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Earlier and later components of tone burst evoked myogenic potentials
Hearing Research 191 (2004) 59–66 www.elsevier.com/locate/heares
Earlier and later components of tone burst evoked myogenic potentials Chi-Te Wang, Yi-Ho Young
*
Department of Otolaryngology, National Taiwan University Hospital, National Taiwan University College of Medicine, 1 Chang-Te Street, Taipei, Taiwan Received 21 September 2003; accepted 1 January 2004
Abstract The aim of this study was to further investigate the response rates, thresholds, latencies and amplitudes of the earlier and later components of tone burst evoked myogenic potentials (TEMPs) in conditions of binaural and monaural stimulation and recordings in a group of normal subjects in response to a 500-Hz tone burst. Each subject underwent simultaneous binaural acoustic stimulation with bilateral recording (B-TEMP) initially, then monaural acoustic stimulation with ipsilateral recording (M-TEMP) on another day. The results showed 100%, 100%, 54%, and 23% response rates for the earlier components of B-TEMPs, when using 105, 95, 85, and 75 dB acoustic stimulation, respectively. It exhibited a significant decrease in the response rate when the stimulus intensity was attenuated from 95 to 75 dB. In addition, no significant difference in the response rate of the earlier components existed between B-TEMPs and M-TEMPs. For the later components of B-TEMPs obtained from 105, 95, 85, and 75 dB acoustic stimulation, the response rates were 85%, 85%, 62%, and 42%, respectively, higher than those of M-TEMPs significantly. Nevertheless, there were no statistical differences in the mean latencies of each peak (p13, n23, n34, and p44) between B-TEMPs and M-TEMPs under similar stimulus intensity. Meanwhile, no significant relationship existed between the stimulus intensity and the latency, regardless of B-TEMPs or M-TEMPs. Comparing the relative amplitudes between B-TEMPs and M-TEMPs, the former displayed significant smaller p13-n23 amplitude, but larger n34-p44 amplitude. However, the mean thresholds for the earlier and later components between B-TEMPs and M-TEMPs did not differ significantly. In conclusion, monaural acoustic stimulation with ipsilateral recording may elicit larger amplitude of the earlier components, whereas binaural acoustic stimulation with bilateral recording evokes higher response rate and larger amplitude of the later components. Although the nerve pathways for both components are different, the thresholds for these potentials do not differ significantly, indicating that both components may, at least in part, share a common origin, but different pathways. Ó 2004 Elsevier B.V. All rights reserved. Keywords: Earlier component; Later component; Monaural acoustic stimulation; Binaural acoustic stimulation; Vestibular evoked myogenic potential; Tone burst
1. Introduction Bickford et al. (1964) demonstrated that loud acoustic stimuli could cause myogenic ‘‘inion response’’ * Corresponding author. Tel.: +886-2-2312-3456x5221; fax: +886-22394-6674. E-mail address: [email protected] (Y.-H. Young). Abbreviations: B-TEMP, tone burst evoked myogenic potential by simultaneous binaural acoustic stimulation; EMG, electromyography; M-TEMP, tone burst evoked myogenic potential by monaural acoustic stimulation; SCM, sternocleidomastoid; TEMP, tone burst evoked myogenic potential; VEMP, vestibular evoked myogenic potential
0378-5955/$ - see front matter Ó 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2004.01.004
indicative of the activation of vestibular organs. However, it was not until the revision of the recording setting by Colebatch and Halmagyi (1992) that vestibular evoked myogenic potential (VEMP) became a reliable clinical test. It can easily be recorded from the ipsilateral contracting sternocleidomastoid (SCM) muscle by stimulation with loud clicks (Murofushi et al., 1996) or tone bursts (Wu et al., 1999). Colebatch et al. (1994) labeled the serial peaks (p13, n23, n34, p44) of the evoked response according to their latencies, and found that the earlier components (p13, n23) were present in all normal subjects, whereas the later components (n34,
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p44) were only present in 60% of the subjects. Since the inconsistency of the later components, researchers in the past decade almost focused on investigating the clinical significance of the earlier components (Murofushi et al., 2001; Wu et al., 2003; Young et al., 2003). The earlier components of VEMPs are generated via a disynaptic pathway. It begins in the saccular macula, via the inferior vestibular nerve, lateral vestibular nucleus, medial vestibulospinal tract, and terminating to the motor neurons of the SCM muscle (Didier and Cazals, 1989; Kushiro et al., 1999; Murofushi et al., 1995; Sato et al., 1997; Uchino et al., 1997). However, the mechanism for the later components (n34, p44) remains poorly understood. Some investigations contended that later components might be of cochlear origin, since they could be obtained in ears after selective vestibular nerve section (Colebatch et al., 1994). Our recent study reveals that the earlier components of the VEMPs are intact after sudden deafness. In contrast, the response rate of the later components is present as 45% in the deaf ears, 60% in the contralateral ears, and 55% in the normal control ears, showing no significant difference among them (Wu and Young, 2002). Although these results might be explained by a dual origin (both cochlear and vestibular), actual mechanism for the later components has not yet been elucidated. There is a consensus that amplitude of the earlier components depends on the stimulus intensity and voluntary muscular effort obtained by monaural acoustic stimulation (Lim et al., 1995). Whether increased stimulus intensity affecting the response rate of the later components remains unexplored. Since the later components are elicited bilaterally (Colebatch et al., 1994), VEMP test via binaural simultaneous acoustic stimulation (Wang and Young, 2003) may help to evoke higher consistency of the later components. Hence, the aim of this study was to further investigate the response rates, thresholds, latencies and amplitudes of the earlier and later components of tone burst evoked myogenic potentials (TEMPs) in conditions of binaural and monaural stimulation and recordings in a group of normal subjects in responses to a 500-Hz tone burst.
2. Materials and methods 2.1. Subjects Thirteen healthy volunteers from medical students and resident doctors (10 men and 3 women; aged from 22 to 35 years, mean of 27 years), without previous ear disorders underwent VEMP test. Each subject was evoked by simultaneous binaural acoustic stimulation, recorded bilaterally (B-TEMPs), using different stimulus intensities. On another day, all volunteers underwent a serial VEMP
testings using monaural tone burst stimulation for each ear separately, recording ipsilaterally (M-TEMPs). 2.2. VEMP test The sternocleidomastoid (SCM) muscle was chosen as the target to record the TEMPs. Surface electromyographic (EMG) activity was recorded (Smart EP2, Intelligent hearing system, USA) on the subject being in a supine position with a 0.9 cm Ag/AgCl electrode on the upper half of the SCM muscle on both sides, and a reference electrode on the lateral end of the upper sternum. During the recording, the instructor kept an eye on the monitor and the subject was instructed to keep the head elevated while in a supine position throughout the entire test. EMG signals were amplified and bandpass filtered between 30 and 3000 Hz, and monitored to maintain muscle activity at a relatively constant level (50–200 lV). When the biphasic waveform became dubious, the subject was aroused to strengthen his/her muscle activity. Acoustic stimuli (short tone bursts; 500 Hz, ramp ¼ 1 ms, plateau ¼ 2 ms) were delivered through an earphone. The stimulation rate was 5 Hz and the analysis time for each response was 60 ms, and 200 responses were averaged for each run. Two consecutive runs were performed on the same ear to verify the reproducibility, and the results were averaged providing the final response. The serial positive/negative polarity of waveforms with peaks termed p13, n23, n34 and p44 based on their latencies were used to determine the presence or absence of the VEMP response. The latencies of each peak (p13, n23, n34 and p44), p13-n23 amplitude, and n34-p44 amplitude were measured. Relative amplitude indicates the amplitude of TEMPs using A method divided by that using B method (Takegoshi and Murofushi, 2003). 2.3. Investigating the thresholds of VEMPs Each subject underwent a serial VEMP testings. Initial stimulus intensity was randomized from either 105 dB HL or 65dB HL, followed by 10-dB step decrement or increment, respectively, until the absence or presence of the waveforms. Subsequent 5-dB step increase or decrease the stimulus intensity until VEMP response reappears, thus the threshold was determined. Using this threshold intensity, two consecutive runs were performed to verify the reproducibility. 2.4. Statistical methods The response rates of all stimulus intensities between B-TEMPs and M-TEMPs were compared by McNemar test. The relationship between the response rates and the stimulus intensities was compared by CochranÕs Q test. The thresholds for the earlier and later components were
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compared using paired or Student t-test. The latencies of p13, n23, n34, and p44 between B-TEMPs and MTEMPs under similar stimulus intensity were compared by paired or Student t-test. The relationship between the stimulus intensity and the latency was analyzed by oneway analysis of variance test. The relative amplitudes of TEMPs between binaural stimulation and monaural stimulation, 105 and 95 dB stimulation, were compared with Wilcoxon signed-ranks test. A significant difference indicates p < 0:05. This study was institutional review board approved, and each subject signed an informed consent.
3. Results 3.1. Comparison of the response rates and thresholds The response rates for the earlier components of BTEMPs using 105, 95, 85 and 75 dB acoustic stimulation were 100%, 100%, 54% and 23%, respectively, exhibiting significant decrease in the response rate when the stimulus intensity was attenuated from 95 to 75 dB (Table 1, CochranÕs Q test, p < 0:01). Similarly, those for the later components of B-TEMPs were 85%, 85%, 62% and 42%, respectively, showing significant decrease in the response rate from 95 to 75 dB stimulus intensity (Table 1, CochranÕs Q test, p < 0:01). Likewise, the response rates for the earlier components of M-TEMPs obtained from 105, 95, 85 and 75 dB acoustic stimulation were 100%, 100%, 38% and 27%, respectively, revealing significant differences among groups of 95, 85 and 75 dB (Table 1, CochranÕs Q test, p < 0:01). Meanwhile, the later components of MTEMPs also demonstrated significant decrease in the response rate when the stimulus intensity was attenuated (Table 1, CochranÕs Q test, p < 0:01).
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Comparison of the response rates for the earlier components between B-TEMPs and M-TEMPs revealed no significant difference under similar stimulus intensity (p < 0:05, McNemar test, Table 1). In contrast, BTEMPs presented higher response rate for the later components than M-TEMPs at all stimulus intensities (p < 0:05, McNemar test, Table 1). The mean thresholds of the earlier components between B-TEMPs (Fig. 1) and M-TEMPs (Fig. 2) were 85 8 (mean SD) dB and 88 10 dB, respectively, showing no significant difference (p > 0:05, paired ttest). Meanwhile, there was also no statistical difference in mean thresholds for the later components between BTEMPs (83 9 dB) and M-TEMPs (85 10 dB) (p > 0:05, Student t-test). Likewise, the mean thresholds of the earlier versus later components did not differ significantly, regardless of B-TEMPs or M-TEMPs (p > 0:05, Student t-test, Table 1). 3.2. Comparison of the latencies The mean latencies of p13, n23, n34 and p44 for the B-TEMPs using 105 dB acoustic stimulation were 13.82 1.07 ms, 20.35 1.60 ms, 31.68 1.46 ms, and 37.42 1.68 ms, respectively. Compared to those for the M-TEMPs: 14.08 1.27 ms, 20.66 1.52 ms, 31.86 2.16 ms, and 38.18 2.03 ms, respectively, revealed no significant difference between these values. Likewise, there was no significant difference in the latencies of p13, n23, n34 and p44 between the B-TEMPs and M-TEMPs, respectively, when using 95, 85, or 75 dB tone burst stimulation (paired or Student t-test, p > 0:05) (Table 2). Furthermore, there was no significant relationship between the stimulus intensity and the mean latency, despite using binaural or monaural stimulation and recordings (p > 0:05, one-way analysis of variance test, Table 2).
Table 1 Comparison of response rates and thresholds of the earlier and later components of tone burst evoked myogenic potentials among different stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB 85 dB 75 dB
N (ears)
B-TEMP p13-n23
p13-n23
26 26 26 26
26 (100%) 26 (100%)* 14 (54%)* 6 (23%)*
26 (100%) 26 (100%)# 10 (38%)# 7 (27%)#
p > 0:05 (McNemar test) p > 0:05 (McNemar test)
85 8 dB
88 10 dB
p > 0:05 (paired t-test)
n34-p44
n34-p44
22 22 16 11
11 (42%) 11 (42%)## 3 (12%)## 2 (8%)##
< 0:05 < 0:05 < 0:05 < 0:05
85 10 dB
p > 0:05 (Student t-test)
Thresholds (mean SD)
105 dB 95 dB 85 dB 75 dB Thresholds (mean SD)
26 26 26 26
(85%) (85%)** (62%)** (42%)**
83 9 dB
*,**,#,##: p < 0:01, among three groups, CochranÕs Q test.
M-TEMP
p-Value
(McNemar (McNemar (McNemar (McNemar
test) test) test) test)
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Fig. 1. Myogenic potentials evoked by simultaneous binaural acoustic stimulation using tone burst with different stimulus intensities in a 22-year-old man. It reveals the thresholds as 75 dB for both p13-n23 and n34-p44 components, bilaterally. (I, p13; II, n23; III, n34; IV, p44; 105B: 105 dB, binaural stimulation; A, right side recording; B, left side recording.)
Fig. 2. Myogenic potentials evoked by monaural acoustic stimulation using tone burst with different stimulus intensities in a 24-year-old man. It reveals the thresholds as 70 dB for both p13-n23 and n34-p44 components of the right side, and 75 dB for both components of the left side. (I, p13; II, n23; III, n34; IV, p44; 105, 105 dB, R, right ear stimulation; A, right side recording; L, left ear stimulation; B, left side recording.)
3.3. Comparison of the amplitudes Because the amplitude of the VEMP varies substantially between subjects, the relative amplitude (amplitude of B-TEMP divided by that of M-TEMP) was used for comparison. The median relative amplitudes for the earlier components were 0.95 (0.69–1.18) [median (minimum–maximum)], 0.87 (0.52–1.27), 0.87 (0.63– 0.96), and 0.85 (0.73–0.97), when using 105, 95, 85, and 75 dB acoustic stimulation, respectively. It revealed
significant decrease in the p13-n23 amplitude of BTEMPs at all stimulus intensities, when compared with the respective group of M-TEMPs (p < 0:05, Wilcoxon signed-ranks test, Table 3). In contrast, the median relative amplitudes of the later components (n34-p44) obtained from 105, 95, 85, and 75 dB stimulation, were 1.29 (0.91–1.97) [median (minimum–maximum)], 1.18 (0.70–2.30), 1.73 (1.59– 2.86), and 1.25 (1.12–1.40), respectively. It showed significant larger n34-p44 amplitude of B-TEMPs than
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Table 2 Comparison of latencies of the earlier and later components of tone burst evoked myogenic potentials among different stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB 85 dB 75 dB
N (ears)
B-TEMP Latency p13 (ms)
Latency n23 (ms)
26 26 14 6
13.82 1.07 13.53 1.60 13.06 0.96 12.62 1.07
20.35 1.60 20.30 1.60 19.68 1.00 19.52 1.80
(p > 0:05)
(p > 0:05)
(p > 0:05)
(p > 0:05)
Latency n34 (ms)
Latency p44 (ms)
Latency n34 (ms)
Latency p44 (ms)
31.68 1.46 31.33 2.26 30.72 0.83 31.30 0.64
37.42 1.68 36.62 2.07 37.32 1.08 37.30 1.23
31.86 2.16 31.30 1.28 31.50 1.32 31.38 1.59
38.18 2.03 37.36 1.47 38.17 0.73 37.88 1.06
(p > 0:05)
(p > 0:05)
p-Value
105 dB 95 dB 85 dB 75 dB
22 22 16 11
p-Value
N (ears)
26 26 10 7
11 11 3 2
M-TEMP Latency p13 (ms)
Latency n23 (ms)
14.08 1.27 13.24 1.09 13.95 1.87 13.18 0.70
20.66 1.52 20.11 1.48 20.34 2.16 19.34 1.15
(NS) (NS) (NS) (NS)
(NS) (NS) (NS) (NS)
(p > 0:05)
(NS) (NS) (NS) (NS)
(NS) (NS) (NS) (NS)
(p > 0:05)
Data are expressed as mean SD. p-Value, relationship between the stimulus intensity and the latency (one-way analysis of variance test). NS, not statistically significant (p > 0:05, paired or Student t-test, B-TEMP group compared with the respective M-TEMP group).
Table 3 Comparison of amplitudes of the earlier and later components of tone burst evoked myogenic potentials among different stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB 85 dB 75 dB
N (ears)
B-TEMP p13-n23 (lV)
N (ears)
M-TEMP p13-n23 (lV)
N (ears)
B-TEMP/M-TEMP Relative amplitude
p-Value
26 26 14 6
116.5 112.6 108.0 102.4
26 26 10 7
142.6 137.6 129.1 119.0
26 26 10 6
0.95 0.87 0.87 0.85
0.013 0.039 0.005 0.028
(58.3–229.2) (61.9–232.7) (51.8–174.9) (84.0–125.7)
n34-p44 (lV) 105 dB 95 dB 85 dB 75 dB
22 22 16 11
145.2 (121.3–177.9) 112.1 (84.8–206.9) 100.0 (73.4–169.8) 99.7 (76.0–181.0)
(81.5–239.0) (86.3–212.6) (82.0–191.4) (93.5–172.5)
n34-p44 (lV) 11 11 3 2
114.5 (61.5–187.8) 99.4 (77.0–149.5) 91.7 (52.7–106.6) 83.7 (81.3–86.2)
(0.69–1.18) (0.52–1.27) (0.63–0.96) (0.73–0.97)
Relative amplitude 11 11 3 2
1.29 1.18 1.73 1.25
(0.91–1.97) (0.70–2.30) (1.59–2.86) (1.12–1.40)
0.046 0.026 0.109 0.180
Data are expressed as median (minimum–maximum). The relative amplitudes between B-TEMP and M-TEMP are compared with Wilcoxon signed-ranks test.
M-TEMPs, when elicited by either 105 or 95 dB acoustic stimulation (p < 0:05, Wilcoxon signed-ranks test, Table 3). However, the relative amplitudes of later components did not reach statistical significance when using 85 or 75 dB tone burst stimulation (p > 0:05, Wilcoxon signed-ranks test, Table 3), possibly due to small sample size (3 ears). Because the amplitude of the VEMP varies substantially in one subject between trials, moreover, less responses obtained from 85 or 75 dB acoustic stimulation, hence only relative amplitudes between 105 and 95 dB groups were compared. The median relative amplitudes (amplitude of 105 dB group divided by that 95 dB group) of the earlier components for B-TEMPs were 1.10 (0.40–2.29) [median (minimum–maximum)], indicating a significant increase in the p13-n23 amplitude of 105 dB group (p < 0:05, Wilcoxon signed-ranks test,
Table 4). Whereas those for the later components of BTEMPs were 1.12 (0.52–1.96) [median (minimum–maximum)], showing non-significant difference (p > 0:05, Wilcoxon signed-ranks test, Table 4). In contrast, the relative amplitudes of both earlier and later components for M-TEMPs between 105 and 95 dB groups demonstrated a significant increase in amplitudes of both components of the 105 dB group (p < 0:05, Wilcoxon signed-ranks test, Table 4). Fig. 3 illustrates the difference between B-TEMPs and M-TEMPs in a 24-year-old healthy subject. Myogenic potentials elicited by monaural 95 dB tone burst stimulation with ipsilateral recording demonstrate earlier components, but without later components. However, both the earlier and later components of myogenic potentials can be obtained when using binaural 95 dB tone burst stimulation with bilateral recording.
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Table 4 Comparison of amplitudes of the earlier and later components of tone burst evoked myogenic potentials between105 and 95 dB stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB
N (ears)
B-TEMP p13-n23 (lV)
N (ears)
M-TEMP p13-n23 (lV)
26 26
116.5 (58.3–229.2) 112.6 (61.9–232.7)
26 26
142.6 (81.5–239.0) 137.6 (86.3–212.6)
Relative amplitude (105 dB/95 dB) p-Value
1.10 (0.40–2.29) 0.020
1.13(0.61–1.93) 0.020 n34-p44 (lV)
105 dB 95 dB Relative amplitude (105 dB/95 dB) p-Value
22 22
145.2 (121.3–177.9) 112.1 (84.8–206.9) 1.12 (0.52–1.96) 0.170
n34-p44 (lV) 11 11
114.5 (61.5–187.8) 99.4 (77.0–149.5) 1.31 (0.99–2.05) 0.028
Data are expressed as median (minimum–maximum). The relative amplitudes between 105 dB group and 95 dB group are compared with Wilcoxon signed-ranks test.
Fig. 3. Myogenic potentials elicited by monaural 95 dB acoustic stimulation (the upper two tracings) showing earlier components (p13, n23) only. Whereas myogenic potentials evoked by binaural 95 dB acoustic stimulation (the lower two tracings) demonstrate both earlier and later (n34, p44) components. (I, p13; II, n23; III, n34; IV, p44; 95R(A): 95 dB, right ear stimulation, right side recording; 95L(B): 95 dB, left ear stimulation, left side recording; 95B(A): 95 dB, binaural stimulation, right side recording; 95B(B): 95 dB, binaural stimulation, left side recording.)
4. Discussion The ideal stimulation mode for tone evoking the earlier components of VEMP is suggested as follows: intensity 95 dB; frequency 500 Hz; stimulation repetition rate 5 Hz; rise/fall time 1 ms; and plateau time 2 ms; recorded unilaterally (Murofushi et al., 1999; Cheng and Murofushi, 2001a,b). The waveform morphology of the VEMP responses observed with this stimulation mode is simultaneously the most constant and remarkable. However, this stimulation mode elicits only 45–60% response rate for the later components (Wu and Young, 2002). Since the earlier components of VEMPs are present with high intensity sound, tone bursts with different stimulus intensities are used to stimulate the ears binaurally or monaurally, in order to investigate the characteristics of the earlier and later components in subjects with normal sacculo-collic reflex.
The results showed 100%, 100%, 54%, and 23% response rates for the earlier components of B-TEMPs, when using 105, 95, 85, and 75 dB acoustic stimulation, respectively, indicating a significant decrease in the response rate when the stimulus intensity was attenuated from 95 to 75 dB (Table 1). In comparison with those for the earlier components of M-TEMPs, 100%, 100%, 38%, and 27% response rate, respectively, revealed no significant difference in these vlues between B-TEMPs and M-TEMPs (Table 1). However, the response rates for the later components of B-TEMPs obtained from 105, 95, 85, and 75 dB acoustic stimulation were 85%, 85%, 62%, and 42%, respectively. Compared to 42%, 42%, 12% and 8% for those of M-TEMPs, respectively, demonstrated significant higher response rates in the later components when using binaural acoustic stimulation (Table 1).
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Nevertheless, there is no statistical difference in the mean latencies of each peak (p13, n23, n34, and p44) between B-TEMPs and M-TEMPs at all stimulus intensities. Meanwhile, there is also no significant relationship between the stimulus intensity and the latency, despite using binaural or monaural stimulation and recordings (Table 2). In comparison with the relative amplitudes of the earlier components between B-TEMPs and M-TEMPs reveals significant reduction in the p13-n23 amplitude in the former (Table 3), compatible with our recent report (Wang and Young, 2003). This is possibly because that the amplitude of ipsilateral B-TEMPs could be contaminated by ÔcrossoverÔ inverted VEMPs (Sato et al., 1997), leading to reduction of the p13-n23 amplitude of B-TEMPs, after subtraction from the contralateral TEMPs. However, the later components in B-TEMPs demonstrate significant larger n34-p44 amplitude than M-TEMPs (Table 3), further supports that the later components originated from bilateral acoustic stimulation (Colebatch et al., 1994). In comparison with the relative amplitudes of the earlier components between 105 and 95 dB groups reveals significant increase in relation to the elevation of the stimulus intensity, regardless of B-TEMPs or MTEMPs (Table 4). Similar condition is also demonstrated in the later components of M-TEMPs. However, the relative amplitudes of the later components of BTEMPs between 105 and 95 dB groups do not differ significantly, possibly because the later components elicited from 105 dB stimulation binaurally have saturated via additive effects from binaural acoustic stimulation (Table 4). Since the amplitudes of the earlier components are larger with monaural acoustic stimulation, whereas amplitudes of the later components are larger with binaural acoustic stimulation, will the thresholds for eliciting both components be different between BTEMPs and M-TEMPs? From Table 1, the mean thresholds for the earlier components elicited by binaural or monaural stimulation were 85 8 and 88 10 dB, respectively, showing non-significant difference. Likewise, there is no significant difference in the mean thresholds of the later components between B-TEMPs and M-TEMPs. Furthermore, the mean thresholds of the earlier versus later components did not differ significantly, regardless of B-TEMPs or M-TEMPs. Compared to the guinea pigs, the threshold for evoking responses of saccular afferent is 60–70 dB above the auditory brainstem response threshold (Murofushi et al., 1995), consistent with our results. Thus, although the earlier components originate ipsilaterally and the later components bilaterally, thresholds for both components do not differ significantly, implying that both components may, at least in part, share a common origin.
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One may ask why the later components demonstrate a 30 ms increased latency? One of the answers is attributable to more synapses leading to longer distance of the nerve pathways. However, some other unknown factors remain to be clarified. Further more clinical patients and experimental animals undergoing VEMP test, using binaural acoustic stimulation with bilateral recording, may help to elucidate the mechanism of the later components.
5. Conclusion Monaural acoustic stimulation with ipsilateral recording may elicit larger amplitude of the earlier components of TEMPs, whereas binaural acoustic stimulation with bilateral recording evokes higher response rate and larger amplitude of the later components. This finding further supports that the earlier components originate from ipsilateral acoustic stimulation, whereas the later components are elicited from bilateral acoustic stimulation. Although the nerve pathways for both components are different, their thresholds do not differ significantly, indicating that both components may, at least in part, share a common origin, but different pathways.
Acknowledgements This work was supported by a research grant (Grant no. NSC 92-2314-B002-349) from National Science Council, Taipei, Taiwan.
References Bickford, R.G., Jacobson, J.L., Cody, D.T.R., 1964. Nature of averaged evoked potentials to sound and other stimuli in man. Ann. NY Acad. Sci. 112, 204–223. Cheng, P.W., Murofushi, T., 2001a. The effect of rise/fall time on vestibular-evoked myogenic potential triggered by short tone bursts. Acta Otolaryngol. 121, 696–699. Cheng, P.W., Murofushi, T., 2001b. The effect of plateau time on vestibular-evoked myogenic potential triggered by tone bursts. Acta Otolaryngol. 121, 935–938. Colebatch, J.G., Halmagyi, G.M., 1992. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 42, 1635–1636. Colebatch, J.G., Halmagyi, G.M., Skuse, N.F., 1994. Myogenic potentials generated by a click-evoked vestibulocollic reflex. J. Neurol. Neurosurg. Psychiatr. 57, 190–197. Didier, A., Cazals, Y., 1989. Acoustic responses recorded from the saccule bundle on the eighth nerve of the guinea pigs. Hear. Res. 37, 123–128. Kushiro, K., Zakir, M., Ogawa, Y., et al., 1999. Saccular and utricular inputs to sternocleidomastoid motorneurons of decerebrate cat. Exp. Brain Res. 126, 410–416. Lim, C.L., Clouston, P., Sheean, G., Yiannikas, C., 1995. The influence of voluntary EMG activity and click intensity on the
66
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vestibular click evoked myogenic potential. Muscle Nerve 18, 1210–1213. Murofushi, T., Curthoys, I.S., Gilchrist, D.P., 1996. Response of guinea pig vestibular nucleus neurons to clicks. Exp. Brain Res. 111, 149–152. Murofushi, T., Curthoys, I.S., Topple, A.N., Colebatch, J.G., Halmagyi, G.M., 1995. Responses of guinea pig primary vestibular neurons to clicks. Exp. Brain Res. 103, 174–178. Murofushi, T., Matsuzaki, M., Wu, C.H., 1999. Short tone burstevoked myogenic potentials on sternocleidomastoid muscle. Are these potentials also of vestibular origin? Arch. Otolaryngol. Head Neck Surg. 125, 660–664. Murofushi, T., Shimizu, K., Takegoshi, H., Cheng, P.W., 2001. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potential. Arch. Otolaryngol. Head Neck Surg. 127, 1069–1072. Sato, H., Imagawa, M., Isu, M., Uchino, Y., 1997. Properties of saccular nerve-activated vestibulo-spinal neurons in cats. Exp. Brain Res. 116, 381–388.
Uchino, Y., Sato, H., Sasaki, M., et al., 1997. Sacculocollic reflex arcs in cats. J. Neurophysiol. 77, 3003–3012. Takegoshi, H., Murofushi, T., 2003. Effect of white noise on vestibular evked myogenic potentials. Hear. Res. 176, 59–64. Wang, S.J., Young, Y-H., 2003. Vestibular evoked myogenic potentials using simultaneous binaural acoustic stimulation. Hear. Res. 185, 43–48. Wu, C.H., Young, Y-H., Murofushi, T., 1999. Tone burst-evoked myogenic potentials in human neck flexor and extensor. Acta Otolaryngol. Stockholm 119, 741–744. Wu, C.C., Young, Y-H., 2002. Vestibular evoked myogenic potentials are intact after sudden deafness. Ear Hearing 23, 235– 238. Wu, C.C., Young, Y-H., Ko, J.Y., 2003. Effect of irradiation on vestibular evoked myogenic potentials on nasopharyngeal carcinoma survivors. Head Neck 25, 482–487. Young, Y-H., Huang, T.W., Cheng, P.W., 2003. Assessing the stage of MeniereÕs disease using vestibular evoked myogenic potentials. Arch. Otolaryngol. Head Neck Surg. 129, 815–818.
Earlier and later components of tone burst evoked myogenic potentials Chi-Te Wang, Yi-Ho Young
*
Department of Otolaryngology, National Taiwan University Hospital, National Taiwan University College of Medicine, 1 Chang-Te Street, Taipei, Taiwan Received 21 September 2003; accepted 1 January 2004
Abstract The aim of this study was to further investigate the response rates, thresholds, latencies and amplitudes of the earlier and later components of tone burst evoked myogenic potentials (TEMPs) in conditions of binaural and monaural stimulation and recordings in a group of normal subjects in response to a 500-Hz tone burst. Each subject underwent simultaneous binaural acoustic stimulation with bilateral recording (B-TEMP) initially, then monaural acoustic stimulation with ipsilateral recording (M-TEMP) on another day. The results showed 100%, 100%, 54%, and 23% response rates for the earlier components of B-TEMPs, when using 105, 95, 85, and 75 dB acoustic stimulation, respectively. It exhibited a significant decrease in the response rate when the stimulus intensity was attenuated from 95 to 75 dB. In addition, no significant difference in the response rate of the earlier components existed between B-TEMPs and M-TEMPs. For the later components of B-TEMPs obtained from 105, 95, 85, and 75 dB acoustic stimulation, the response rates were 85%, 85%, 62%, and 42%, respectively, higher than those of M-TEMPs significantly. Nevertheless, there were no statistical differences in the mean latencies of each peak (p13, n23, n34, and p44) between B-TEMPs and M-TEMPs under similar stimulus intensity. Meanwhile, no significant relationship existed between the stimulus intensity and the latency, regardless of B-TEMPs or M-TEMPs. Comparing the relative amplitudes between B-TEMPs and M-TEMPs, the former displayed significant smaller p13-n23 amplitude, but larger n34-p44 amplitude. However, the mean thresholds for the earlier and later components between B-TEMPs and M-TEMPs did not differ significantly. In conclusion, monaural acoustic stimulation with ipsilateral recording may elicit larger amplitude of the earlier components, whereas binaural acoustic stimulation with bilateral recording evokes higher response rate and larger amplitude of the later components. Although the nerve pathways for both components are different, the thresholds for these potentials do not differ significantly, indicating that both components may, at least in part, share a common origin, but different pathways. Ó 2004 Elsevier B.V. All rights reserved. Keywords: Earlier component; Later component; Monaural acoustic stimulation; Binaural acoustic stimulation; Vestibular evoked myogenic potential; Tone burst
1. Introduction Bickford et al. (1964) demonstrated that loud acoustic stimuli could cause myogenic ‘‘inion response’’ * Corresponding author. Tel.: +886-2-2312-3456x5221; fax: +886-22394-6674. E-mail address: [email protected] (Y.-H. Young). Abbreviations: B-TEMP, tone burst evoked myogenic potential by simultaneous binaural acoustic stimulation; EMG, electromyography; M-TEMP, tone burst evoked myogenic potential by monaural acoustic stimulation; SCM, sternocleidomastoid; TEMP, tone burst evoked myogenic potential; VEMP, vestibular evoked myogenic potential
0378-5955/$ - see front matter Ó 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2004.01.004
indicative of the activation of vestibular organs. However, it was not until the revision of the recording setting by Colebatch and Halmagyi (1992) that vestibular evoked myogenic potential (VEMP) became a reliable clinical test. It can easily be recorded from the ipsilateral contracting sternocleidomastoid (SCM) muscle by stimulation with loud clicks (Murofushi et al., 1996) or tone bursts (Wu et al., 1999). Colebatch et al. (1994) labeled the serial peaks (p13, n23, n34, p44) of the evoked response according to their latencies, and found that the earlier components (p13, n23) were present in all normal subjects, whereas the later components (n34,
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p44) were only present in 60% of the subjects. Since the inconsistency of the later components, researchers in the past decade almost focused on investigating the clinical significance of the earlier components (Murofushi et al., 2001; Wu et al., 2003; Young et al., 2003). The earlier components of VEMPs are generated via a disynaptic pathway. It begins in the saccular macula, via the inferior vestibular nerve, lateral vestibular nucleus, medial vestibulospinal tract, and terminating to the motor neurons of the SCM muscle (Didier and Cazals, 1989; Kushiro et al., 1999; Murofushi et al., 1995; Sato et al., 1997; Uchino et al., 1997). However, the mechanism for the later components (n34, p44) remains poorly understood. Some investigations contended that later components might be of cochlear origin, since they could be obtained in ears after selective vestibular nerve section (Colebatch et al., 1994). Our recent study reveals that the earlier components of the VEMPs are intact after sudden deafness. In contrast, the response rate of the later components is present as 45% in the deaf ears, 60% in the contralateral ears, and 55% in the normal control ears, showing no significant difference among them (Wu and Young, 2002). Although these results might be explained by a dual origin (both cochlear and vestibular), actual mechanism for the later components has not yet been elucidated. There is a consensus that amplitude of the earlier components depends on the stimulus intensity and voluntary muscular effort obtained by monaural acoustic stimulation (Lim et al., 1995). Whether increased stimulus intensity affecting the response rate of the later components remains unexplored. Since the later components are elicited bilaterally (Colebatch et al., 1994), VEMP test via binaural simultaneous acoustic stimulation (Wang and Young, 2003) may help to evoke higher consistency of the later components. Hence, the aim of this study was to further investigate the response rates, thresholds, latencies and amplitudes of the earlier and later components of tone burst evoked myogenic potentials (TEMPs) in conditions of binaural and monaural stimulation and recordings in a group of normal subjects in responses to a 500-Hz tone burst.
2. Materials and methods 2.1. Subjects Thirteen healthy volunteers from medical students and resident doctors (10 men and 3 women; aged from 22 to 35 years, mean of 27 years), without previous ear disorders underwent VEMP test. Each subject was evoked by simultaneous binaural acoustic stimulation, recorded bilaterally (B-TEMPs), using different stimulus intensities. On another day, all volunteers underwent a serial VEMP
testings using monaural tone burst stimulation for each ear separately, recording ipsilaterally (M-TEMPs). 2.2. VEMP test The sternocleidomastoid (SCM) muscle was chosen as the target to record the TEMPs. Surface electromyographic (EMG) activity was recorded (Smart EP2, Intelligent hearing system, USA) on the subject being in a supine position with a 0.9 cm Ag/AgCl electrode on the upper half of the SCM muscle on both sides, and a reference electrode on the lateral end of the upper sternum. During the recording, the instructor kept an eye on the monitor and the subject was instructed to keep the head elevated while in a supine position throughout the entire test. EMG signals were amplified and bandpass filtered between 30 and 3000 Hz, and monitored to maintain muscle activity at a relatively constant level (50–200 lV). When the biphasic waveform became dubious, the subject was aroused to strengthen his/her muscle activity. Acoustic stimuli (short tone bursts; 500 Hz, ramp ¼ 1 ms, plateau ¼ 2 ms) were delivered through an earphone. The stimulation rate was 5 Hz and the analysis time for each response was 60 ms, and 200 responses were averaged for each run. Two consecutive runs were performed on the same ear to verify the reproducibility, and the results were averaged providing the final response. The serial positive/negative polarity of waveforms with peaks termed p13, n23, n34 and p44 based on their latencies were used to determine the presence or absence of the VEMP response. The latencies of each peak (p13, n23, n34 and p44), p13-n23 amplitude, and n34-p44 amplitude were measured. Relative amplitude indicates the amplitude of TEMPs using A method divided by that using B method (Takegoshi and Murofushi, 2003). 2.3. Investigating the thresholds of VEMPs Each subject underwent a serial VEMP testings. Initial stimulus intensity was randomized from either 105 dB HL or 65dB HL, followed by 10-dB step decrement or increment, respectively, until the absence or presence of the waveforms. Subsequent 5-dB step increase or decrease the stimulus intensity until VEMP response reappears, thus the threshold was determined. Using this threshold intensity, two consecutive runs were performed to verify the reproducibility. 2.4. Statistical methods The response rates of all stimulus intensities between B-TEMPs and M-TEMPs were compared by McNemar test. The relationship between the response rates and the stimulus intensities was compared by CochranÕs Q test. The thresholds for the earlier and later components were
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compared using paired or Student t-test. The latencies of p13, n23, n34, and p44 between B-TEMPs and MTEMPs under similar stimulus intensity were compared by paired or Student t-test. The relationship between the stimulus intensity and the latency was analyzed by oneway analysis of variance test. The relative amplitudes of TEMPs between binaural stimulation and monaural stimulation, 105 and 95 dB stimulation, were compared with Wilcoxon signed-ranks test. A significant difference indicates p < 0:05. This study was institutional review board approved, and each subject signed an informed consent.
3. Results 3.1. Comparison of the response rates and thresholds The response rates for the earlier components of BTEMPs using 105, 95, 85 and 75 dB acoustic stimulation were 100%, 100%, 54% and 23%, respectively, exhibiting significant decrease in the response rate when the stimulus intensity was attenuated from 95 to 75 dB (Table 1, CochranÕs Q test, p < 0:01). Similarly, those for the later components of B-TEMPs were 85%, 85%, 62% and 42%, respectively, showing significant decrease in the response rate from 95 to 75 dB stimulus intensity (Table 1, CochranÕs Q test, p < 0:01). Likewise, the response rates for the earlier components of M-TEMPs obtained from 105, 95, 85 and 75 dB acoustic stimulation were 100%, 100%, 38% and 27%, respectively, revealing significant differences among groups of 95, 85 and 75 dB (Table 1, CochranÕs Q test, p < 0:01). Meanwhile, the later components of MTEMPs also demonstrated significant decrease in the response rate when the stimulus intensity was attenuated (Table 1, CochranÕs Q test, p < 0:01).
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Comparison of the response rates for the earlier components between B-TEMPs and M-TEMPs revealed no significant difference under similar stimulus intensity (p < 0:05, McNemar test, Table 1). In contrast, BTEMPs presented higher response rate for the later components than M-TEMPs at all stimulus intensities (p < 0:05, McNemar test, Table 1). The mean thresholds of the earlier components between B-TEMPs (Fig. 1) and M-TEMPs (Fig. 2) were 85 8 (mean SD) dB and 88 10 dB, respectively, showing no significant difference (p > 0:05, paired ttest). Meanwhile, there was also no statistical difference in mean thresholds for the later components between BTEMPs (83 9 dB) and M-TEMPs (85 10 dB) (p > 0:05, Student t-test). Likewise, the mean thresholds of the earlier versus later components did not differ significantly, regardless of B-TEMPs or M-TEMPs (p > 0:05, Student t-test, Table 1). 3.2. Comparison of the latencies The mean latencies of p13, n23, n34 and p44 for the B-TEMPs using 105 dB acoustic stimulation were 13.82 1.07 ms, 20.35 1.60 ms, 31.68 1.46 ms, and 37.42 1.68 ms, respectively. Compared to those for the M-TEMPs: 14.08 1.27 ms, 20.66 1.52 ms, 31.86 2.16 ms, and 38.18 2.03 ms, respectively, revealed no significant difference between these values. Likewise, there was no significant difference in the latencies of p13, n23, n34 and p44 between the B-TEMPs and M-TEMPs, respectively, when using 95, 85, or 75 dB tone burst stimulation (paired or Student t-test, p > 0:05) (Table 2). Furthermore, there was no significant relationship between the stimulus intensity and the mean latency, despite using binaural or monaural stimulation and recordings (p > 0:05, one-way analysis of variance test, Table 2).
Table 1 Comparison of response rates and thresholds of the earlier and later components of tone burst evoked myogenic potentials among different stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB 85 dB 75 dB
N (ears)
B-TEMP p13-n23
p13-n23
26 26 26 26
26 (100%) 26 (100%)* 14 (54%)* 6 (23%)*
26 (100%) 26 (100%)# 10 (38%)# 7 (27%)#
p > 0:05 (McNemar test) p > 0:05 (McNemar test)
85 8 dB
88 10 dB
p > 0:05 (paired t-test)
n34-p44
n34-p44
22 22 16 11
11 (42%) 11 (42%)## 3 (12%)## 2 (8%)##
< 0:05 < 0:05 < 0:05 < 0:05
85 10 dB
p > 0:05 (Student t-test)
Thresholds (mean SD)
105 dB 95 dB 85 dB 75 dB Thresholds (mean SD)
26 26 26 26
(85%) (85%)** (62%)** (42%)**
83 9 dB
*,**,#,##: p < 0:01, among three groups, CochranÕs Q test.
M-TEMP
p-Value
(McNemar (McNemar (McNemar (McNemar
test) test) test) test)
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Fig. 1. Myogenic potentials evoked by simultaneous binaural acoustic stimulation using tone burst with different stimulus intensities in a 22-year-old man. It reveals the thresholds as 75 dB for both p13-n23 and n34-p44 components, bilaterally. (I, p13; II, n23; III, n34; IV, p44; 105B: 105 dB, binaural stimulation; A, right side recording; B, left side recording.)
Fig. 2. Myogenic potentials evoked by monaural acoustic stimulation using tone burst with different stimulus intensities in a 24-year-old man. It reveals the thresholds as 70 dB for both p13-n23 and n34-p44 components of the right side, and 75 dB for both components of the left side. (I, p13; II, n23; III, n34; IV, p44; 105, 105 dB, R, right ear stimulation; A, right side recording; L, left ear stimulation; B, left side recording.)
3.3. Comparison of the amplitudes Because the amplitude of the VEMP varies substantially between subjects, the relative amplitude (amplitude of B-TEMP divided by that of M-TEMP) was used for comparison. The median relative amplitudes for the earlier components were 0.95 (0.69–1.18) [median (minimum–maximum)], 0.87 (0.52–1.27), 0.87 (0.63– 0.96), and 0.85 (0.73–0.97), when using 105, 95, 85, and 75 dB acoustic stimulation, respectively. It revealed
significant decrease in the p13-n23 amplitude of BTEMPs at all stimulus intensities, when compared with the respective group of M-TEMPs (p < 0:05, Wilcoxon signed-ranks test, Table 3). In contrast, the median relative amplitudes of the later components (n34-p44) obtained from 105, 95, 85, and 75 dB stimulation, were 1.29 (0.91–1.97) [median (minimum–maximum)], 1.18 (0.70–2.30), 1.73 (1.59– 2.86), and 1.25 (1.12–1.40), respectively. It showed significant larger n34-p44 amplitude of B-TEMPs than
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Table 2 Comparison of latencies of the earlier and later components of tone burst evoked myogenic potentials among different stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB 85 dB 75 dB
N (ears)
B-TEMP Latency p13 (ms)
Latency n23 (ms)
26 26 14 6
13.82 1.07 13.53 1.60 13.06 0.96 12.62 1.07
20.35 1.60 20.30 1.60 19.68 1.00 19.52 1.80
(p > 0:05)
(p > 0:05)
(p > 0:05)
(p > 0:05)
Latency n34 (ms)
Latency p44 (ms)
Latency n34 (ms)
Latency p44 (ms)
31.68 1.46 31.33 2.26 30.72 0.83 31.30 0.64
37.42 1.68 36.62 2.07 37.32 1.08 37.30 1.23
31.86 2.16 31.30 1.28 31.50 1.32 31.38 1.59
38.18 2.03 37.36 1.47 38.17 0.73 37.88 1.06
(p > 0:05)
(p > 0:05)
p-Value
105 dB 95 dB 85 dB 75 dB
22 22 16 11
p-Value
N (ears)
26 26 10 7
11 11 3 2
M-TEMP Latency p13 (ms)
Latency n23 (ms)
14.08 1.27 13.24 1.09 13.95 1.87 13.18 0.70
20.66 1.52 20.11 1.48 20.34 2.16 19.34 1.15
(NS) (NS) (NS) (NS)
(NS) (NS) (NS) (NS)
(p > 0:05)
(NS) (NS) (NS) (NS)
(NS) (NS) (NS) (NS)
(p > 0:05)
Data are expressed as mean SD. p-Value, relationship between the stimulus intensity and the latency (one-way analysis of variance test). NS, not statistically significant (p > 0:05, paired or Student t-test, B-TEMP group compared with the respective M-TEMP group).
Table 3 Comparison of amplitudes of the earlier and later components of tone burst evoked myogenic potentials among different stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB 85 dB 75 dB
N (ears)
B-TEMP p13-n23 (lV)
N (ears)
M-TEMP p13-n23 (lV)
N (ears)
B-TEMP/M-TEMP Relative amplitude
p-Value
26 26 14 6
116.5 112.6 108.0 102.4
26 26 10 7
142.6 137.6 129.1 119.0
26 26 10 6
0.95 0.87 0.87 0.85
0.013 0.039 0.005 0.028
(58.3–229.2) (61.9–232.7) (51.8–174.9) (84.0–125.7)
n34-p44 (lV) 105 dB 95 dB 85 dB 75 dB
22 22 16 11
145.2 (121.3–177.9) 112.1 (84.8–206.9) 100.0 (73.4–169.8) 99.7 (76.0–181.0)
(81.5–239.0) (86.3–212.6) (82.0–191.4) (93.5–172.5)
n34-p44 (lV) 11 11 3 2
114.5 (61.5–187.8) 99.4 (77.0–149.5) 91.7 (52.7–106.6) 83.7 (81.3–86.2)
(0.69–1.18) (0.52–1.27) (0.63–0.96) (0.73–0.97)
Relative amplitude 11 11 3 2
1.29 1.18 1.73 1.25
(0.91–1.97) (0.70–2.30) (1.59–2.86) (1.12–1.40)
0.046 0.026 0.109 0.180
Data are expressed as median (minimum–maximum). The relative amplitudes between B-TEMP and M-TEMP are compared with Wilcoxon signed-ranks test.
M-TEMPs, when elicited by either 105 or 95 dB acoustic stimulation (p < 0:05, Wilcoxon signed-ranks test, Table 3). However, the relative amplitudes of later components did not reach statistical significance when using 85 or 75 dB tone burst stimulation (p > 0:05, Wilcoxon signed-ranks test, Table 3), possibly due to small sample size (3 ears). Because the amplitude of the VEMP varies substantially in one subject between trials, moreover, less responses obtained from 85 or 75 dB acoustic stimulation, hence only relative amplitudes between 105 and 95 dB groups were compared. The median relative amplitudes (amplitude of 105 dB group divided by that 95 dB group) of the earlier components for B-TEMPs were 1.10 (0.40–2.29) [median (minimum–maximum)], indicating a significant increase in the p13-n23 amplitude of 105 dB group (p < 0:05, Wilcoxon signed-ranks test,
Table 4). Whereas those for the later components of BTEMPs were 1.12 (0.52–1.96) [median (minimum–maximum)], showing non-significant difference (p > 0:05, Wilcoxon signed-ranks test, Table 4). In contrast, the relative amplitudes of both earlier and later components for M-TEMPs between 105 and 95 dB groups demonstrated a significant increase in amplitudes of both components of the 105 dB group (p < 0:05, Wilcoxon signed-ranks test, Table 4). Fig. 3 illustrates the difference between B-TEMPs and M-TEMPs in a 24-year-old healthy subject. Myogenic potentials elicited by monaural 95 dB tone burst stimulation with ipsilateral recording demonstrate earlier components, but without later components. However, both the earlier and later components of myogenic potentials can be obtained when using binaural 95 dB tone burst stimulation with bilateral recording.
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Table 4 Comparison of amplitudes of the earlier and later components of tone burst evoked myogenic potentials between105 and 95 dB stimulus intensities, in conditions of binaural stimulation with bilateral recording (B-TEMP) and monaural stimulation with ipsilateral recording (M-TEMP)
105 dB 95 dB
N (ears)
B-TEMP p13-n23 (lV)
N (ears)
M-TEMP p13-n23 (lV)
26 26
116.5 (58.3–229.2) 112.6 (61.9–232.7)
26 26
142.6 (81.5–239.0) 137.6 (86.3–212.6)
Relative amplitude (105 dB/95 dB) p-Value
1.10 (0.40–2.29) 0.020
1.13(0.61–1.93) 0.020 n34-p44 (lV)
105 dB 95 dB Relative amplitude (105 dB/95 dB) p-Value
22 22
145.2 (121.3–177.9) 112.1 (84.8–206.9) 1.12 (0.52–1.96) 0.170
n34-p44 (lV) 11 11
114.5 (61.5–187.8) 99.4 (77.0–149.5) 1.31 (0.99–2.05) 0.028
Data are expressed as median (minimum–maximum). The relative amplitudes between 105 dB group and 95 dB group are compared with Wilcoxon signed-ranks test.
Fig. 3. Myogenic potentials elicited by monaural 95 dB acoustic stimulation (the upper two tracings) showing earlier components (p13, n23) only. Whereas myogenic potentials evoked by binaural 95 dB acoustic stimulation (the lower two tracings) demonstrate both earlier and later (n34, p44) components. (I, p13; II, n23; III, n34; IV, p44; 95R(A): 95 dB, right ear stimulation, right side recording; 95L(B): 95 dB, left ear stimulation, left side recording; 95B(A): 95 dB, binaural stimulation, right side recording; 95B(B): 95 dB, binaural stimulation, left side recording.)
4. Discussion The ideal stimulation mode for tone evoking the earlier components of VEMP is suggested as follows: intensity 95 dB; frequency 500 Hz; stimulation repetition rate 5 Hz; rise/fall time 1 ms; and plateau time 2 ms; recorded unilaterally (Murofushi et al., 1999; Cheng and Murofushi, 2001a,b). The waveform morphology of the VEMP responses observed with this stimulation mode is simultaneously the most constant and remarkable. However, this stimulation mode elicits only 45–60% response rate for the later components (Wu and Young, 2002). Since the earlier components of VEMPs are present with high intensity sound, tone bursts with different stimulus intensities are used to stimulate the ears binaurally or monaurally, in order to investigate the characteristics of the earlier and later components in subjects with normal sacculo-collic reflex.
The results showed 100%, 100%, 54%, and 23% response rates for the earlier components of B-TEMPs, when using 105, 95, 85, and 75 dB acoustic stimulation, respectively, indicating a significant decrease in the response rate when the stimulus intensity was attenuated from 95 to 75 dB (Table 1). In comparison with those for the earlier components of M-TEMPs, 100%, 100%, 38%, and 27% response rate, respectively, revealed no significant difference in these vlues between B-TEMPs and M-TEMPs (Table 1). However, the response rates for the later components of B-TEMPs obtained from 105, 95, 85, and 75 dB acoustic stimulation were 85%, 85%, 62%, and 42%, respectively. Compared to 42%, 42%, 12% and 8% for those of M-TEMPs, respectively, demonstrated significant higher response rates in the later components when using binaural acoustic stimulation (Table 1).
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Nevertheless, there is no statistical difference in the mean latencies of each peak (p13, n23, n34, and p44) between B-TEMPs and M-TEMPs at all stimulus intensities. Meanwhile, there is also no significant relationship between the stimulus intensity and the latency, despite using binaural or monaural stimulation and recordings (Table 2). In comparison with the relative amplitudes of the earlier components between B-TEMPs and M-TEMPs reveals significant reduction in the p13-n23 amplitude in the former (Table 3), compatible with our recent report (Wang and Young, 2003). This is possibly because that the amplitude of ipsilateral B-TEMPs could be contaminated by ÔcrossoverÔ inverted VEMPs (Sato et al., 1997), leading to reduction of the p13-n23 amplitude of B-TEMPs, after subtraction from the contralateral TEMPs. However, the later components in B-TEMPs demonstrate significant larger n34-p44 amplitude than M-TEMPs (Table 3), further supports that the later components originated from bilateral acoustic stimulation (Colebatch et al., 1994). In comparison with the relative amplitudes of the earlier components between 105 and 95 dB groups reveals significant increase in relation to the elevation of the stimulus intensity, regardless of B-TEMPs or MTEMPs (Table 4). Similar condition is also demonstrated in the later components of M-TEMPs. However, the relative amplitudes of the later components of BTEMPs between 105 and 95 dB groups do not differ significantly, possibly because the later components elicited from 105 dB stimulation binaurally have saturated via additive effects from binaural acoustic stimulation (Table 4). Since the amplitudes of the earlier components are larger with monaural acoustic stimulation, whereas amplitudes of the later components are larger with binaural acoustic stimulation, will the thresholds for eliciting both components be different between BTEMPs and M-TEMPs? From Table 1, the mean thresholds for the earlier components elicited by binaural or monaural stimulation were 85 8 and 88 10 dB, respectively, showing non-significant difference. Likewise, there is no significant difference in the mean thresholds of the later components between B-TEMPs and M-TEMPs. Furthermore, the mean thresholds of the earlier versus later components did not differ significantly, regardless of B-TEMPs or M-TEMPs. Compared to the guinea pigs, the threshold for evoking responses of saccular afferent is 60–70 dB above the auditory brainstem response threshold (Murofushi et al., 1995), consistent with our results. Thus, although the earlier components originate ipsilaterally and the later components bilaterally, thresholds for both components do not differ significantly, implying that both components may, at least in part, share a common origin.
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One may ask why the later components demonstrate a 30 ms increased latency? One of the answers is attributable to more synapses leading to longer distance of the nerve pathways. However, some other unknown factors remain to be clarified. Further more clinical patients and experimental animals undergoing VEMP test, using binaural acoustic stimulation with bilateral recording, may help to elucidate the mechanism of the later components.
5. Conclusion Monaural acoustic stimulation with ipsilateral recording may elicit larger amplitude of the earlier components of TEMPs, whereas binaural acoustic stimulation with bilateral recording evokes higher response rate and larger amplitude of the later components. This finding further supports that the earlier components originate from ipsilateral acoustic stimulation, whereas the later components are elicited from bilateral acoustic stimulation. Although the nerve pathways for both components are different, their thresholds do not differ significantly, indicating that both components may, at least in part, share a common origin, but different pathways.
Acknowledgements This work was supported by a research grant (Grant no. NSC 92-2314-B002-349) from National Science Council, Taipei, Taiwan.
References Bickford, R.G., Jacobson, J.L., Cody, D.T.R., 1964. Nature of averaged evoked potentials to sound and other stimuli in man. Ann. NY Acad. Sci. 112, 204–223. Cheng, P.W., Murofushi, T., 2001a. The effect of rise/fall time on vestibular-evoked myogenic potential triggered by short tone bursts. Acta Otolaryngol. 121, 696–699. Cheng, P.W., Murofushi, T., 2001b. The effect of plateau time on vestibular-evoked myogenic potential triggered by tone bursts. Acta Otolaryngol. 121, 935–938. Colebatch, J.G., Halmagyi, G.M., 1992. Vestibular evoked potentials in human neck muscles before and after unilateral vestibular deafferentation. Neurology 42, 1635–1636. Colebatch, J.G., Halmagyi, G.M., Skuse, N.F., 1994. Myogenic potentials generated by a click-evoked vestibulocollic reflex. J. Neurol. Neurosurg. Psychiatr. 57, 190–197. Didier, A., Cazals, Y., 1989. Acoustic responses recorded from the saccule bundle on the eighth nerve of the guinea pigs. Hear. Res. 37, 123–128. Kushiro, K., Zakir, M., Ogawa, Y., et al., 1999. Saccular and utricular inputs to sternocleidomastoid motorneurons of decerebrate cat. Exp. Brain Res. 126, 410–416. Lim, C.L., Clouston, P., Sheean, G., Yiannikas, C., 1995. The influence of voluntary EMG activity and click intensity on the
66
C.-T. Wang, Y.-H. Young / Hearing Research 191 (2004) 59–66
vestibular click evoked myogenic potential. Muscle Nerve 18, 1210–1213. Murofushi, T., Curthoys, I.S., Gilchrist, D.P., 1996. Response of guinea pig vestibular nucleus neurons to clicks. Exp. Brain Res. 111, 149–152. Murofushi, T., Curthoys, I.S., Topple, A.N., Colebatch, J.G., Halmagyi, G.M., 1995. Responses of guinea pig primary vestibular neurons to clicks. Exp. Brain Res. 103, 174–178. Murofushi, T., Matsuzaki, M., Wu, C.H., 1999. Short tone burstevoked myogenic potentials on sternocleidomastoid muscle. Are these potentials also of vestibular origin? Arch. Otolaryngol. Head Neck Surg. 125, 660–664. Murofushi, T., Shimizu, K., Takegoshi, H., Cheng, P.W., 2001. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potential. Arch. Otolaryngol. Head Neck Surg. 127, 1069–1072. Sato, H., Imagawa, M., Isu, M., Uchino, Y., 1997. Properties of saccular nerve-activated vestibulo-spinal neurons in cats. Exp. Brain Res. 116, 381–388.
Uchino, Y., Sato, H., Sasaki, M., et al., 1997. Sacculocollic reflex arcs in cats. J. Neurophysiol. 77, 3003–3012. Takegoshi, H., Murofushi, T., 2003. Effect of white noise on vestibular evked myogenic potentials. Hear. Res. 176, 59–64. Wang, S.J., Young, Y-H., 2003. Vestibular evoked myogenic potentials using simultaneous binaural acoustic stimulation. Hear. Res. 185, 43–48. Wu, C.H., Young, Y-H., Murofushi, T., 1999. Tone burst-evoked myogenic potentials in human neck flexor and extensor. Acta Otolaryngol. Stockholm 119, 741–744. Wu, C.C., Young, Y-H., 2002. Vestibular evoked myogenic potentials are intact after sudden deafness. Ear Hearing 23, 235– 238. Wu, C.C., Young, Y-H., Ko, J.Y., 2003. Effect of irradiation on vestibular evoked myogenic potentials on nasopharyngeal carcinoma survivors. Head Neck 25, 482–487. Young, Y-H., Huang, T.W., Cheng, P.W., 2003. Assessing the stage of MeniereÕs disease using vestibular evoked myogenic potentials. Arch. Otolaryngol. Head Neck Surg. 129, 815–818.