were asked to return to the specific marker during subsequent recordings thereby reducing variations. Order effects were minimised by randomly varying the electrode pairs used for the recordings. 2.5. Statistical analysis
Fig. 2. Grand average oVEMP waveforms recorded with: (a) reference electrode in position ‘r’ and (b) with electrode configuration p4,1. The arrows denote the n10 feature and position ‘x’ represents a theoretical null-point.
The data were analysed using SPSS version 16.0 (SPSS Inc., Chicago, IL, USA). The oVEMP amplitudes and latencies from all subjects were first assessed for consistency with a normal–distribution using the Shapiro–Wilk test in combination with Q–Q plots. Depending upon the outcome the variables were either compared using an independent t-test (for parametric data) and the Mann Whitney test (for non-parametric data). A difference was regarded as being significant at p < 0.01. 3. Results 3.1. Measurements made using ‘r’ as the reference electrode The prevalence of air-conduction oVEMP responses in configurations p1,r, p2,r, p3,r, and p4,r, was 100%. The prevalence in configuration p5,r was 50%. The grand averages of the waveforms generated are shown in Fig. 2a. The n10 peak was identified in individual waveforms and the amplitudes were averaged across all ears (Fig. 3a). The electrode arrangement that resulted in the largest averaged amplitude across all ears was p4,r with n10 measuring 3.17 ± 2.13 lV (sd) with 9 ears showing a maximum amplitude in this position. The remaining 7 ears all showed a maximal n10 amplitude in position p3,r. As the active electrode was moved into adjacent position 3 and 5 the magnitude of the oVEMP remained positive but decreased to 3.05 ± 2.11 lV (sd) and 0.62 ± 0.85 lV (sd) respectively. The difference in amplitude between positions 3 and 4 was not statistically significant however the discrepancy between position 3 and 5 was statistically significant (p < 0.01). When the active electrode was moved to positions 2 the amplitude once again decreased however strikingly the n10 peak changed polarity becoming negative in 15 of the 16 ears tested, measuring 2.15 ± 2.25 lV (sd). Similarly when the active electrode was moved to position 1, the amplitude inverted in all 16 ears tested resulting in an average amplitude of
Fig. 3. Amplitude and latency data for oVEMP traces averaged over all sixteen ears tested. Open circles represent data collected with electrodes in p1 5,r configurations and the closed circles represent data collated with electrodes in the p4,1 configuration. Error bars represent standard errors.
J.S. Sandhu et al. / Clinical Neurophysiology 124 (2013) 1232–1236
1.73 ± 1.36 lV (sd). Relative to the standard montage with the active electrode in position 3 both these amplitude values were statistically significant (p < 0.01). Interestingly the entire morphologies of the waveforms recorded in configurations p2,r and p1,r were inverted relative to the waveforms measured in p3,r, p4,r and p5,r. The latencies of the n10 feature in the various electrode configurations are shown in Fig. 3b. 3.2. Measurements made in electrode configuration p4,1 The grand average of the waveforms recorded in configuration p4,1 is shown in figure 2b. The morphology is very similar to that recorded using the standard-montage (p3,r). The n10 peaks were identified in individual waveforms and the amplitude then averaged across all 16 ears thereby allowing direct comparison with the results obtained with the reference electrode at site r. Using this configuration, the n10 amplitude was found to be significantly larger than that recorded with electrodes in the p3,r arrangement in all sixteen ears, measuring 5.67 ± 3.42 lV (sd) (p < 0.01), see Figure 3a. The average latency of the n10 response is shown in figure 3b and was 10.71 ± 0.89 ms (sd). This was not statistically different to the average latency recorded using the standard montage. 4. Discussion In this study we have shown that the amplitude and polarity of the n10 feature of the oVEMP response is dependent upon the position of the active electrode. The majority of published oVEMP studies utilise a montage in which the active electrode is placed just below the contralateral eye in the orbital midline and the reference electrode placed approximately 2 cm below this. This configuration is chosen as it provides reasonably large response amplitudes, a finding confirmed by this study. However the disadvantage of this method highlighted by our results is that deviations of the active electrode from the midline position can result in variations in the response amplitude. The effect of electrode placement on the response size is shown in Fig. 3a. This shows a positive maximum with the electrodes in position p4,r. As the active electrode is moved laterally the amplitude decreases but remains positive. In contrast as the active electrode is moved medially towards the nose the amplitude both decreases and changes polarity. Of the 16 ears tested an inversion of signal was observed in 15 ears in position 2, which indicates that within our sample, in over 90% of cases there exists a null-point between electrode positions 2 and 3 where there is no oVEMP response present. In order to explain these morphological changes in the oVEMP response the anatomical location of the inferior oblique muscle from which the EMG modulation is being recorded must first be considered. The inferior oblique is a narrow muscle, which is 37 mm in length. It originates a few millimetres behind the medial end of the inferior orbital rim just lateral to the lacrimal fossa and proceeds posteriorly and temporally at an angle of 51° with the frontal plane passing beneath the inferior rectus. It inserts beneath the inferior border of the lateral rectus muscle, approximately 12 mm from the insertion of the lateral rectus (Kumar et al., 2011). Given this anatomy it is clear that electrode positions 3 and 4 coincide with the belly of the muscle and therefore equate to maximal EMG activity. In the standard-montage (p3,r), the reference electrode is positioned directly below electrode 3. At this point there is some inevitable far-field contamination as a result of volume conduction (Rutkove, 2007). The net effect of the synchronised EMG being present on both the active and reference electrode in this set-up is a subtraction of signal. Thereby resulting in a reduction of the recorded oVEMP amplitude. This phenomenon is more evident with the active electrodes in positions 2 and 1. Gi-
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ven the anatomical arrangement of the inferior oblique muscle these electrode positions are sufficiently distant from the belly of the inferior oblique muscle such that they sense a signal which is smaller than that recorded at the reference site which is geometrically closer the generation site of the synchronised EMG. As a result there is an inversion of the waveform captured with these recording montages. Interpolating these findings suggests that there exists a position between electrodes 2 and 3 where the EMG is equal to that present at the reference electrode thereby creating a null-point at which no oVEMP response is recorded. Given that these anomalies are due to the location of the reference electrode, the simplest solution would be to move the reference to a site where it is less likely to be contaminated. The most commonly used site for the reference electrode in EMG recordings is the tendon of the muscle, giving rise to the belly-tendon montage (Loeb and Gans, 1986). The oVEMP waveforms recorded in configuration p4,1 essentially follow this belly-tendon configuration. Indeed the results obtained using this arrangement showed significantly larger n10 amplitudes. However the amplitude of the response is not the only factor that must be taken into consideration, as reflex purity is also important. By moving the reference electrode to a medial position it is inevitably brought closer to the bellies of other extraocular muscles, which may also be activated by the oVEMP stimulus. Similarly, positioning the active electrode laterally will move it towards the lateral rectus muscle, which has been shown to exhibit electrical activity in response to oVEMP stimuli (Govender et al., 2011). Therefore there are potential disadvantages of using the belly-tendon set-up and further work is needed to compare the montages, especially in subjects with vestibular deficits in which contamination issues may become more evident.
5. Clinical relevance The findings of this study provide further evidence that the airconducted oVEMP is recorded from the inferior oblique muscle. The work highlights that using the standard-montage the oVEMP response amplitude is sensitive to the position of the active electrode, especially when it is moved medially. This may explain the variability of the oVEMP magnitude and prevalence reported in the literature to date. Whilst the results of the study show that the belly-tendon montage provides larger response amplitudes, the set-up has the inherent disadvantage of being more sensitive to extraneous signals from neighbouring extraocular muscles. We suggest that if when using the standard montage the oVEMP responses recorded are small or absent, the operator try moving the active electrode laterally to ascertain if the null-point described in this paper may be a contributing factor.
Acknowledgements The authors are grateful to Dr. Christopher Degg for help setting up the equipment and to Dr. Duncan Farrell for helpful discussions regarding interpretation of the findings.
References Chihara Y, Iwasaki S, Ushio M, Murofushi T. Vestibular-evoked extraocular potentials by air-conducted sound: another clinical test for vestibular function. Clin Neurophysiol 2007;118:2745–51. Colebatch JG, Halmagyi GM. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 1992;42:1635–6. Curthoys IS, Vulovic V, Manzari L. Ocular vestibular-evoked myogenic potential (oVEMP) to test utricular function: neural and oculomotor evidence. Acta Otorhinolaryngol Ital 2012;32:41–5.
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Curthoys IS, Iwasaki S, Chihara Y, Ushio M, McGarvie LA, Burgess AM. The ocular vestibular-evoked myogenic potential to air-conducted sound; probable superior vestibular nerve origin. Clin Neurophysiol 2011;122:611–6. Govender S, Rosengren SM, Todd NP, Colebatch JG. Ocular vestibular evoked myogenic potentials produced by impulsive lateral acceleration in unilateral vestibular dysfunction. Clin Neurophysiol 2011;122:2498–504. Govender S, Rosengren SM, Colebatch JG. The effect of gaze direction on the ocular vestibular evoked myogenic potential produced by air-conducted sound. Clin Neurophysiol 2009;120:1386–91. Kumar V, Murlimanju BV, Devika P, Narga N, Pai SR, Pulakunta T, et al. An anatomical study of the inferior oblique muscle with emphasis on its nerve entry. Chang Gung Med J 2011;34:293–7. Leigh RJ, Zee DS. The neurology of eye movements. 3rd ed. New York: Oxford University Press; 1999. Loeb GE, Gans C. Electromyography for experimentalists. Chicago (IL): University of Chicago Press; 1986. Manzari L, Burgess AM, Curthoys IS. Dissociation between cVEMP and oVEMP responses: different vestibular origins of each VEMP? Eur Arch Otorhinolaryngol 2010;267:1487–9.
Murofushi T, Wakayama K, Chihara Y. OVEMP to air-conducted tones reflects functions of different vestibular populations from cVEMP? Eur Arch Otorhinolaryngol 2010;267:995–6. Rosengren SM, Todd NPM, Colebatch JG. Vestibular-evoked extraocular potentials produced by stimulation with bone-conducted sound. Clin Neurophysiol 2005;116:1938–48. Rutkove SB. Introduction to volume conduction. In: Blum AS, Rutkove SB, editors. The clinical neurophysiology primer. Totowa (NJ): Humana Press; 2007. p. 43–57. Sandhu JS, Low R, Rea PA, Saunders NC. Altered frequency dynamics of cervical and ocular vestibular evoked myogenic potentials in patients with Ménière’s disease. Otol Neurotol 2012;33:444–9. Todd NPM, Rosengren SM, Aw ST, Colebatch JG. Ocular vestibular evoked myogenic potentials (OVEMPs) produced by air- and bone-conducted sound. Clin Neurophysiol 2007;118:381–90. Weber KP, Rosengren SM, Michels R, Sturm V, Strauman D, Landau K. Single motor unit activity in human extraocular muscles during the vestibulo-ocular reflex. J Physiol 2012;590:3091–6. Welgampola MS, Colebatch JG. Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology 2005;64:1682–8.
Contents lists available at SciVerse ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
The effect of electrode positioning on the ocular vestibular evoked myogenic potential to air-conducted sound Jaswinder S. Sandhu a,b,⇑, Stefan R. George a, Peter A. Rea b a b
Leicester Medical School, University of Leicester, Leicester LE1 9HN, UK Ear Nose and Throat Department, University Hospitals of Leicester, Leicester LE1 5WW, UK
See Editorial, pages 1051–1052
a r t i c l e
i n f o
Article history: Available online 18 January 2013 Keywords: Ocular vestibular evoked myogenic potential (oVEMP) Air-conducted sound (ACS) Electrode Montage Null-point
h i g h l i g h t s This study demonstrates that the amplitude of the oVEMP is highly sensitive to the relative positions of the active and reference electrodes. Small changes in the active electrode position result in amplitude inversion and exhibit an intermediate null-point where no response is detected. An alternative montage is proposed which avoids the null-point and furthermore enhances the oVEMP response amplitude.
a b s t r a c t Objective: To assess the effect of electrode position on the amplitude and latency of ocular vestibular evoked myogenic potentials (oVEMPs) produced by air-conducted (AC) sound with a view to optimisation of the recording paradigm. Methods: Eight otologically normal subjects (16 ears) were stimulated by 500 Hz AC tone bursts at 95 dBnHL; oVEMP traces were recorded below the eye contralateral to the acoustic stimulation. Five independent oVEMP measurements were recorded with the active electrode in equally spaced positions in the infra-orbital plane relative to a reference electrode positioned 2 cm below the lower lid in the orbital midline. These measurements included the accepted standard-montage in which the electrodes were positioned vertically above and below each other in the orbital midline. A further recording was made using a belly-tendon montage with reference to the inferior oblique muscle. Results: Of the six recording paradigms tested the largest amplitude oVEMP response was found using the belly-tendon montage with an n10 average of 5.67 ± 3.42 lV (sd). This was significantly larger than the amplitude recorded using the standard-montage (p < 0.01). With the reference electrode in the orbital midline, the position of the active electrode in the infra-orbital plane was found to significantly alter the response magnitude. As the active electrode was moved laterally the response reduced in amplitude, however when moved medially the response polarity reversed indicating the existence of a null-point at which no response was present. Conclusions: The location of oVEMP recording electrodes significantly alters the response amplitude. Whilst the standard-montage provides a reasonable method for recording oVEMPs, the belly-tendon montage results in a significantly larger amplitude response. Furthermore medial and lateral variations in the position of the active electrode using the standard-montage significantly affect the magnitude and polarity of the response. Significance: The standard-montage used for recording oVEMPs is sensitive to the placement of the active electrode. Small variations in position result in significant changes in the n10 amplitude and this may account for the variability reported in the literature. Using the belly-tendon montage, larger amplitude responses can be elicited which may improve the robustness with which oVEMPs can be collected. However this enhancement in response amplitude must be balanced against the increased possibility of signal contamination from neighbouring extraocular muscles. Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
⇑ Corresponding author at: Leicester Medical School, University of Leicester, Leicester LE1 9HN, UK. Tel.: +44 (0) 7921189307. E-mail address: [email protected] (J.S. Sandhu). 1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinph.2012.11.019
J.S. Sandhu et al. / Clinical Neurophysiology 124 (2013) 1232–1236
1. Introduction Over the past decade, literature concerning the cervical vestibular evoked myogenic potential (cVEMP) has proliferated and the technique has now become widely accepted as a test of saccule and inferior vestibular nerve integrity (Colebatch and Halmagyi, 1992; Welgampola and Colebatch, 2005). Recently a novel variation of the cVEMP known as the ocular vestibular evoked myogenic potential (oVEMP) has emerged. The oVEMP is a short-latency (10 ms), initially negative potential (n10) that can be recorded from the extraocular muscles in response to air or bone conducted stimulation (Rosengren et al., 2005; Todd et al., 2007; Chihara et al., 2007). The oVEMP is a predominately crossed vestibulo-ocular response. Whilst there remains some debate regarding the end organ involved in the generation of the air-conducted oVEMP, there is increasing evidence that the response is mediated via the superior division of the vestibular nerve (Sandhu et al., 2012; Curthoys et al., 2011, 2012; Murofushi et al., 2010; Manzari et al., 2010). The oVEMP is recorded with upward gaze as this increases the response magnitude (Govender et al., 2009). The oVEMP is thought to result from synchronisation of electromyography (EMG) generated by the inferior oblique extraocular muscles, as these are most active with elevation and extorsion of the eyes (Todd et al., 2007; Leigh and Zee, 1999). More recently direct evidence examining single motor unit activity of the inferior oblique and an inferior rectus muscle has confirmed that the n10 peak originates in the inferior oblique muscle during both vibration and sound evoked oVEMP recordings (Weber et al., 2012). The configuration used most commonly to record the oVEMP response utilises a pair of electrodes positioned just beneath the eye contralateral to the auditory stimulus with the active electrode placed around 2 cm above the reference electrode. A more distant site such as the sternum is used for the ground electrode. The evidence for this electrode montage is based on work by Rosengren et al. (2005) in which bone-conducted oVEMPs responses were recorded from electrodes placed superior, inferior, lateral and medial to the orbit with a reference electrode attached to the earlobe. In all four positions, dominantly negative waveforms were reported with the largest magnitudes obtained on the midline and closest to the eye. This work was further developed by Todd et al. (2007) who used a more selective bipolar montage to exclude more distant electrical activity and thereby showed that the extraocular potentials were not universally negative. Indeed there was a polarity change between the superiorly and inferiorly placed pair of electrodes. A combination of these findings has resulted in the currently favoured montage in which the active electrode is placed inferior to the contralateral eye and the reference electrode is placed directly below it. However, the electrode positions used in these initial studies were limited to the midline of the orbit and therefore lateral and medial variations have not been fully explored. In this paper we aim to investigate the distribution of the amplitude and polarity of the oVEMP response between the lateral and medial canthi in the infra-orbital plane in order to evaluate optimal electrode positioning. Furthermore we aim to investigate the use of a belly-tendon montage in which the reference electrode is placed at the inner canthus and the active just lateral to the orbital midline.
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deficits. Otoscopy was carried out to confirm patency of the external canal and visualisation of the tympanic membranes. Normal hearing (no worse than 20 dBHL at octave frequencies from 250 Hz to 8 kHz) was confirmed by pure tone audiometry and normal middle ear function and pressure confirmed by tympanometry prior to the oVEMP recordings. Informed consent was obtained from all individuals prior to the commencement of the recordings. The local ethics committee provided approval for the study. 2.2. Stimulus design The oVEMP recordings were carried out using an auditory evoked potential system, Navigation Pro, Version 6.1.0 (Bio-logicÒ System Corp, IL, USA). The stimulus was delivered via TDH-39 headphones and consisted of 500 Hz alternating polarity tone bursts with a rise/fall time of 1 cycle and a plateau time of 2 cycles. The stimulation rate was 5.2 Hz. The stimulus amplitude was set to 95 dBnHL. A time-average of 128 tone bursts was recorded for each run with bandpass filtering set to 3–1000 Hz. Two consecutive runs were recorded using AEP version 6.3.0 software package (Bio-logicÒ System Corp, IL, USA). The waveforms were then checked for authenticity by comparing the two runs. Reliable traces were then averaged into a single trace, which was used in the analysis. Amplitudes and latencies were taken at the first peak that occurred around 10 ms. 2.3. Positioning of electrodes and labelling of oVEMP waveforms The oVEMP responses were measured contralateral to the stimulation ear. The skin was prepared using alcohol wipes and six 4 mm silver/silver chloride electrodes were attached using impedance matching gel such that the contact resistances were kept below 10 kX in all cases. Five surface recording electrodes, numbered
2. Materials and methods 2.1. Subjects A total of 16 ears from 8 normal subjects were tested: 5 male and 3 female, age range 22–36 years, average age 26. None of the subjects reported any hearing, vestibular, neurological or visual
Fig. 1. Electrode positions and recording configurations used for oVEMP measurements (left eye shown).
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J.S. Sandhu et al. / Clinical Neurophysiology 124 (2013) 1232–1236
1–5, were placed equally spaced apart inferior to the lower lid margin with electrode 1 adjacent to the medial canthus, electrode 5 close to the lateral canthus, electrode 3 in the midline of the orbit, electrode 2 between electrodes 1 and 3 and electrode 4 between electrodes 3 and 5 (Fig. 1). A reference electrode (r) was placed 2 cm below electrode 3 and a ground electrode was placed on the sternum. In order to avoid ambiguity over the recording configuration used, the following nomenclature was adopted; pa,b, where a and b were the sites of the active and reference electrodes respectively. For example, with the active electrode in position 3 and the reference in position r the corresponding waveform label is p3,r. It is of note that the p3,r electrode configuration is favoured by the majority of investigators in the field and is therefore referred to interchangeably in this paper as the standard-montage. In addition to the five oVEMP recordings p1,r, p2,r, p3,r, p4,r and p5,r a further recording was made with the active electrode in position 4 and the reference electrode in position 1 (p4,1). 2.4. Recording procedure Response variability was minimised by standardising the seating orientation and by using target markers on the examination room ceiling. Subjects were asked to maintain focus upon a marker during oVEMP recordings such that they maximised upward gaze whilst retaining ocular comfort. Subjects were asked to return to the specific marker during subsequent recordings thereby reducing variations. Order effects were minimised by randomly varying the electrode pairs used for the recordings. 2.5. Statistical analysis
Fig. 2. Grand average oVEMP waveforms recorded with: (a) reference electrode in position ‘r’ and (b) with electrode configuration p4,1. The arrows denote the n10 feature and position ‘x’ represents a theoretical null-point.
The data were analysed using SPSS version 16.0 (SPSS Inc., Chicago, IL, USA). The oVEMP amplitudes and latencies from all subjects were first assessed for consistency with a normal–distribution using the Shapiro–Wilk test in combination with Q–Q plots. Depending upon the outcome the variables were either compared using an independent t-test (for parametric data) and the Mann Whitney test (for non-parametric data). A difference was regarded as being significant at p < 0.01. 3. Results 3.1. Measurements made using ‘r’ as the reference electrode The prevalence of air-conduction oVEMP responses in configurations p1,r, p2,r, p3,r, and p4,r, was 100%. The prevalence in configuration p5,r was 50%. The grand averages of the waveforms generated are shown in Fig. 2a. The n10 peak was identified in individual waveforms and the amplitudes were averaged across all ears (Fig. 3a). The electrode arrangement that resulted in the largest averaged amplitude across all ears was p4,r with n10 measuring 3.17 ± 2.13 lV (sd) with 9 ears showing a maximum amplitude in this position. The remaining 7 ears all showed a maximal n10 amplitude in position p3,r. As the active electrode was moved into adjacent position 3 and 5 the magnitude of the oVEMP remained positive but decreased to 3.05 ± 2.11 lV (sd) and 0.62 ± 0.85 lV (sd) respectively. The difference in amplitude between positions 3 and 4 was not statistically significant however the discrepancy between position 3 and 5 was statistically significant (p < 0.01). When the active electrode was moved to positions 2 the amplitude once again decreased however strikingly the n10 peak changed polarity becoming negative in 15 of the 16 ears tested, measuring 2.15 ± 2.25 lV (sd). Similarly when the active electrode was moved to position 1, the amplitude inverted in all 16 ears tested resulting in an average amplitude of
Fig. 3. Amplitude and latency data for oVEMP traces averaged over all sixteen ears tested. Open circles represent data collected with electrodes in p1 5,r configurations and the closed circles represent data collated with electrodes in the p4,1 configuration. Error bars represent standard errors.
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1.73 ± 1.36 lV (sd). Relative to the standard montage with the active electrode in position 3 both these amplitude values were statistically significant (p < 0.01). Interestingly the entire morphologies of the waveforms recorded in configurations p2,r and p1,r were inverted relative to the waveforms measured in p3,r, p4,r and p5,r. The latencies of the n10 feature in the various electrode configurations are shown in Fig. 3b. 3.2. Measurements made in electrode configuration p4,1 The grand average of the waveforms recorded in configuration p4,1 is shown in figure 2b. The morphology is very similar to that recorded using the standard-montage (p3,r). The n10 peaks were identified in individual waveforms and the amplitude then averaged across all 16 ears thereby allowing direct comparison with the results obtained with the reference electrode at site r. Using this configuration, the n10 amplitude was found to be significantly larger than that recorded with electrodes in the p3,r arrangement in all sixteen ears, measuring 5.67 ± 3.42 lV (sd) (p < 0.01), see Figure 3a. The average latency of the n10 response is shown in figure 3b and was 10.71 ± 0.89 ms (sd). This was not statistically different to the average latency recorded using the standard montage. 4. Discussion In this study we have shown that the amplitude and polarity of the n10 feature of the oVEMP response is dependent upon the position of the active electrode. The majority of published oVEMP studies utilise a montage in which the active electrode is placed just below the contralateral eye in the orbital midline and the reference electrode placed approximately 2 cm below this. This configuration is chosen as it provides reasonably large response amplitudes, a finding confirmed by this study. However the disadvantage of this method highlighted by our results is that deviations of the active electrode from the midline position can result in variations in the response amplitude. The effect of electrode placement on the response size is shown in Fig. 3a. This shows a positive maximum with the electrodes in position p4,r. As the active electrode is moved laterally the amplitude decreases but remains positive. In contrast as the active electrode is moved medially towards the nose the amplitude both decreases and changes polarity. Of the 16 ears tested an inversion of signal was observed in 15 ears in position 2, which indicates that within our sample, in over 90% of cases there exists a null-point between electrode positions 2 and 3 where there is no oVEMP response present. In order to explain these morphological changes in the oVEMP response the anatomical location of the inferior oblique muscle from which the EMG modulation is being recorded must first be considered. The inferior oblique is a narrow muscle, which is 37 mm in length. It originates a few millimetres behind the medial end of the inferior orbital rim just lateral to the lacrimal fossa and proceeds posteriorly and temporally at an angle of 51° with the frontal plane passing beneath the inferior rectus. It inserts beneath the inferior border of the lateral rectus muscle, approximately 12 mm from the insertion of the lateral rectus (Kumar et al., 2011). Given this anatomy it is clear that electrode positions 3 and 4 coincide with the belly of the muscle and therefore equate to maximal EMG activity. In the standard-montage (p3,r), the reference electrode is positioned directly below electrode 3. At this point there is some inevitable far-field contamination as a result of volume conduction (Rutkove, 2007). The net effect of the synchronised EMG being present on both the active and reference electrode in this set-up is a subtraction of signal. Thereby resulting in a reduction of the recorded oVEMP amplitude. This phenomenon is more evident with the active electrodes in positions 2 and 1. Gi-
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ven the anatomical arrangement of the inferior oblique muscle these electrode positions are sufficiently distant from the belly of the inferior oblique muscle such that they sense a signal which is smaller than that recorded at the reference site which is geometrically closer the generation site of the synchronised EMG. As a result there is an inversion of the waveform captured with these recording montages. Interpolating these findings suggests that there exists a position between electrodes 2 and 3 where the EMG is equal to that present at the reference electrode thereby creating a null-point at which no oVEMP response is recorded. Given that these anomalies are due to the location of the reference electrode, the simplest solution would be to move the reference to a site where it is less likely to be contaminated. The most commonly used site for the reference electrode in EMG recordings is the tendon of the muscle, giving rise to the belly-tendon montage (Loeb and Gans, 1986). The oVEMP waveforms recorded in configuration p4,1 essentially follow this belly-tendon configuration. Indeed the results obtained using this arrangement showed significantly larger n10 amplitudes. However the amplitude of the response is not the only factor that must be taken into consideration, as reflex purity is also important. By moving the reference electrode to a medial position it is inevitably brought closer to the bellies of other extraocular muscles, which may also be activated by the oVEMP stimulus. Similarly, positioning the active electrode laterally will move it towards the lateral rectus muscle, which has been shown to exhibit electrical activity in response to oVEMP stimuli (Govender et al., 2011). Therefore there are potential disadvantages of using the belly-tendon set-up and further work is needed to compare the montages, especially in subjects with vestibular deficits in which contamination issues may become more evident.
5. Clinical relevance The findings of this study provide further evidence that the airconducted oVEMP is recorded from the inferior oblique muscle. The work highlights that using the standard-montage the oVEMP response amplitude is sensitive to the position of the active electrode, especially when it is moved medially. This may explain the variability of the oVEMP magnitude and prevalence reported in the literature to date. Whilst the results of the study show that the belly-tendon montage provides larger response amplitudes, the set-up has the inherent disadvantage of being more sensitive to extraneous signals from neighbouring extraocular muscles. We suggest that if when using the standard montage the oVEMP responses recorded are small or absent, the operator try moving the active electrode laterally to ascertain if the null-point described in this paper may be a contributing factor.
Acknowledgements The authors are grateful to Dr. Christopher Degg for help setting up the equipment and to Dr. Duncan Farrell for helpful discussions regarding interpretation of the findings.
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