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The Journal of Physiology logoLink to The Journal of Physiology
. 2007 Jan 18;580(Pt 1):195–209. doi: 10.1113/jphysiol.2006.123240

Origin of sound-evoked EMG responses in human masseter muscles

Franca Deriu 1, Enzo Ortu 1,3, Saverio Capobianco 2, Elena Giaconi 1, Francesco Melis 1, Elena Aiello 3, John C Rothwell 4, Eusebio Tolu 1
PMCID: PMC2075422  PMID: 17234698

Abstract

Sound is a natural stimulus for both cochlear and saccular receptors. At high intensities it evokes in active masseter muscles of healthy subjects two overlapping reflexes: p11/n15 and p16/n21 waves, whose origin has not yet been demonstrated. Our purpose was to test which receptor in the inner ear is responsible for these reflexes. We compared masseter EMG responses induced in normal subjects (n = 9) by loud clicks (70–100 dB normal hearing level (NHL), 0.1 ms, 3 Hz) to those evoked in subjects with a selective lesion of the cochlea (n = 5), of the vestibule (n = 1) or with mixed cochlear-vestibular failure (n = 5). In controls, 100 dB clicks induced bilaterally, in the unrectified mean EMG (unrEMG), a clear p11 wave followed by a less clear n15 wave and a subsequent n21 wave. Lowering the intensity to 70 dB clicks abolished the p11/n15 wave, while a p16 wave appeared. Rectified mean EMG (rectEMG) showed, at all intensities, an inhibitory deflection corresponding to the p16/n21 wave in the unrEMG. Compared to controls, all deaf subjects had a normal p11 wave, together with more prominent n15 wave; however, the p16/n21 waves, and their corresponding inhibition in the rectEMG, were absent. The vestibular patient had bilaterally clear p11 waves only when 100 dB clicks were delivered bilaterally or to the unaffected ear. Stimulation of the affected ear induced only p16/n21 waves. Data from mixed patients were consistent with those of deaf and vestibular patients. We conclude that click-induced masseter p11/n15 waves are vestibular dependent, while p16/n21 waves depend on cochlear integrity.

It was recently shown that unilateral or bilateral electric vestibular stimulation (EVS) could evoke a short-latency, short-duration bilateral EMG response in active masseter muscles of healthy subjects (Deriu et al. 2003). This response consists of a symmetric biphasic potential which has opposite polarity depending on the polarity of electric stimulation. The cathodal response is a positive–negative p11/n15 wave which is larger and more consistent than the anodal (n11/p15) response. Single motor unit (SMU) studies demonstrated that the p11/n15 wave in the surface EMG, corresponds to a short-latency, brief and abrupt interruption of ongoing masseter SMU firing. Based on results of control experiments, on the physiological properties of the response and on its similarity with the EVS-induced vestibulocollic reflex (Watson and Colebatch, 1998; Colebatch & Rothwell, 2004), it was concluded that the EVS-induced masseter response is of vestibular origin and, hence, it was termed a vestibulomasseteric reflex (VMR) (Deriu et al. 2003).

EVS-induced responses in masseter muscles are not the only example of a vestibular influence on the trigeminal motor system. Previous studies performed on anaesthetized animals (Tolu & Pugliatti, 1993; Tolu et al. 1996) and in humans (Hickenbottom et al. 1985; Deriu et al. 2000) have shown that vestibular stimulation exerts a bilateral, asymmetric, long-lasting, excitatory control on trigeminal motoneurones via polysynaptic pathways. These vestibular-induced masseter responses have physiological features very different from those of the VMR, with the latter being bilaterally symmetrical, short duration, inhibitory and mediated by no more than three synapses (Deriu et al. 2003, 2005). These two sets of results were considered compatible with the operation of two parallel pathways between the vestibule and masseter (Deriu et al. 2003, 2005), analogous to the situation widely described in limb muscles (Britton et al. 1993; Fitzpatrick et al. 1994; Watson & Colebatch, 1997), i.e. a short-latency, short-duration response followed by a longer-lasting response of opposite polarity. In the masseter, it has been suggested that the former response is activated by phasic inhibitory inputs, which may be of minor importance in postural control, but which may be more important in fine-tuning of voluntary motor output by allowing vestibular inputs a rapid access to jaw muscle control. The later sustained and more powerful response, induced by the tonic activation of indirect excitatory pathways, has been proposed to be of importance in postural control of the masseters by stabilizing the jaw during head movements in space.

In addition to EVS, which activates the vestibular system by acting at the level of the most distal part of the vestibular nerve (Goldberg et al. 1984; Courjon et al. 1987), high-intensity acoustic stimulation is well known to activate, in addition to cochlear receptors, saccular hair cells (Cazals et al. 1983; McCue & Guinan, 1994; Halmagyi & Colebatch, 1995; Murofushi et al. 1995), which project monosynaptically to neurones in the ispilateral lateral vestibular nucleus (Murofushi et al. 1996a; Murofushi & Curthoys, 1997).

Loud clicks have also been demonstrated to evoke, in the ipsilateral active sternocleidomastoid muscle, a short-latency p13/n23 response (Colebatch et al. 1994), which depends on the integrity of vestibular afferents (Colebatch & Halmagyi, 1992; Colebatch et al. 1994). Since then, the so-called ‘vestibular evoked myogenic potential’ (VEMP) has been used to explore saccular function (Murofushi et al. 1996b; Colebatch et al. 1998; Matsuzaki et al. 1999; Clarke, 2001; Colebatch, 2002; Patko et al. 2003; Welgampola & Colebatch, 2005) and, more recently, vestibulo-spinal conduction in man (Itoh et al. 2001; Murofushi et al. 2001; Sartucci & Logi, 2002; Versino et al. 2002; Welgampola & Colebatch, 2005).

Following on from these observations, we (Deriu et al. 2005) investigated in healthy subjects whether sound-induced saccular activation could induce vestibular reflex responses in the masseter muscles, in addition to the previously described response evoked by EVS. Masseter responses to loud acoustic stimulation had already been described in previous work, as a bilateral, long-latency, long-lasting silent period in active masseter EMG. However, this response was attributed to activation of cochlear rather than vestibular afferents (Kiang, 1963; Meier-Ewert et al. 1974), and so it was called the ‘jaw acoustic reflex’ (Meier-Ewert et al. 1974). Deriu et al. (2005) found that masseter responses to loud clicks consisted of two bilateral and symmetrical short-latency waves, which partially overlap in the urnectified averaged EMG: a high-threshold, early p11/n15 wave, and a lower-threshold, later p16/n21 wave. The authors hypothesized that the p11/n15 and the p16/n21 responses originate from saccular and cochlear activation, respectively (Deriu et al. 2005). This hypothesis was based on the following criteria: (i) different physiological properties (threshold, latency, duration, appearance in the rectified mean EMG) of the two responses; (ii) similarity of the p11/n15 response to the EVS-induced VMR (Deriu et al. 2003) and to the click-induced VEMPs (Colebatch et al. 1994); (iii) similarity of the p16/n21 response to the jaw acoustic reflex (Meier-Ewert et al. 1974). However, a direct test of the hypothesis, by examining responses in subjects with selective lesion of click-activated vestibular and cochlear receptors was lacking.

The present study fills this gap in our knowledge by investigating click-induced short-latency masseter EMG responses in patients affected by vestibular failure and/or sensorineural deafness, in order to confirm the vestibular origin of the p11/n15 wave and the cochlear origin of the p16/n21 wave.

Methods

Subjects

Twenty subjects were studied, some more than once, after they had given informed consent. Based on accurate medical history and neuro-otological assessment, subjects were divided into four groups: (1) normal subjects (controls, n = 9: 2 males and 7 females, aged 21–42 years); (2) subjects with sensorineural deafness but normal vestibular function bilaterally (deaf, n = 5: 3 males and 2 females, aged 22–58 years); (3) subjects with unilateral vestibular failure but intact auditory function bilaterally (vestibular, n = 1, male, 57 years old); (4) subjects with auditory and vestibular deficits (mixed, n = 5: 2 males and 3 females, aged 32–59 years).

Experiments were carried out in a silent room with the subjects seated on a comfortable chair, with the head straight, the trunk upright, and the lower limbs in a semiflexed position. The protocol, approved by the local ethics committee, was in accordance with the ethical standards established in the Helsinki II Declaration.

Neuro-otological tests

All subjects underwent three neuro-otological tests prior to testing click-induced masseter muscle responses.

Auditory function was explored with tonal audiometry (Amplifon audiometer 300 E 815) performed following international standard procedures ISO 6189-1983.

Vestibular ampullar function was evaluated with caloric testing. This was performed with the subject reclining, and the head inclined 30 deg from horizontal so as to make the lateral canal horizontal. Electronystagmogram (ENG) was recorded after stimulation with 50 ml water at 30° and 44°C (i.e. 7°C below or above assumed body temperature), injected into each external auditory canal for 30 s. The time interval between two consecutive stimulations was 5 min. During the culmination phase, from 30 to 50 s after stimulation, both the nystagmus frequency and slow component velocity (SCV) were evaluated in a time window of 10 s. It is considered that normal mean ± s.d. values for frequency lie within the range 1.8 ± 0.5 jerk s−1 and for SCV in the range 16 ± 8 deg.

Vestibular saccular function was assessed by recording click-induced VEMPs (p13/n23 wave) from symmetrical sites over the upper half of the belly of each sternocleidomastoid muscle. An active electrode was placed 8–12 cm up the belly of the sternocleidomastoid muscle from its sternal insertion, a reference electrode over the sternocostal junction and ground electrode over the upper sternum (Colebatch et al. 1994; Colebatch & Rothwell, 2004). During data collection, the subject voluntarily activated their sternocleidomastoid muscles by pushing their forehead against resistance offered by the hands of one of the experimenters, who stood behind him/her.

Masseter muscle EMG recording

Surface EMG responses elicited by click stimulation in active masseter muscles were recorded bilaterally, using standard techniques. Positive deflections are shown as downward deflections in the average unrectified EMG. Masseter muscle EMG recordings were always made with the reference electrode placed at the level of the lower border of the mandible, the active electrode about 2 cm above this, and the ground electrode over the forehead. This electrode location was previously found (Deriu et al. 2003, 2005) to be the site where the largest responses could be detected. The subjects were asked to activate the masseter muscles at a target level (30–50% of maximal voluntary contraction) and to maintain it steadily during data collection. To assist subjects, they were given visual feedback of filtered and rectified masseter EMG on an oscilloscope screen.

Both unrectified and rectified EMG activities were recorded simultaneously (OTE PHASIS EMG machine, ESAOTE Biomedica, Italy). The EMG was amplified, filtered (0.3–2000 Hz) and sampled (5 kHz) from 50 ms before to 100 ms after stimulus delivery, using a 1401 plus A/D converter (Cambridge Electronic Design, Cambridge, UK) and Signal 2.10 software on a PC.

Click stimulation

Click stimuli of 0.1 ms duration were generated by a click generator included in the OTE PHASIS EMG machine and delivered through TDH-49P earphones (Telephonics, Huntington, NY, USA) either to the right or left or to both ears at a frequency of 3 Hz. All click intensities are expressed with respect to the normal hearing threshold for such clicks (0 dB NHL (normal hearing level) equal to 45 dB SPL (sound pressure level)). Click intensities were always the same in each ear. Intensities routinely used were 100 dB NHL, suprathreshold intensity for both the masseter p11/n15 wave (Deriu et al. 2005) and VEMPs (Colebatch et al. 1994), and 70 dB NHL, subthreshold intensity for the masseter p11/n15 wave (Deriu et al. 2005) and VEMPs (Colebatch et al. 1994), but suprathreshold for the masseter p16/n21 wave (Deriu et al. 2005).

Data analysis

Masseter and sternocleidomastoid reflex responses induced by click stimulation were measured from the unrectified averages (n = 300–500). The rectified averages were also evaluated and used to quantify the level of muscle tonic activation. Response amplitudes in unrectified EMG were measured either for a single peak or peak to peak, with reference to the mean level of activity in the 50 ms preceding the clicks. These amplitude values were then divided by the mean of the rectified EMG for the 50 ms preceding the stimulus onset. This gives a value for response amplitude relative to the level of background muscle activation.

Values are given as means ± s.d. The latencies of p11 and p16 waves (right and left masseters) in normal subjects were compared using Student's t test (paired two sample for means) and the average p11 – p16 difference was calculated. The p11 waves (left and right masseter) elicited by 100 dB clicks in normal, deaf and mixed patients were compared using the one-way ANOVA test. The p16 waves of controls and mixed patients (right and left masseters) were compared using Student's t test for independent samples.

Results

Masseter responses to click stimulation in normal subjects

In all normal subjects (n = 9), unilateral and bilateral click stimulation at 100 dB NHL induced a clear bilateral p11 wave in the mean unrectified masseter EMG, that was followed by a less-defined n15 wave, and a later variable n21 wave. In most subjects the n15 wave was just an inflexion in the trace, or was not visible at all, so that the response consisted of a simple biphasic p11/n21 wave. Since the n15 wave was not present in all subjects, only the p11 wave was evaluated. It was symmetrical with an onset latency of 8.4 ± 0.7 ms and a peak latency of 11.9 ± 0.9 ms (mean ± s.d. calculated on 18 muscles, right and left masseters, of 9 subjects). The p11 responses to bilateral clicks were significantly (P < 0.01) larger than responses to unilateral clicks (ratio p11 amplitude/mean prestimulus EMG level was 0.94 ± 0.26 following bilateral clicks and 0.53 ± 0.2 following unilateral clicks).

Clicks of 70 dB were subthreshold for the p11 wave. At this stimulation intensity, a p16 wave, preceding the n21 wave, became evident in the unrectified mean EMG. The p16 wave was symmetrical with an onset latency of 12.0 ± 1.3 ms and a peak latency of 16.6 ± 1.1 ms (mean ± s.d. calculated on 18 muscles, right and left masseters, of 9 subjects). A statistical comparison of the p11 and p16 waves in controls demonstrated that these waves differed significantly (P < 0.0001) in onset and peak latency, with an average peak latency difference p11 – p16 wave of 4.7 ± 1.2 ms.

At all stimulation intensities, there was a reduction in the rectified mean EMG beginning 11–12 ms (11.6 ± 0.5 ms) after stimulus delivery and lasting 12–14 ms. This deflection, corresponding to the p16/n21 wave in the unrectified average, was occasionally preceded by a small upward deflection corresponding to the p11 response, which was not visible on most occasions in the rectified mean EMG.

Figure 1 shows masseter responses, in the unrectified averaged EMG, to bilateral click stimulation at 100 and 70 dB in the nine normal subjects who participated in this study.

Figure 1. Responses induced in masseter muscles of normal subjects by bilateral click stimulation at 100 and 70 dB NHL.

Figure 1

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Responses of active right and left masseters recorded in the unrectified averaged EMG are shown for all the normal subjects (n = 9) tested in this study. For each subject, responses to click stimuli of 100 dB are shown in black, while responses to click stimuli of 70 dB are shown in grey. The level of masseter activation performed by the subjects ranged from 30% to 50% of maximal voluntary contraction. In all traces, arrows indicate the time of stimulus application.

Figure 2A shows masseter responses in the unrectified and rectified mean EMG from a representative normal subject (subject A of Fig. 1) to click stimulation at 100 and 70 dB NHL, delivered during tonic muscle activation at 50% of maximal voluntary contraction. Figure 2B shows VEMPs recorded from the same subject illustrated in Fig. 2A.

Figure 2. Masseter and sternocleidomastoid muscle EMG responses to bilateral and unilateral click stimulation recorded from a representative normal subject.

Figure 2

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A, responses of right and left active masseter muscle to bilateral and unilateral click stimuli of 100 dB NHL and to bilateral clicks of 70 dB NHL (0.1 ms duration, 3 Hz). B, vestibular evoked myogenic potentials (VEMPs) induced in right and left active sternocleidomastoid muscle by bilateral and unilateral click stimuli of 100 dB NHL. For each set of recordings, unrectified and rectified EMG averages (each of 500 trials) are reported. All sets of averages were obtained with the same click duration (0.1 ms) and frequency (3 Hz). In all traces, arrows indicate the time of stimulus application. The mean level of prestimulus activity is shown on one side of each rectified mean EMG trace. Vertical calibrations refer to unrectified averages, while horizontal calibrations refer to all traces.

All subjects included in the control group showed normal responses to neuro-otological tests. With particular regard to assessment of their saccular function, the mean VEMP (namely, the p13/n23 wave) onset latency was 8.4 ± 0.7 ms, and mean peak latency was 13.2 ± 0.9 ms for the p13 wave and 20.8 ± 1.8 ms for the n23 wave. Like the masseter p11 response, the sternocleidomastoid p13/n23 response usually did not appear in the mean rectified EMG, although it sometimes corresponded to an upward deflection of the rectified trace. Click stimuli of 70 dB NHL were subthreshold also for VEMPs. At this intensity, only later potentials were visible in the unrectified EMG.

A comparison of threshold intensity for the p11 wave and VEMPs was not made in this study; however, previous data obtained in normal subjects (Deriu et al. 2005) suggested that it is the same in any one individual, and that the mean threshold for the p11 wave is 84 dB.

Masseter responses to click stimulation in subjects with sensorineural deafness but normal vestibular function

Five subjects affected by profound bilateral sensorineural deafness (four congenital and one acquired) were studied. All of them had bilaterally normal vestibular responses to ENG and VEMP recordings. Latencies (onset: 8.6 ± 0.8 ms; peak latency 11.7 ± 0.8 ms; mean ± s.d. calculated on 10 muscles, right and left masseters, of five subjects) and amplitudes of the masseter p11 wave elicited by bilateral and unilateral clicks at 100 dB also were not significantly different from those recorded in normal subjects. On the contrary, the n15 wave, which was usually not visible in controls, was always clearly evident and well defined in deaf people.

When the intensity of stimulation was lowered to an intensity subthreshold for the p11 wave, but suprathreshold for the p16 wave in normal subjects (70 dB NHL), none of the deaf subjects showed any signs of a p16 wave. This also held true, at all stimulation intensities used, for later potentials, like the n21 wave. In addition, no inhibitory deflection was seen in the rectified mean EMG at any stimulus intensity.

Figure 3 shows recordings from one representative subject affected by bilateral congenital sensorineural deafness but with normal vestibular function.

Figure 3. Recordings from one subject affected by bilateral congenital deafness but with normal vestibular function.

Figure 3

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A, responses induced in masseter unrectified EMG averages (each of 500 trials) by bilateral and unilateral click stimulation at 100 and 70 dB NHL. Note that the patient (MM, female, 23 years old) was unable to hear the 100 dB stimulus when it was presented bilaterally. In all traces arrows indicate the time of stimulus application. B, tonal audiograms showing a profound sensorineural hearing loss in both ears. There was no response (n-r) from the patient to bone conduction (> and <) at maximal output from the stimulator. C, vestibular evoked myogenic potentials (VEMPs) induced by bilateral and unilateral clicks at 100 dB, in the averaged unrectified EMG (n = 300) recorded from right and left active sternocleidomastoid muscle. VEMP recording clearly demonstrates a normal saccular function bilaterally in this patient. Arrows indicate the time of stimulus application. D, electronistagmogram (ENG) recorded following caloric stimulation demonstrated normal responses from both ears. Upward deflections indicate rightward eye movement, downward deflection indicates leftward eye movements.

Masseter responses to click stimulation in a subject with selective unilateral vestibular failure and normal hearing bilaterally

Figure 4 illustrates recordings obtained from a subject affected by acute left vestibular neuronitis. Figure 4A reports masseter muscle responses to 100 and 70 dB clicks. Symmetric p11/n21 waves were seen in the mean unrectified EMG only when 100 dB clicks were delivered to both ears or to the right unaffected ear. Unlike controls, amplitudes of responses to bilateral and unilateral clicks were not significantly different. By contrast, when 100 dB clicks were delivered to the left affected ear, no p11/n15 waves were seen; a symmetric p16/n21 wave, superimposable on that induced by 70 dB clicks, was instead detected bilaterally in the unrectified averaged EMG. Rectified averages (not shown in Fig. 4) showed bilaterally, at all stimulation intensities, an inhibitory deflection corresponding in latency and duration to the p16/n21 wave in the unrectified mean EMG.

Figure 4. Recordings from one subject with acute left vestibular failure but normal hearing bilaterally.

Figure 4

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A, masseter muscle responses to bilateral and unilateral click stimulation at 100 dB and to bilateral click stimulation at 70 dB, in a subject with left acute vestibular neuronitis (PC, male, 57 years old). B, tonal audiograms showed intact auditory function bilaterally. C, VEMP recordings demonstrated no saccular responses on the left side, but normal saccular responses on the right side. D, electronystagmogram (ENG) demonstrated a vestibular inexcitability on the left side and right vestibular responses within the normal range.

In this subject, audiometry revealed that auditory function was intact bilaterally (Fig. 4B); VEMP recording demonstrated a failure of the left sacculus (Fig. 4C), and caloric testing demonstrated a vestibular inexcitability on the left side but vestibular responses from the right ear within the norm (Fig. 4D).

Masseter responses to click stimulation in subjects with mixed disorder

Four out of the five subjects with mixed disorder had undergone complete section of the vestibulocochlear nerve of one side (three right side, one left side) following a surgical excision of an acoustic schwannoma, while contralateral inner ear functions were intact. In these subjects, stimulation of the affected ear did not induce any response in the masseter EMG. Click-induced bilateral responses in the masseter were evoked only by stimuli delivered bilaterally or to the unaffected ear. In the unrectified averaged EMG, they consisted bilaterally of symmetric p11/n21 waves following 100 dB clicks and of symmetric p16/n21 waves following 70 dB clicks. There was suppression of the rectified mean EMG at a latency corresponding to the p16/n21 wave, following 100 dB as well as 70 dB clicks. Latency values of the p11 waves observed in mixed patients were significantly (P < 0.0001) different from those of the p16 waves of the same group. In contrast, no significant differences were found between latencies of the p11 and p16 waves observed in mixed patients and in normal subjects. Unlike controls, the amplitudes of responses to bilateral and unilateral stimulation were the same amplitude in mixed patients. Figure 5 shows recordings from a representative subject with section of the left VIIIth nerve.

Figure 5. Recordings from a subject with complete section of the left VIIIth cranial nerve and both vestibular and cochlear functions preserved on the right side.

Figure 5

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In this subject (FT, male, 54 years old), click stimulation at 100 dB was effective in inducing symmetric p11/n15 waves only when given to both ears or to the right intact ear. Stimulation of the left affected ear was unable to induce either p11/n15 or p16/n21 waves. B, tonal audiometry demonstrated a left anacusia and right normal hearing. C, VEMP recordings demonstrated a left saccular failure but normal responses from the right ear. D, ENG recordings demonstrated a left vestibular areflexia with compensatory reduction of the slow component velocity (SCV) on the right side.

The fifth patient from the mixed group had bilateral congenital sensorineural deafness and a left vestibular failure, due to acute neuronitis. Recordings from this subject are shown in Fig. 6. Clear p11/n15 waves were evoked bilaterally in the masseter unrectified EMG (Fig. 6A) only if 100 dB clicks were given bilaterally or to the right ear, with intact vestibular function. The amplitude of responses to bilateral and unilateral stimulation were the same. The p11/n15 response was absent when 100 dB clicks were delivered to the left ear, with vestibular failure (see Figs 6C, D). As for the p16/n21 wave, this was absent after 100 dB clicks delivered to the ear with vestibular failure, or by bilateral clicks of 70 dB. Consistent with this last finding, no responses were seen in the rectified mean EMG (not shown in Fig. 6), following click stimulation at any intensity.

Figure 6. Recordings from a subject affected by bilateral congenital deafness and left acquired vestibular lesion.

Figure 6

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In this subject (AP, male, 34 years old), masseter muscle responses (A) to 100 dB clicks consisted of symmetric p11/n15 waves following bilateral or unilateral right stimulation. No masseter response (neither p11/n15 wave nor p16/n21 wave) was instead detectable following unilateral left stimulation at 100 dB or bilateral click stimulation at 70 dB. B, audiograms showed a profound sensorineural hearing loss bilaterally. C, VEMP recordings demonstrated the existence of a left saccular failure. D, ENG recordings showed a left vestibular hypoexcitability but vestibular responses from the right ear within the norm.

Discussion

Masseter muscle responses to loud click stimulation consist of two partially overlapping short-latency reflexes, a p11/n15 wave and a p16/n21 wave. Their different physiological features suggest that they originate from the activation of different inner ear receptors: saccular receptors for the p11/n15 response and cochlear receptors for the p16/n21 response (Deriu et al. 2005). However, loud clicks are not selective stimuli, as they activate both saccular and cochlear receptors (Cazals et al. 1983; McCue & Guinan, 1994; Halmagyi & Colebatch, 1995; Murofushi et al. 1995). We argue below that the present study of click-induced masseter responses, in conditions in which there is a selective lesion of one of the activated receptors, provides further evidence for our original hypothesis (Deriu et al. 2005) that the masseter p11/n15 wave has a vestibular origin (vestibulomasseteric reflex), whereas the p16/n21 wave has a cochlear origin (jaw acoustic reflex).

Characteristics of click-induced masseter responses in normal subjects and in subjects affected by sensorineural deafness and/or vestibular failure

Sound-induced p11/n15 and p16/n21 responses in masseter muscles of normal subjects have been described in a previous paper (Deriu et al. 2005). These responses do not appear as clearly separated in time as the sternocleidomastoid p13/n23 and n34/p44 potentials, so criteria to be used to discriminate them were also provided in that paper.

Table 1 reports, for both normal subjects and patients, onset and peak latency values of both the first ‘p’ wave elicited by click stimuli above the vestibular (VEMP) threshold (100 dB) and the first ‘p’ wave elicited by stimuli lower than the vestibular threshold (70 dB).

Table 1.

The table shows, for normal subjects and for patients, onset and peak latency values (ranges and mean ± s.d.) of the first ‘p’ wave observed in the unrectified averaged masseter EMG following click stimulation at intensities suprathreshold (100 dB) and subthreshold (70 dB) for the vestibular (VEMP) response

Subjects First ‘p’ wave elicited by 100 dB clicks First ‘p’ wave elicited by 70 dB clicks
Onset (ms) Peak latency (ms) Onset (ms) Peak latency (ms)
Controls (n = 9)
  Right masseter 6.5–9.1 (8.5 ± 0.9) 10.5–13.1 (12.0 ± 0.8)  9.8–12.9 (11.8 ± 1.1) 14.8–18.3 (16.5 ± 1.1)
  Left masseter 7.4–8.8 (8.3 ± 0.5) 10.4–13.2 (11.8 ± 0.9) 10.1–14.8 (12.1 ± 1.5) 14.6–18.5 (16.7 ± 1.3)
Bilateral deafness (n = 5)
  Bilateral clicks
  Right masseter 7.4–9.4 (8.7 ± 0.8) 10.7–13.1 (11.6 ± 0.9) — —
  Left masseter 7.2–9.4 (8.6 ± 0.9) 11.1–13.1 (11.7 ± 0.8) — —
Left vestibular lesion (n = 1)
  Left clicks
  Right masseter 11.2 15.2 11.2 15.2
  Left masseter 11.2 15.2 11.2 15.2
 Bilateral and right clicks
  Right masseter 8.5–9.2 (8.9 ± 0.5) 12.2–12.3 (12.3 ± 0.1) 11.4 15.1
  Left masseter 7.6–8.2 (7.9 ± 0.4) 12.3–12.4 (12.4 ± 0.1) 11.2 15.1
Mixed lesions (n = 5)
  Right VIIIth nerve surgical excision (n = 3)
  Right clicks
  Right masseter — — — —
  Left masseter — — — —
  Bilateral and left clicks
  Right masseter 8.0–8.5 (8.3 ± 0.2) 10.8–13.0 (12.0 ± 0.9) 11.0–13.4 (12.1 ± 0.1) 15.5–17.5 (16.7 ± 0.9)
  Left masseter 7.9–8.7 (8.4 ± 0.3) 10.7–12.9 (11.7 ± 0.8) 10.9–12.3 (11.7 ± 0.6) 15.1–18.1 (16.8 ± 1.2)
  Left VIIIth nerve surgical excision (n = 1)
  Left clicks
  Right masseter — — — —
  Left masseter — — — —
 Bilateral and right clicks
  Right masseter 8.3–8.4 (8.4 ± 0.1) 11.6–11.8 (11.7 ± 0.1) 11.3–13.8 (13.4 ± 0.6) 16.5–16.8 (16.7 ± 0.2)
  Left masseter 7.9–8.4 (8.2 ± 0.4) 11.8–12.1 (12.0 ± 0.2) 12.5–13.2 (12.9 ± 0.5) 17.0–17.3 (17.2 ± 0.2)
Bilateral deafness and left vestibular lesion (n = 1)
 Left clicks
  Right masseter — — — —
  Left masseter — — — —
  Bilateral and right clicks
  Right masseter 8.5–8.9 (8.7 ± 0.3) 12.4–12.6 (12.5 ± 0.1) — —
  Left masseter 8.4–8.8 (8.6 ± 0.3) 11.8–12.5 (12.5 ± 0.5) — —
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In the present study, the findings obtained from normal subjects confirmed those previously described. Thus bilateral or unilateral click stimuli above the vestibular (VEMP) threshold evoked bilateral responses in the unrectified averaged masseter EMG, beginning with a symmetric p11 peak and a barely visible n15 peak which, on most occasions, merged into a later n21 wave. The lack of a clear n15 component, in contrast to the consistency of the n15 wave evoked by EVS (Deriu et al. 2003), was suggested to be due to its overlap with a concomitant p16 wave evoked by stimulation of the cochlea (Deriu et al. 2005). When the stimulus intensity was lowered below the VEMP threshold, the p11 peak in the unrectified mean EMG was replaced by a p16 peak. The p11 and p16 waves elicited in normal subjects by VEMP suprathreshold and subthreshold intensities (100 and 70 dB, respectively) differ significantly as for onset and peak latency values. Thus we can discriminate the p11 from the p16 wave on the basis of threshold intensity as well as latency. These responses also differ in their appearance in the rectified mean EMG: the p11/n15 response does not appear in the rectified mean EMG, although it is sometimes visible as a small upward deflection corresponding to the p11 wave in the unrectified EMG; the p16 response appears in the rectified mean EMG as an inhibitory deflection which is detectable at all stimulation intensities.

Cochlear deaf patients have clear p11 and n15 peaks but no p16 responses below vestibular threshold and no sign of inhibition in the rectified EMG. Their p11 waves do not differ from those of normal subjects, while in contrast to normal subjects, the n15 wave was always clearly visible when the stimulation was delivered to the deaf ear. We speculate that absence of the p16 wave in deaf people allows the n15 wave to be observed much more clearly than in normal subjects. This hypothesis is supported by the fact that EVS, which is believed to activate vestibular rather than cochlear afferents (Lobel et al. 1998; Watson et al. 1998; Watson & Colebatch, 1998) induces in normal subjects, clear p11/n15 peaks (Deriu et al. 2003). We conclude that the p16/n21 wave depends on cochlear integrity. In contrast, the p11/n15 response is uninfluenced by loss of cochlear function, provided that vestibular function is intact.

The unique patient with selective unilateral vestibular lesion, but intact auditory function bilaterally, only showed the late p16/n21 wave rather than the earlier p11 wave upon stimulation of the affected ear at 100 dB. In contrast, 100 dB click stimulation evoked symmetric bilateral p11 responses, which were the same amplitude whether the clicks were delivered bilaterally or to the contralateral intact ear. This contrasts with the situation in controls where the p11 waves are larger following bilateral than unilateral stimulation, because inputs from both sides contribute to its origin. These findings confirmed that the p11 wave depends on the integrity of vestibular receptors and is independent of cochlear receptors.

Mixed patients showed responses consistent with those obtained from selective deaf or vestibular patients. In particular, neither waveform was observed when clicks were delivered to the ear with both vestibular and cochlear lesion.

Anatomical pathways of the vestibulomasseteric reflex

The vestibulomasseteric reflex shares many physiological features with the VEMP except that the VMR is bilateral whereas the VEMP is ipsilateral. However, although the neural pathway from vestibular receptors to the sternocleidomastoid muscle is well characterized, we have less information on the anatomy of the VMR. The pathway for the VEMP starts with the projection of primary vestibular afferents to the vestibular nuclear complex (lateral and spinal vestibular nuclei) and hence, via the medial vestibulospinal tract to sternocleidomastoid motoneurones in the ipsilateral accessory nucleus (Uchino et al. 1997a; Kushiro et al. 1999). This knowledge has recently induced many authors to use VEMPs not only as a test of otolith function (Murofushi et al. 1996b; Colebatch et al. 1998; Matsuzaki et al. 1999; Patko et al. 2003), but also as a test of vestibulo-spinal conduction (Itoh et al. 2001; Murofushi et al. 2001; Sartucci & Logi, 2002; Versino et al. 2002; Welgampola & Colebatch, 2005).

The neural pathway mediating the VMR may be more complex. It has been suggested, on the basis of physiological data obtained in both animals (Tolu & Pugliatti, 1993; Tolu et al. 1996) and humans (Deriu et al. 2000, 2003, 2005), to be organized as a pair of opposing pathways: a bilateral, asymmetric, excitatory tonic control, exerted through polysynaptic pathways, and a bilateral, symmetric, inhibitory phasic control exerted through oligosynaptic pathways. In a recent anatomical study, using transynaptic retrograde tracing with pseudorabies virus-Bartha injection into the masseter muscle of rats (Giaconi et al. 2006), we provided the first direct evidence that neurons in the vestibular nuclei (VN) and in the prepositus hypoglossi nucleus (PH) project bilaterally, mainly through multisynaptic pathways, to populations of motoneurones innervating the lower third of the superficial layer of the masseter muscle. In particular, the medial vestibular nucleus, the PH and the spinal vestibular nucleus have been suggested to play a predominant role in producing vestibulo-trigeminal responses. The pontomedullary reticular formation, the reticular zone (intertrigeminal nucleus, supratrigeminal nucleus and peritrigeminal zone) surrounding the trigeminal motor nucleus (Mo5) and the premotor zone included in the trigeminal sensory complex (spinal trigeminal nucleus and principal trigeminal nucleus) are potential relays from the complex VN/PH to Mo5. More recently, using a combination of anterograde and retrograde monosynaptic tracers, we found anterogradely labelled vestibular terminals making contact with retrogradely labelled motoneurones in the ipsilateral and contralateral Mo5. These results (Cuccurazzu et al. 2007) indicate the existence of a direct and crossed monosynaptic pathway that links the dorsomedial part of the parvicellular division of the medial vestibular nucleus and the ventromedial part of the PH to motoneurones innervating the masseter muscle. The anatomical pathways surrounding the vestibulo-trigeminal functional relationships as well as the VEMPs are outlined in Fig. 7.

Figure 7. Anatomical pathways involved in masseter responses to vestibular inputs.

Figure 7

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The diagram is based on recent neuroanatomical findings obtained in rats following retrograde labelling of vestibular neurones by pseudorabbies virus-Bartha injected into the masseter muscle (Giaconi et al. 2006) and following a dual labelling of trigeminal motoneurones by both an anterograde tracer injected in the vestibular complex and a retrograde tracer injected in the masseter muscle (Cuccurazzu et al. 2007). These findings showed that the MVe/SpVe/PH complex (outlined by a bold line) is connected to the ispilateral and contralateral motor trigeminal nucleus, through multisynaptic pathways as well as through a direct and crossed monosynaptic pathway. For simplicity, only ipsilateral pathways are outlined in the diagram. The VEMP circuit is also shown. XI. accessory motor nucleus; C1–C5, spinal cord from the first to the fifth level; I5, intertrigeminal nucleus; LVe, lateral vestibular nucleus; Mo5, motor trigeminal nucleus; MVe, medial vestibular nucleus; MVST, medial vestibular spinal tract; P5, peritrigeminal zone; PH, prepositus hypoglossi nucleus; Pr5, principal trigeminal nucleus; RF, pontomedullar reticular formation; Sp5, spinal trigeminal nucleus (O, pars oralis; I, interpolaris; C, caudalis); SpVe, spinal vestibular nucleus; Su5, supratrigeminal nucleus; SuVe, superior vestibular nucleus.

Although some functional data obtained in humans (Deriu et al. 2000) confirm functional findings obtained in animals (Tolu & Pugliatti, 1993; Tolu et al. 1996), it should be noted that the anatomical data above were obtained in rats, and must be applied to humans with due caution, until further data are available from localized lesions in clinical studies. However, when this work is completed we propose that VMR may be a useful addition to existing methods for testing (Ref. in Aramideh & Ongerboer de Visser, 2002) the functional integrity of brainstem circuits in humans.

Possible functional implications of sound-induced masseter responses

At this stage no conclusive answer to the question about the functional meaning of the vestibulomasseteric reflex and of the jaw acoustic reflex can be given without a large number of new experiments. However, we would like to offer some speculation, although there is no evidence for it so far.

Vestibular inputs may evoke phasic reflexes to stabilize the position of a given part of the body in response to sudden imposed disturbances, or they may act to define a desired position with respect to gravity. The receptors mediating responses specifically dependent on gravity are the otholiths, which are sensitive to tilt (Fernandez et al. 1972) and are activated by sound in a way that resembles natural linear acceleration (Ogawa et al. 2000; Uchino et al. 1997b). In this respect, the natural function of the vestibulomasseteric reflex may be to respond to sudden head tilt upwards or downwards. For instance, if the head is suddenly dropped, it may be of value to inhibit the masseters, and vice versa if the head is suddenly pitched upwards. In the same respect, a vestibular influence on the masseters may contribute to stabilize the jaw during locomotion, together with soft-tissue visco-elasticity and stretch reflexes (Miles et al. 2004a,b), or to keep forces equal on each side of the mandible while chewing with the head tilted to one side. This last hypothesis may be supported by our earlier findings of a tilt-induced asymmetrical modulation of the VMR amplitude (Deriu et al. 2005) as well as of tonic masseter activity (Deriu et al. 2000). This vestibular action may be of importance in adjusting precisely the forces and movements when the subject performs motor tasks requiring asymmetric activation of the masseter muscles, such as during extreme laterotrusion and protrusion/retrusion (Goto et al. 2001).

The vestibulomasseteric reflex appears to be weak, requiring the average of many trials to become evident, which makes one doubt its value for controlling the muscles in a real-time manner. However, it may be that it modulates activity at a more subtle level than is suggested by an overt reflex response. Its consistency and reproducibility in all subjects is compatible with this idea. Indeed, the fact that the pathway is so direct, having at the most only three synapses (vestibular receptors–vestibular nuclei–motor trigeminal nucleus–neuromuscular junction) (Fig. 7) makes us suspect that it may well have an important physiological role.

As for the function of the jaw acoustic reflex, the fact that it is inhibitory may allow it to play a role in preventing the subject biting his/her tongue when startled. It would thus be a local protective response as first suggested by Meier-Ewert et al. (1974).

Acknowledgments

This work was supported by grants from the Regione Autonoma della Sardegna (RAS) and from the Ministero dell'Istruzione, dell'Università e della Ricerca (MIUR).

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