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Selective effects of head posture on ocular vestibular-evoked myogenic potential (oVEMP) by bone-conducted vibration
Clinical Neurophysiology 125 (2014) 621–626
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Selective effects of head posture on ocular vestibular-evoked myogenic potential (oVEMP) by bone-conducted vibration Shou-Jen Wang a, Chia-Chen Tseng b, Yi-Ho Young b,⇑ a b
Department of Otolaryngology, Catholic Cardinal Tien Hospital, Fu-Jen Catholic University, Taipei, Taiwan Department of Otolaryngology, National Taiwan University Hospital, Taipei, Taiwan
a r t i c l e
i n f o
Article history: Accepted 2 September 2013 Available online 10 October 2013 Keywords: Dynamic shearing force Head hanging Ocular vestibular-evoked myogenic potential Static gravitational force
h i g h l i g h t s Using bone-conducted vibration (BCV) stimulation, mean nI–pI amplitude with the head hanging
position was significantly larger than that with the sitting position, but not significantly larger than that with the supine position. Using air-conducted sound (ACS) stimulation, mean nI–pI amplitude did not differ significantly among the sitting, supine, and head hanging positions. Gravitational force can exert a selective effect on the reflex amplitude of oVEMPs elicited by BCV stimuli, but not by ACS stimuli.
a b s t r a c t Objective: By altering head postures from sitting, supine to head hanging, this study investigated the effects of gravitational force on ocular vestibular-evoked myogenic potential (oVEMP) via either air-conducted sound (ACS) or bone-conducted vibration (BCV) stimuli. Methods: Twenty healthy volunteers underwent the oVEMP test via ACS or BCV stimuli with the sitting, supine, and head hanging positions on the same day in a randomized order. Results: All subjects had clear BCV oVEMPs in the three head postures. No significant differences existed in terms of mean nI and pI latencies, the nI–pI interval, and asymmetry ratio regardless of various positions. However, the mean nI–pI amplitude with the head hanging position (15.9 ± 6.4 lV) was significantly larger than that with the sitting position (13.8 ± 6.0 lV), but not significantly larger than that with the supine position (14.7 ± 6.1 lV). Nevertheless, such a difference in reflex amplitude does not exist in oVEMPs elicited by ACS stimuli. With the sitting position, mean linear acceleration at the mastoids in response to BCV stimuli was 0.06 ± 0.02, 0.20 ± 0.04 and 0.04 ± 0.02 g along the x-, y-, and z-axis, respectively, which did not differ significantly from those with the head hanging position. Conclusion: By altering head postures from sitting to head hanging, gravitational force can exert a selective effect on the reflex amplitude of oVEMPs elicited by BCV stimuli, but not by ACS stimuli. Significance: Compared to ACS mode, BCV mode can provoke higher response rate, generate earlier and larger waveforms, and be influenced by both dynamic shearing force and static gravitational force to enlarge the reflex amplitude of oVEMPs. Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction In humans, the two otolithic organs, namely the utricle and saccule, are aligned in the horizontal and vertical planes, respectively. Each organ is composed of otoconia (otoliths) embedded in a gelat⇑ Corresponding author. Address: Department of Otolaryngology, National Taiwan University Hospital, 1 Chang-te St., Taipei, Taiwan. Tel.: +886 2 23123456x65221; fax: +886 2 23946774. E-mail address: [email protected] (Y.-H. Young).
inous matrix with a mean thickness of 50 lm, and the gelatinous layer contains hair cells (De Vries, 1951). These otolithic organs can respond to dynamic alternating vibration with shearing movement on the otoconial membrane. The hair cells then transmit displacement information of the otoconial membrane to the central nervous system. Additionally, the otolithic organs also sense static gravitational force, serving a functional role in maintaining postural stability. Clinically, dynamic otolithic function can be assessed by recently emerging vestibular-evoked myogenic potential (VEMP)
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.2013.09.002
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tests via air-conducted sound (ACS) or bone-conducted vibration (BCV) stimuli, including cervical VEMP (cVEMP) recorded on contracted neck muscles, and ocular VEMP (oVEMP) collected on extraocular muscles (Colebatch et al., 1994; Rosengren et al., 2005). Based on the efferent specificity, cVEMP represents predominantly saccular function, while oVEMP reflects mainly utricular function (Curthoys, 2010) although the otolith origin of the oVEMP is not yet universally agreed upon (Colebatch, 2010; Papathanasiou, 2012). Recent studies demonstrated that as linear acceleration increases, oVEMP amplitude enlarges (Todd et al., 2009; Cai et al., 2011; Wang et al., 2012). However, little attention has focused on the impact of static gravitational force on oVEMPs. In humans, Jombík and Bahyl (2005) have first mentioned the effect of interaction of the static gravity vector and dynamic acceleration vector induced by skull bone vibration on the ocular potentials recorded by electrooculography. Later more detailed studies by Ito et al. (2007) revealed that there is some effect of head position in the pitch and roll planes on tonic excitation of the saccule, resulting in altered latencies of cVEMPs. Further, head tilt in the roll plane increased the asymmetry ratio of oVEMP amplitude elicited by BCV stimuli (Iwasaki et al., 2012). Restated, different geometry may reflect a different interaction of the static gravity and the dynamic inertial acceleration vectors. However, the effect of static gravitational force in the pitch plane on oVEMPs remains unclear. By altering head postures from sitting, supine to head hanging, this study investigated the effect of gravitational force on oVEMPs via either ACS or BCV stimuli. 2. Subjects and methods 2.1. Subjects Twenty healthy volunteers, 12 males and 8 females (age, 22– 36 years; mean, 27 years), who denied having previous ear disorders were enrolled. Subjects were further checked by otoscopy and audiometry, confirming intact eardrums and normal hearing. All subjects underwent the oVEMP test via BCV stimuli with the sitting, supine and head hanging positions on the same day randomly. The head hanging position means the subject in a supine position with his/her head hanging backward in a pitch plane maximally without rotating the neck to the roll plane. On another day, all subjects underwent the same test paradigm, but the oVEMP test was performed via ACS stimuli. This study was approved by the institutional review board, and each subject signed the informed consent to participate. 2.2. oVEMP test using BCV stimuli
Fig. 1. Illustration of oVEMP tests by BCV stimuli with the sitting, supine, and head hanging positions.
Surface potentials, predominantly electromyographic (EMG) activities, were recorded (Smart EP 3.90, Intelligent Hearing Systems, Miami, FL, USA). Two active electrodes were placed around 1 cm below the center of the two lower eyelids. The other two reference electrodes were positioned about 1–2 cm below the active ones, and one ground electrode was placed on the sternum. During recording, the subject was instructed to look upward at a small fixed target on the wall >2 m from the eyes under sitting position, on the ceiling >2 m from the eyes under supine position, or on the floor >2 m from the eyes under head hanging position (Fig. 1). A vertical visual angle was approximately 30o above horizontal. The EMG signals were amplified and bandpass filtered between 1 and 1000 Hz (Wang et al., 2013). The stimulation rate was 5/s. The duration of analysis of each response was 50 ms, and 30 responses were averaged for each run. The BCV stimuli used a hand-held electromechanical vibrator (minishaker 4810, Bruel and Kjaer, Naerum, Denmark) fitted with
a short bolt terminated in a bakelite cap. The operator held the vibrator by hand, supported most of its weight, and delivered a repeatable tap on the subject’s skull at Fz (midline of the hairline). The input signal was 500 Hz sine wave, driven by a custom amplifier. The drive voltage was adjusted and fixed to produce a peak force equivalent to 128 dB force level. The initial negative–positive biphasic waveform comprised peaks nI and pI. Consecutive runs were performed to confirm the reproducibility of peaks nI and pI, and oVEMPs were deemed to be present. Thus, latencies of the nI and pI peaks, and amplitude of nI–pI were measured. The asymmetry ratio (%) was defined as the difference of the amplitude nI–pI on each ear divided by the sum of amplitude nI–pI of both ears, that is, (amplitude on the left ear–amplitude on the right ear)/(amplitude on the left ear + amplitude on the right ear) 100 (%).
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2.3. oVEMP test using ACS stimuli All 20 subjects also underwent oVEMP test via ACS stimulation. The latter consisted of 105 dB nHL (127 dB pe SPL) short tone bursts (500 Hz, rise/fall time = 1 ms, plateau time = 2 ms) with rarefaction polarity and were delivered through an insert earphone. The other setting was the same as that stimulated by BCV mode, except that the ground electrode was placed on the forehead. The stimulation rate was 6.7/s and analytical time for each response was 50 ms; 100 responses were averaged for each run. Binaural acoustic stimulation with bilateral recordings was employed (Wang et al., 2009).
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tion magnitudes along the x-, y-, and z-axis in response to BCV stimuli were analyzed by one-way repeated-measures analysis of variance (ANOVA), and Bonferroni-adjusted paired t-test was applied for multiple comparisons. Further, the Student’s t test was used to compare the characteristic parameters between the oVEMP elicited by the two stimuli, whichever in the various positions. The difference of linear acceleration along the x-, y- and z-axes between the sitting and head hanging positions was examined by the paired t test. A significant difference is suggested by a p value <0.05. 3. Results 3.1. BCV oVEMPs
2.4. Triaxial accelerometry at the mastoid One miniature (10 mm3, 5 g) triaxial accelerometer (Endevco model 65-100, San Juan Capistrano, CA, USA) accompanied by a tight elastic bandage surrounding the head girth was fixed to each subject’s left mastoid area just behind the auricle. Using the head as the reference point, the accelerometer was utilized to measure the three-dimensional linear acceleration along the x-axis (anterior–posterior), y-axis (inter-aural), and z-axis (rostro-caudal) simultaneously. Forward, outward, and upward were defined as the positive x, y, and z directions, respectively. The voltage sensitivity was 100 mV/g and the frequency response was 1.5–6000 Hz (±1 dB). The triaxial accelerometer signals were digitalized at 10 kHz using a dynamic signal analyzer (NI USB-4431, National Instruments, Austin, Texas, USA), which provided signal conditioning and constant current supply (2.1 mA) to the accelerometer. The acceleration magnitude was simultaneously measured throughout oVEMP testing, and ten runs of reproducible sweep were recorded. The initial peak magnitudes of linear acceleration were analyzed using a customized program (LabVIEW 8.5, National Instruments, Austin, Texas, USA) (Wang et al., 2012). In total, six subjects (4 men and 2 women, aged 22–34 years) undertook triaxial accelerometry at the mastoid with different head postures randomly.
All twenty healthy volunteers (100%) had clear oVEMPs beneath both eyes by BCV stimuli regardless of whether the subject was positioned in sitting, supine, or head hanging (Fig. 2). Because there were no significant differences in the characteristic parameters between the right and left oVEMPs, and the asymmetry ratios of amplitude were well below 40%, the values for both eyes were therefore pooled for subsequent analyses. The mean nI and pI latencies in the sitting position were 8.3 ± 0.4 (mean ± SD) and 12.3 ± 1.1 ms, respectively, not significantly different from those in the supine and head hanging position (p > 0.05, one-way repeated-measures ANOVA, Table 1). Similarly, no significant differences in the nI–pI interval and asymmetry ratio existed regardless of various positions (p > 0.05, Table 1). However, there were significant differences in the nI–pI amplitudes among the three positions (p < 0.05, one-way repeated-measures ANOVA, Table 1). Bonferroni-adjusted paired t-test demonstrated that mean nI–pI amplitude with the head hanging position (15.9 ± 6.4 lV) was significantly larger than that with the sitting position (13.8 ± 6.0 lV) (p < 0.05, Table 1), but the nI–pI amplitudes did not significantly differ between the sitting and supine positions or between the supine and head hanging positions (p > 0.05, Table 1).
2.5. Statistical methods
3.2. ACS oVEMPs
The response rate among the three positions was compared by the Cochran’s Q test. The characteristic parameters, either using different stimuli, among the three head postures and the accelera-
All subjects also participated in oVEMP testing by ACS stimuli (Fig. 3). Thirty-two (80%) of 40 ears had clear oVEMPs in the sitting position, not significantly different from the response rate of 80%
Fig. 2. Male, 25 years old, oVEMPs by BCV stimuli. There are significant differences in the nI–pI amplitudes among the three positions. The nI–pI amplitudes with the head hanging position (R/L: 18.1/19.7 lV) are larger than those with the sitting position (R/L: 14.0/14.9 lV), but do not significantly differ from those with supine position (R/L: 15.8/16.9 lV).
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Table 1 Comparison of BCV oVEMPs among the three positions. Position
N (ears)
Response rate (%)
nI latency (ms)
pI latency (ms)
nI-pI interval (ms)
nI–pI amplitude (lV)
Asymmetry ratio (%)
Sitting Supine Head hanging p Value
40 40 40
100 100 100
8.3 ± 0.4 8.3 ± 0.5 8.4 ± 0.4 >0.05
12.3 ± 1.1 12.3 ± 1.0 12.4 ± 0.9 >0.05
4.0 ± 1.0 4.0 ± 0.9 4.1 ± 0.8 >0.05
13.8 ± 6.0 14.7 ± 6.1 15.9 ± 6.4* <0.05
3.7 ± 10.3 3.0 ± 8.5 0.7 ± 10.8 >0.05
Data are expressed as mean ± SD; p value: one-way repeated-measures ANOVA test. p < 0.05, Bonferroni-adjusted paired t-test for multiple comparisons, as compared with the nI–pI amplitude with the sitting position.
*
(32/40 ears) in the supine or head hanging position (p > 0.05, Cochran’s Q test). The mean latencies of nI and pI, the nI–pI interval, nI– pI amplitude, and asymmetry ratio did not significantly differ among the three positions (p > 0.05, one-way repeated-measures ANOVA, Table 2). 3.3. BCV oVEMPs vs. ACS oVEMPs The characteristic parameters of BCV oVEMPs and ACS oVEMPs were analyzed. With the sitting position, the mean nI and pI latencies of BCV oVEMPs (8.3 ± 0.4 and 12.3 ± 1.1 ms) were significantly earlier than the respective 10.6 ± 0.7 and 15.5 ± 1.4 ms of ACS oVEMPs (p < 0.05, Student’s t test). In terms of nI–pI amplitude, BCV oVEMPs (13.8 ± 6.0 lV) had significantly larger responses than ACS oVEMPs (8.3 ± 3.0 lV) (p < 0.05). Similar differences also existed with the supine or head hanging position. 3.4. Triaxial acceleration: sitting vs. head hanging positions Since the nI–pI amplitudes did not significantly differ between the supine position and sitting/head hanging position, comparison of the triaxial acceleration was thus conducted between sitting and head hanging positions. In response to BCV stimuli at Fz, mean lin-
ear acceleration at the mastoids were 0.06 ± 0.02 g along the xaxis, 0.20 ± 0.04 g along the y-axis, and 0.04 ± 0.02 g along the z-axis with the sitting position, not significantly different from the 0.05 ± 0.02, 0.19 ± 0.03, and 0.04 ± 0.01 g along the respective axis with the head hanging position (p > 0.05, paired t test). Among the three axes, the largest acceleration magnitude was along the y-axis regardless of sitting or head hanging position (p < 0.01, one-way repeated measures ANOVA and Bonferroni adjusted paired t-test). 4. Discussion Similar to the linear accelerometer in the contemporary smartphone which senses device direction, the otolithic organs in the temporal bone detect static gravitational force and help determine the head’s orientation. This is likely because regularly firing otolithic afferents change their sensitivity with respect to variations in gravitational force (Fernandez and Goldberg, 1976). During linear acceleration tangential to the surface of the utricular macula, two vector forces, namely, dynamic shearing force and static gravitational force, instantaneously act upon the macula (De Vries, 1951). To ascertain the sensitivity of the utricle under these circumstances, 20 healthy subjects under-
Fig. 3. Same subject as in Fig. 2, oVEMPs by ACS stimuli. The nI–pI amplitudes do not differ significantly among the three positions (sitting: R/L: 6.5/7.6 lV; supine: R/L: 6.6/ 6.9 lV; head hanging: R/L: 6.7/7.4 lV).
Table 2 Comparison of ACS oVEMPs among the three positions. Position
N (ears)
Response rate (%)
nI latency (ms)
pI latency (ms)
nI-pI interval (ms)
nI-pI amplitude (lV)
Asymmetry ratio (%)
Sitting Supine Head hanging p value
40 40 40
80 80 80
10.6 ± 0.7 10.7 ± 0.7 10.6 ± 0.6 >0.05
15.5 ± 1.4 15.7 ± 1.3 15.5 ± 1.3 >0.05
4.9 ± 1.1 5.0 ± 1.1 4.9 ± 1.2 >0.05
8.3 ± 3.0 8.0 ± 3.1 8.2 ± 2.9 >0.05
1.9 ± 17.3 -0.9 ± 18.0 0.2 ± 17.6 >0.05
Data are expressed as mean ± SD; p value: one-way repeated-measures ANOVA test.
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went oVEMP testing via BCV stimuli with the sitting, supine, and head hanging positions (Fig. 1). No significant differences were evident in terms of nI and pI latencies, the nI–pI interval, or the asymmetry ratio among the three positions (Table 1). However, mean amplitude of oVEMPs with the head hanging position was significantly larger than that with the sitting position (Fig. 2), probably due to the effect of dynamic shearing force or static gravitational force.
4.1. Effect of dynamic shearing force on oVEMPs Dynamic shearing force was measured with triaxial accelerometry at the mastoid and represented as three-dimensional linear acceleration. With the sitting or head hanging position, the largest acceleration magnitude was along the y-axis i.e., interaural direction, which is compatible with previous reports (Iwasaki et al., 2008; Wang et al., 2012). A comparison of linear acceleration in the sitting and head hanging positions revealed no significant difference along the x-, y-, or z-axis. Restated, the dynamic shearing force induced by BCV stimuli was unrelated to the two head positions. Instead, large oVEMP amplitudes with the head hanging position may be caused by altered direction of static gravitational force.
4.2. Effect of static gravitational force on oVEMPs The position of a load on the otolithic receptors depends on the magnitude and direction of the force acting upon it. Morphologically, the otoconial membrane is above the utricular maculae in the sitting position, and vice versa in the head hanging position (Fig. 4). When the otoliths were hanging perpendicularly in the endolymphatic space, the otoconial membrane may apply stronger shearing force upon the nearby stereocilia (Bos et al., 1963; Jongkees and Philipszoon, 1963). Thus, as compared with the BCV oVEMPs in the sitting position, enlarged reflex amplitude was noted in the head hanging position, but not in the intermediate (supine) position (Table 1). Restated, when the utricular otoliths hang beneath the macula, increased sensitivity to linear acceleration leads to an enlarged effect on the reflex amplitude of BCV oVEMP. Similarly, amplitude of the first wave in vestibular evoked potentials (VsEP) to linear acceleration stimuli would be greater in the ‘‘head up’’ position of rats when compared to that in the ‘‘head down’’ position (Plotnik et al., 1999). However, such an enlarged effect was not observed in the reflex amplitude of oVEMPs via ACS stimulation (Fig. 3), as demonstrated by no significant difference in reflex amplitudes among the three positions (Table 2). The main reason is because both stimulation modes act differently. The BCV stimuli exerted to the head cause vibrational waves to travel around and through the head, resulting in linear accelerations at the mastoids (Iwasaki et al., 2008; Todd et al., 2009). Conversely, ACS stimuli cannot provoke skull acceleration, but act moving the perilymph and saccular membrane, which then causes movement in the endolymph. One may argue that the enlarged effect might be caused by different involvement of the neck proprioceptors in the two positions. In contrast to the sitting position, the neck is bent in the head hanging position, implying that the positions of head and torso are different with respect to each other. However, it had been reported that changes in the cervical input did not influence oVEMPs in response to BCV stimuli (Iwasaki et al., 2012). Thus, this possibility could be neglected, plausibly because the pathway mediating the cervico-ocular reflex is polysynaptic and this reflex would not occur with latency less than 40 ms (Popov et al., 1999).
Fig. 4. Illustration of the relationships between the otoconia and utricular macula in sitting vs. head hanging positions. The utricle is composed of otoconia (grey area) embedded in a gelatinous matrix, and the gelatinous layer contains hair cells.
4.3. BCV oVEMPs vs. ACS oVEMPs Both BCV and ACS stimulation modes have been widely used to elicit oVEMPs in clinical patients (Young, 2013). Since both modes
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can activate otolithic maculae, many laboratories utilized ACS mode instead of BCV mode to eliminate the need to purchase a new instrument. Thus, differences between ACS oVEMPs and BCV oVEMPs warrant further investigation. First, the mean latencies of nI and pI, and the nI–pI interval of ACS oVEMPs were significantly prolonged when compared with those of BCV oVEMPs, regardless of head position. The variation between stimulation duration (ACS of 4 ms and BCV of 1 ms) may account for this difference. Second, the response rate and reflex amplitude of ACS oVEMPs were significantly less than those of BCV oVEMPs, regardless of the sitting, supine, or head hanging position. These findings may be because the two stimuli evoked dissimilar populations of otolithic afferents (Iwasaki et al., 2012). Although ACS stimuli are suitable for activating otolithic afferents (Murofushi et al., 1995), they are not sufficiently effective for eliciting oVEMPs (Chihara et al., 2007; Cheng et al., 2009; Wang et al., 2010), probably because only some irregular otolithic afferents are activated by the ACS stimuli. On the other hand, BCV mode might activate irregular otolithic afferents more efficiently, leading to larger reflex amplitude when compared with that in ACS mode (Curthoys and Vulovic, 2011). Another possibility for the differences between ACS oVEMPs and BCV oVEMPs is that ACS mode mainly activates the saccular macula and BCV mode stimulates the utricle. As the macula in the saccule is vertically orientated, and the macula in the utricle is horizontally orientated, one would expect that rotation in the pitch plane would affect the saccule and the utricle differently (Welgampola and Colebatch, 2005; Papathanasiou and Papacostas, 2013). Nevertheless, more evidences are needed to unravel the mystery of the oVEMP origin. In sum, compared to ACS mode, BCV mode can provoke higher response rate, generate earlier and larger waveforms, and be influenced by both dynamic shearing force and static gravitational force to enlarge the reflex amplitude of oVEMPs. Thus, BCV mode is preferable to ACS mode in eliciting oVEMPs. We therefore recommend using BCV mode to study oVEMPs for getting more information. 5. Conclusion By altering head postures from sitting to head hanging, static gravitational force can exert a selective effect on the reflex amplitude of oVEMP elicited by BCV stimuli, but not by ACS stimuli. 6. Conflict of Interest None. Acknowledgment Grant no. NSC 100-2314-B002-041-MY3 from National Science Council, Taipei, Taiwan. References Bos JH, Jongkees LB, Philipszoon AJ. On the action of linear accelerations upon the otoliths. Acta Otolaryngol 1963;56:477–89.
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Selective effects of head posture on ocular vestibular-evoked myogenic potential (oVEMP) by bone-conducted vibration Shou-Jen Wang a, Chia-Chen Tseng b, Yi-Ho Young b,⇑ a b
Department of Otolaryngology, Catholic Cardinal Tien Hospital, Fu-Jen Catholic University, Taipei, Taiwan Department of Otolaryngology, National Taiwan University Hospital, Taipei, Taiwan
a r t i c l e
i n f o
Article history: Accepted 2 September 2013 Available online 10 October 2013 Keywords: Dynamic shearing force Head hanging Ocular vestibular-evoked myogenic potential Static gravitational force
h i g h l i g h t s Using bone-conducted vibration (BCV) stimulation, mean nI–pI amplitude with the head hanging
position was significantly larger than that with the sitting position, but not significantly larger than that with the supine position. Using air-conducted sound (ACS) stimulation, mean nI–pI amplitude did not differ significantly among the sitting, supine, and head hanging positions. Gravitational force can exert a selective effect on the reflex amplitude of oVEMPs elicited by BCV stimuli, but not by ACS stimuli.
a b s t r a c t Objective: By altering head postures from sitting, supine to head hanging, this study investigated the effects of gravitational force on ocular vestibular-evoked myogenic potential (oVEMP) via either air-conducted sound (ACS) or bone-conducted vibration (BCV) stimuli. Methods: Twenty healthy volunteers underwent the oVEMP test via ACS or BCV stimuli with the sitting, supine, and head hanging positions on the same day in a randomized order. Results: All subjects had clear BCV oVEMPs in the three head postures. No significant differences existed in terms of mean nI and pI latencies, the nI–pI interval, and asymmetry ratio regardless of various positions. However, the mean nI–pI amplitude with the head hanging position (15.9 ± 6.4 lV) was significantly larger than that with the sitting position (13.8 ± 6.0 lV), but not significantly larger than that with the supine position (14.7 ± 6.1 lV). Nevertheless, such a difference in reflex amplitude does not exist in oVEMPs elicited by ACS stimuli. With the sitting position, mean linear acceleration at the mastoids in response to BCV stimuli was 0.06 ± 0.02, 0.20 ± 0.04 and 0.04 ± 0.02 g along the x-, y-, and z-axis, respectively, which did not differ significantly from those with the head hanging position. Conclusion: By altering head postures from sitting to head hanging, gravitational force can exert a selective effect on the reflex amplitude of oVEMPs elicited by BCV stimuli, but not by ACS stimuli. Significance: Compared to ACS mode, BCV mode can provoke higher response rate, generate earlier and larger waveforms, and be influenced by both dynamic shearing force and static gravitational force to enlarge the reflex amplitude of oVEMPs. Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction In humans, the two otolithic organs, namely the utricle and saccule, are aligned in the horizontal and vertical planes, respectively. Each organ is composed of otoconia (otoliths) embedded in a gelat⇑ Corresponding author. Address: Department of Otolaryngology, National Taiwan University Hospital, 1 Chang-te St., Taipei, Taiwan. Tel.: +886 2 23123456x65221; fax: +886 2 23946774. E-mail address: [email protected] (Y.-H. Young).
inous matrix with a mean thickness of 50 lm, and the gelatinous layer contains hair cells (De Vries, 1951). These otolithic organs can respond to dynamic alternating vibration with shearing movement on the otoconial membrane. The hair cells then transmit displacement information of the otoconial membrane to the central nervous system. Additionally, the otolithic organs also sense static gravitational force, serving a functional role in maintaining postural stability. Clinically, dynamic otolithic function can be assessed by recently emerging vestibular-evoked myogenic potential (VEMP)
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.2013.09.002
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tests via air-conducted sound (ACS) or bone-conducted vibration (BCV) stimuli, including cervical VEMP (cVEMP) recorded on contracted neck muscles, and ocular VEMP (oVEMP) collected on extraocular muscles (Colebatch et al., 1994; Rosengren et al., 2005). Based on the efferent specificity, cVEMP represents predominantly saccular function, while oVEMP reflects mainly utricular function (Curthoys, 2010) although the otolith origin of the oVEMP is not yet universally agreed upon (Colebatch, 2010; Papathanasiou, 2012). Recent studies demonstrated that as linear acceleration increases, oVEMP amplitude enlarges (Todd et al., 2009; Cai et al., 2011; Wang et al., 2012). However, little attention has focused on the impact of static gravitational force on oVEMPs. In humans, Jombík and Bahyl (2005) have first mentioned the effect of interaction of the static gravity vector and dynamic acceleration vector induced by skull bone vibration on the ocular potentials recorded by electrooculography. Later more detailed studies by Ito et al. (2007) revealed that there is some effect of head position in the pitch and roll planes on tonic excitation of the saccule, resulting in altered latencies of cVEMPs. Further, head tilt in the roll plane increased the asymmetry ratio of oVEMP amplitude elicited by BCV stimuli (Iwasaki et al., 2012). Restated, different geometry may reflect a different interaction of the static gravity and the dynamic inertial acceleration vectors. However, the effect of static gravitational force in the pitch plane on oVEMPs remains unclear. By altering head postures from sitting, supine to head hanging, this study investigated the effect of gravitational force on oVEMPs via either ACS or BCV stimuli. 2. Subjects and methods 2.1. Subjects Twenty healthy volunteers, 12 males and 8 females (age, 22– 36 years; mean, 27 years), who denied having previous ear disorders were enrolled. Subjects were further checked by otoscopy and audiometry, confirming intact eardrums and normal hearing. All subjects underwent the oVEMP test via BCV stimuli with the sitting, supine and head hanging positions on the same day randomly. The head hanging position means the subject in a supine position with his/her head hanging backward in a pitch plane maximally without rotating the neck to the roll plane. On another day, all subjects underwent the same test paradigm, but the oVEMP test was performed via ACS stimuli. This study was approved by the institutional review board, and each subject signed the informed consent to participate. 2.2. oVEMP test using BCV stimuli
Fig. 1. Illustration of oVEMP tests by BCV stimuli with the sitting, supine, and head hanging positions.
Surface potentials, predominantly electromyographic (EMG) activities, were recorded (Smart EP 3.90, Intelligent Hearing Systems, Miami, FL, USA). Two active electrodes were placed around 1 cm below the center of the two lower eyelids. The other two reference electrodes were positioned about 1–2 cm below the active ones, and one ground electrode was placed on the sternum. During recording, the subject was instructed to look upward at a small fixed target on the wall >2 m from the eyes under sitting position, on the ceiling >2 m from the eyes under supine position, or on the floor >2 m from the eyes under head hanging position (Fig. 1). A vertical visual angle was approximately 30o above horizontal. The EMG signals were amplified and bandpass filtered between 1 and 1000 Hz (Wang et al., 2013). The stimulation rate was 5/s. The duration of analysis of each response was 50 ms, and 30 responses were averaged for each run. The BCV stimuli used a hand-held electromechanical vibrator (minishaker 4810, Bruel and Kjaer, Naerum, Denmark) fitted with
a short bolt terminated in a bakelite cap. The operator held the vibrator by hand, supported most of its weight, and delivered a repeatable tap on the subject’s skull at Fz (midline of the hairline). The input signal was 500 Hz sine wave, driven by a custom amplifier. The drive voltage was adjusted and fixed to produce a peak force equivalent to 128 dB force level. The initial negative–positive biphasic waveform comprised peaks nI and pI. Consecutive runs were performed to confirm the reproducibility of peaks nI and pI, and oVEMPs were deemed to be present. Thus, latencies of the nI and pI peaks, and amplitude of nI–pI were measured. The asymmetry ratio (%) was defined as the difference of the amplitude nI–pI on each ear divided by the sum of amplitude nI–pI of both ears, that is, (amplitude on the left ear–amplitude on the right ear)/(amplitude on the left ear + amplitude on the right ear) 100 (%).
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2.3. oVEMP test using ACS stimuli All 20 subjects also underwent oVEMP test via ACS stimulation. The latter consisted of 105 dB nHL (127 dB pe SPL) short tone bursts (500 Hz, rise/fall time = 1 ms, plateau time = 2 ms) with rarefaction polarity and were delivered through an insert earphone. The other setting was the same as that stimulated by BCV mode, except that the ground electrode was placed on the forehead. The stimulation rate was 6.7/s and analytical time for each response was 50 ms; 100 responses were averaged for each run. Binaural acoustic stimulation with bilateral recordings was employed (Wang et al., 2009).
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tion magnitudes along the x-, y-, and z-axis in response to BCV stimuli were analyzed by one-way repeated-measures analysis of variance (ANOVA), and Bonferroni-adjusted paired t-test was applied for multiple comparisons. Further, the Student’s t test was used to compare the characteristic parameters between the oVEMP elicited by the two stimuli, whichever in the various positions. The difference of linear acceleration along the x-, y- and z-axes between the sitting and head hanging positions was examined by the paired t test. A significant difference is suggested by a p value <0.05. 3. Results 3.1. BCV oVEMPs
2.4. Triaxial accelerometry at the mastoid One miniature (10 mm3, 5 g) triaxial accelerometer (Endevco model 65-100, San Juan Capistrano, CA, USA) accompanied by a tight elastic bandage surrounding the head girth was fixed to each subject’s left mastoid area just behind the auricle. Using the head as the reference point, the accelerometer was utilized to measure the three-dimensional linear acceleration along the x-axis (anterior–posterior), y-axis (inter-aural), and z-axis (rostro-caudal) simultaneously. Forward, outward, and upward were defined as the positive x, y, and z directions, respectively. The voltage sensitivity was 100 mV/g and the frequency response was 1.5–6000 Hz (±1 dB). The triaxial accelerometer signals were digitalized at 10 kHz using a dynamic signal analyzer (NI USB-4431, National Instruments, Austin, Texas, USA), which provided signal conditioning and constant current supply (2.1 mA) to the accelerometer. The acceleration magnitude was simultaneously measured throughout oVEMP testing, and ten runs of reproducible sweep were recorded. The initial peak magnitudes of linear acceleration were analyzed using a customized program (LabVIEW 8.5, National Instruments, Austin, Texas, USA) (Wang et al., 2012). In total, six subjects (4 men and 2 women, aged 22–34 years) undertook triaxial accelerometry at the mastoid with different head postures randomly.
All twenty healthy volunteers (100%) had clear oVEMPs beneath both eyes by BCV stimuli regardless of whether the subject was positioned in sitting, supine, or head hanging (Fig. 2). Because there were no significant differences in the characteristic parameters between the right and left oVEMPs, and the asymmetry ratios of amplitude were well below 40%, the values for both eyes were therefore pooled for subsequent analyses. The mean nI and pI latencies in the sitting position were 8.3 ± 0.4 (mean ± SD) and 12.3 ± 1.1 ms, respectively, not significantly different from those in the supine and head hanging position (p > 0.05, one-way repeated-measures ANOVA, Table 1). Similarly, no significant differences in the nI–pI interval and asymmetry ratio existed regardless of various positions (p > 0.05, Table 1). However, there were significant differences in the nI–pI amplitudes among the three positions (p < 0.05, one-way repeated-measures ANOVA, Table 1). Bonferroni-adjusted paired t-test demonstrated that mean nI–pI amplitude with the head hanging position (15.9 ± 6.4 lV) was significantly larger than that with the sitting position (13.8 ± 6.0 lV) (p < 0.05, Table 1), but the nI–pI amplitudes did not significantly differ between the sitting and supine positions or between the supine and head hanging positions (p > 0.05, Table 1).
2.5. Statistical methods
3.2. ACS oVEMPs
The response rate among the three positions was compared by the Cochran’s Q test. The characteristic parameters, either using different stimuli, among the three head postures and the accelera-
All subjects also participated in oVEMP testing by ACS stimuli (Fig. 3). Thirty-two (80%) of 40 ears had clear oVEMPs in the sitting position, not significantly different from the response rate of 80%
Fig. 2. Male, 25 years old, oVEMPs by BCV stimuli. There are significant differences in the nI–pI amplitudes among the three positions. The nI–pI amplitudes with the head hanging position (R/L: 18.1/19.7 lV) are larger than those with the sitting position (R/L: 14.0/14.9 lV), but do not significantly differ from those with supine position (R/L: 15.8/16.9 lV).
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Table 1 Comparison of BCV oVEMPs among the three positions. Position
N (ears)
Response rate (%)
nI latency (ms)
pI latency (ms)
nI-pI interval (ms)
nI–pI amplitude (lV)
Asymmetry ratio (%)
Sitting Supine Head hanging p Value
40 40 40
100 100 100
8.3 ± 0.4 8.3 ± 0.5 8.4 ± 0.4 >0.05
12.3 ± 1.1 12.3 ± 1.0 12.4 ± 0.9 >0.05
4.0 ± 1.0 4.0 ± 0.9 4.1 ± 0.8 >0.05
13.8 ± 6.0 14.7 ± 6.1 15.9 ± 6.4* <0.05
3.7 ± 10.3 3.0 ± 8.5 0.7 ± 10.8 >0.05
Data are expressed as mean ± SD; p value: one-way repeated-measures ANOVA test. p < 0.05, Bonferroni-adjusted paired t-test for multiple comparisons, as compared with the nI–pI amplitude with the sitting position.
*
(32/40 ears) in the supine or head hanging position (p > 0.05, Cochran’s Q test). The mean latencies of nI and pI, the nI–pI interval, nI– pI amplitude, and asymmetry ratio did not significantly differ among the three positions (p > 0.05, one-way repeated-measures ANOVA, Table 2). 3.3. BCV oVEMPs vs. ACS oVEMPs The characteristic parameters of BCV oVEMPs and ACS oVEMPs were analyzed. With the sitting position, the mean nI and pI latencies of BCV oVEMPs (8.3 ± 0.4 and 12.3 ± 1.1 ms) were significantly earlier than the respective 10.6 ± 0.7 and 15.5 ± 1.4 ms of ACS oVEMPs (p < 0.05, Student’s t test). In terms of nI–pI amplitude, BCV oVEMPs (13.8 ± 6.0 lV) had significantly larger responses than ACS oVEMPs (8.3 ± 3.0 lV) (p < 0.05). Similar differences also existed with the supine or head hanging position. 3.4. Triaxial acceleration: sitting vs. head hanging positions Since the nI–pI amplitudes did not significantly differ between the supine position and sitting/head hanging position, comparison of the triaxial acceleration was thus conducted between sitting and head hanging positions. In response to BCV stimuli at Fz, mean lin-
ear acceleration at the mastoids were 0.06 ± 0.02 g along the xaxis, 0.20 ± 0.04 g along the y-axis, and 0.04 ± 0.02 g along the z-axis with the sitting position, not significantly different from the 0.05 ± 0.02, 0.19 ± 0.03, and 0.04 ± 0.01 g along the respective axis with the head hanging position (p > 0.05, paired t test). Among the three axes, the largest acceleration magnitude was along the y-axis regardless of sitting or head hanging position (p < 0.01, one-way repeated measures ANOVA and Bonferroni adjusted paired t-test). 4. Discussion Similar to the linear accelerometer in the contemporary smartphone which senses device direction, the otolithic organs in the temporal bone detect static gravitational force and help determine the head’s orientation. This is likely because regularly firing otolithic afferents change their sensitivity with respect to variations in gravitational force (Fernandez and Goldberg, 1976). During linear acceleration tangential to the surface of the utricular macula, two vector forces, namely, dynamic shearing force and static gravitational force, instantaneously act upon the macula (De Vries, 1951). To ascertain the sensitivity of the utricle under these circumstances, 20 healthy subjects under-
Fig. 3. Same subject as in Fig. 2, oVEMPs by ACS stimuli. The nI–pI amplitudes do not differ significantly among the three positions (sitting: R/L: 6.5/7.6 lV; supine: R/L: 6.6/ 6.9 lV; head hanging: R/L: 6.7/7.4 lV).
Table 2 Comparison of ACS oVEMPs among the three positions. Position
N (ears)
Response rate (%)
nI latency (ms)
pI latency (ms)
nI-pI interval (ms)
nI-pI amplitude (lV)
Asymmetry ratio (%)
Sitting Supine Head hanging p value
40 40 40
80 80 80
10.6 ± 0.7 10.7 ± 0.7 10.6 ± 0.6 >0.05
15.5 ± 1.4 15.7 ± 1.3 15.5 ± 1.3 >0.05
4.9 ± 1.1 5.0 ± 1.1 4.9 ± 1.2 >0.05
8.3 ± 3.0 8.0 ± 3.1 8.2 ± 2.9 >0.05
1.9 ± 17.3 -0.9 ± 18.0 0.2 ± 17.6 >0.05
Data are expressed as mean ± SD; p value: one-way repeated-measures ANOVA test.
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went oVEMP testing via BCV stimuli with the sitting, supine, and head hanging positions (Fig. 1). No significant differences were evident in terms of nI and pI latencies, the nI–pI interval, or the asymmetry ratio among the three positions (Table 1). However, mean amplitude of oVEMPs with the head hanging position was significantly larger than that with the sitting position (Fig. 2), probably due to the effect of dynamic shearing force or static gravitational force.
4.1. Effect of dynamic shearing force on oVEMPs Dynamic shearing force was measured with triaxial accelerometry at the mastoid and represented as three-dimensional linear acceleration. With the sitting or head hanging position, the largest acceleration magnitude was along the y-axis i.e., interaural direction, which is compatible with previous reports (Iwasaki et al., 2008; Wang et al., 2012). A comparison of linear acceleration in the sitting and head hanging positions revealed no significant difference along the x-, y-, or z-axis. Restated, the dynamic shearing force induced by BCV stimuli was unrelated to the two head positions. Instead, large oVEMP amplitudes with the head hanging position may be caused by altered direction of static gravitational force.
4.2. Effect of static gravitational force on oVEMPs The position of a load on the otolithic receptors depends on the magnitude and direction of the force acting upon it. Morphologically, the otoconial membrane is above the utricular maculae in the sitting position, and vice versa in the head hanging position (Fig. 4). When the otoliths were hanging perpendicularly in the endolymphatic space, the otoconial membrane may apply stronger shearing force upon the nearby stereocilia (Bos et al., 1963; Jongkees and Philipszoon, 1963). Thus, as compared with the BCV oVEMPs in the sitting position, enlarged reflex amplitude was noted in the head hanging position, but not in the intermediate (supine) position (Table 1). Restated, when the utricular otoliths hang beneath the macula, increased sensitivity to linear acceleration leads to an enlarged effect on the reflex amplitude of BCV oVEMP. Similarly, amplitude of the first wave in vestibular evoked potentials (VsEP) to linear acceleration stimuli would be greater in the ‘‘head up’’ position of rats when compared to that in the ‘‘head down’’ position (Plotnik et al., 1999). However, such an enlarged effect was not observed in the reflex amplitude of oVEMPs via ACS stimulation (Fig. 3), as demonstrated by no significant difference in reflex amplitudes among the three positions (Table 2). The main reason is because both stimulation modes act differently. The BCV stimuli exerted to the head cause vibrational waves to travel around and through the head, resulting in linear accelerations at the mastoids (Iwasaki et al., 2008; Todd et al., 2009). Conversely, ACS stimuli cannot provoke skull acceleration, but act moving the perilymph and saccular membrane, which then causes movement in the endolymph. One may argue that the enlarged effect might be caused by different involvement of the neck proprioceptors in the two positions. In contrast to the sitting position, the neck is bent in the head hanging position, implying that the positions of head and torso are different with respect to each other. However, it had been reported that changes in the cervical input did not influence oVEMPs in response to BCV stimuli (Iwasaki et al., 2012). Thus, this possibility could be neglected, plausibly because the pathway mediating the cervico-ocular reflex is polysynaptic and this reflex would not occur with latency less than 40 ms (Popov et al., 1999).
Fig. 4. Illustration of the relationships between the otoconia and utricular macula in sitting vs. head hanging positions. The utricle is composed of otoconia (grey area) embedded in a gelatinous matrix, and the gelatinous layer contains hair cells.
4.3. BCV oVEMPs vs. ACS oVEMPs Both BCV and ACS stimulation modes have been widely used to elicit oVEMPs in clinical patients (Young, 2013). Since both modes
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can activate otolithic maculae, many laboratories utilized ACS mode instead of BCV mode to eliminate the need to purchase a new instrument. Thus, differences between ACS oVEMPs and BCV oVEMPs warrant further investigation. First, the mean latencies of nI and pI, and the nI–pI interval of ACS oVEMPs were significantly prolonged when compared with those of BCV oVEMPs, regardless of head position. The variation between stimulation duration (ACS of 4 ms and BCV of 1 ms) may account for this difference. Second, the response rate and reflex amplitude of ACS oVEMPs were significantly less than those of BCV oVEMPs, regardless of the sitting, supine, or head hanging position. These findings may be because the two stimuli evoked dissimilar populations of otolithic afferents (Iwasaki et al., 2012). Although ACS stimuli are suitable for activating otolithic afferents (Murofushi et al., 1995), they are not sufficiently effective for eliciting oVEMPs (Chihara et al., 2007; Cheng et al., 2009; Wang et al., 2010), probably because only some irregular otolithic afferents are activated by the ACS stimuli. On the other hand, BCV mode might activate irregular otolithic afferents more efficiently, leading to larger reflex amplitude when compared with that in ACS mode (Curthoys and Vulovic, 2011). Another possibility for the differences between ACS oVEMPs and BCV oVEMPs is that ACS mode mainly activates the saccular macula and BCV mode stimulates the utricle. As the macula in the saccule is vertically orientated, and the macula in the utricle is horizontally orientated, one would expect that rotation in the pitch plane would affect the saccule and the utricle differently (Welgampola and Colebatch, 2005; Papathanasiou and Papacostas, 2013). Nevertheless, more evidences are needed to unravel the mystery of the oVEMP origin. In sum, compared to ACS mode, BCV mode can provoke higher response rate, generate earlier and larger waveforms, and be influenced by both dynamic shearing force and static gravitational force to enlarge the reflex amplitude of oVEMPs. Thus, BCV mode is preferable to ACS mode in eliciting oVEMPs. We therefore recommend using BCV mode to study oVEMPs for getting more information. 5. Conclusion By altering head postures from sitting to head hanging, static gravitational force can exert a selective effect on the reflex amplitude of oVEMP elicited by BCV stimuli, but not by ACS stimuli. 6. Conflict of Interest None. Acknowledgment Grant no. NSC 100-2314-B002-041-MY3 from National Science Council, Taipei, Taiwan. References Bos JH, Jongkees LB, Philipszoon AJ. On the action of linear accelerations upon the otoliths. Acta Otolaryngol 1963;56:477–89.
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