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NEUROSCIENCE |
1 MRC Human Movement Group, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, Queen Square, London WC1N 3BG, UK
2 Institute of Neurological Sciences, Prince of Wales Hospital and School of Medicine, University of New South Wales, Sydney 2031, Australia
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Abstract |
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(Received 10 June 2006;
accepted after revision 21 August 2006;
first published online 31 August 2006)
Corresponding author B. L. Day: Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, 8-11 Queen Square, London WC1N 3BG, UK. Email: bday{at}ion.ucl.ac.uk
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Introduction |
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Large oscillatory mechanical stimuli exert a net excitatory effect upon the hair cell bundles through an imbalance between the maximal amplitudes of depolarizing and hyperpolarizing phases of the response (Hudspeth, 1989). Similar mechanisms may underlie activation of vestibular hair cells by sound and vibration conveyed through the endolymph. In experimental animals (cats, guinea pigs, squirrel monkeys) intense air-conducted sound, in addition to being a cochlear stimulus, activates vestibular afferents arising predominantly from the sacculus (Young et al. 1977; McCue & Guinan, 1994; Murofushi et al. 1995). The value of this stimulus for human experimentation is limited by the intensities that are required. Although it is safe to apply short-duration stimuli (clicks and tone bursts), which usefully evoke neck and leg muscle responses (Colebatch et al. 1994; Watson & Colebatch, 1998; Murofushi et al. 1999), the long-duration stimuli required to produce functional whole-body balance responses could be unsafe. In recent studies performed in guinea pigs, audio-frequency bone-conducted sounds of relatively low intensity (median threshold of 44 dB above that for brainstem auditory-evoked potentials) delivered via a clinical bone conductor have been found to selectively activate the irregular afferents of otolith origin (Curthoys et al. 2006). In man, 250–1000 Hz bone-conducted tones (at 70–80 dB above hearing threshold) delivered via the mastoid produces short-latency vestibular-evoked myogenic potentials (VEMPs) recorded from sternocleidomastoid (SCM) muscles (Sheykholeslami et al. 2000; Welgampola et al. 2003). This method therefore is a good candidate for a safe means of activating human vestibular afferents with the long-duration stimuli required to evoke functional balance responses.
In the present study, we wished to determine whether a bone-conducted tone delivered via the mastoid is capable of producing whole-body sway responses in standing subjects, and if so whether the response is consistent with being of vestibular origin. As this study is the first of its kind, we have measured some fundamental characteristics of the sway response (time course, magnitude and direction) and its intra- and intersubject reproducibility. We used a stimulus frequency (500 Hz) known to activate vestibular afferents in guinea pig and man (Curthoys et al. 2006; Welgampola et al. 2003), and a stimulus duration (2–3 s) known to evoke a well-developed whole-body balance response to galvanic vestibular stimulation (Day et al. 1997).
Although we deliberately stimulated over bone, the vibration could be transmitted to muscle spindles by conduction along the bone and tendons. When applied directly to relaxed human muscles and tendons, vibration stimulates muscle spindle primary endings resulting in an abrupt increase in group Ia afferents' discharge rates at the stimulus frequency (up to 200 Hz) or sub-harmonic frequencies (Burke et al. 1976). In the cat, vibration-evoked spindle responses have been reported at frequencies as high as 500 Hz (Brown et al. 1967), the vibration frequency used in the present study. If neck muscle spindle afferents are excited by bone-transmitted vibration then they could produce a whole-body sway response. We therefore compared the direction and magnitude of body sway responses upon stimulation of bone (mastoid and temporal fossa) and of neck musculature at different sites. We specifically chose posterior neck muscles and sternocleidomastoid muscles, which insert over the mastoid process and are the most likely postural muscles to receive transmitted vibration.
To test further whether the sway response might be of vestibular origin we examined the dependence of the evoked sway direction on changes in head position with respect to the feet. Since the vestibular system signals accelerations in craniocentric coordinates, the sway direction of a pure vestibular-evoked response must change by the same amount and in the same direction as a change in head yaw angle.
Finally, we compared the time course and direction of sway produced by the unilateral bone-conducted tone stimulus with that produced by unilateral cathodal galvanic vestibular stimulation (GVS) of the same side. We expected that comparison of these sway profiles in the same subjects would yield information on the end organs activated by the stimulus. GVS activates otolith and semicircular canal afferents (Lowenstein, 1955; Goldberg et al. 1984), but by a process of vector addition and cancellation (Fitzpatrick & Day, 2004; Day & Fitzpatrick, 2005) the net vestibular input is thought to be dominated by the canal component. This is reflected in the directional properties of the whole-body sway response (Cathers et al. 2005) and in the oculomotor response (Schneider et al. 2000) to GVS. If the bone-conducted tone selectively activates otolith afferents with negligible activation of semicircular canal afferents (Curthoys et al. 2006), different sway directions would be expected from the two modes of stimulation. Part of these data has been presented in abstract form (Welgampola & Day, 2004).
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Methods |
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Stimuli and equipment
Bone-conducted tones. Tones were generated using a custom-made gated oscillator controlled by a logic signal and delivered via B71 clinical bone vibrators (Radioear Corporation, New Eagle, PA, USA) which were placed over each mastoid. The B71 is a commonly used piece of audiometric equipment, with a total weight of 19.9 g. The vibrator is housed in (3.0 cm x 1.5 cm x 1.5 cm) plastic casing with a (circular) mastoid contact plate of 1.77 cm2. Each vibrator is secured with a steel spring head-band, which holds it against the mastoid with a force of 4.5–5 N.
The bone conductors were calibrated using a Bruel and Kjaer 4930 artificial coupler and a Bruel and Kjaer 2203 Sound Level Meter (calibrated to read 0 dB at 1 µV). The force sensitivity constant of the coupler was 132 mV N–1 (or 132 x 10–9 V µN–1). The reference equivalent threshold force levels for bone conductors are given in decibells referenced to 1 µN (1 µN = 0 dB). The intensity of our bone-conducted tones using this reference are noted as dB FL (force level). The difference in dB between the µV scale (on the sound level meter) and µN scale is 17.6 (20 log (1 x 10–6/132 x 10–9)).
Stimuli of 500 Hz, 20 V peak-to-peak (p-p) (136 dB FL) lasting 2 s (experiments 1–3) or 3 s (experiment 4) were used. Mastoid vibration was delivered using two B71 clinical bone vibrators placed approximately 3 cm posterior and 2 cm superior to the external acoustic meatus. Care was taken to ensure contact between bone and the entire contact surface of the conductor. The final position of the stimulator was marked such that the same location would be used during the entire study.
Visible startle responses were seen in the first few trials of most subjects. We therefore gave 10 trial stimuli to all subjects before commencing data collection
Galvanic stimulation
In experiment 4, 1 mA monaural cathodal galvanic stimulation was delivered using 2.5 cm diameter circular neurostimulation electrodes (PALs plus, Nidd Valley Medical Ltd, Knaresborough, UK). The active electrode was placed over the left mastoid process and the reference over the T2 spinous process using Micropore. adhesive surgical tape (3M). Electrode gel (Dracard, Maidstone, UK) was used over the electrode–skin interface to improve conductance.
Accelerometer recordings
Peak acceleration was measured in response to a 500 Hz, 136 dB FL, 2 s stimulus (over the standard location) in a single subject using an Entran egaXT-50 uniaxial accelerometer (Fairfield, NJ, USA) attached to the mastoid tip with double-sided adhesive tape. The sensitive axis was aligned mediolaterally, normal to the plane of the mastoid.
Data collection and analysis
Before commencement of each trial, subjects stood quietly on the force platform with their feet together and eyes shut. Data collection was initiated by the experimenter with a button press and commenced after a random delay of 50–500 ms. Each collection lasted for 8 s in total. For every condition tested, each subject's mean response was obtained by averaging 20 trials offline, using a program written in MATLAB (MathWorks Inc., Natick, MA, USA). To quantify whole-body mean responses, we measured three parameters: the changes in ground reaction forces, the velocity of body motion and the body's position change. These measures were expressed in terms of magnitude and direction.
Ground reaction force data were collected using a fixed (Kistler type 9281B, Kistler Instrumente AG, Switzerland) force plate. Forces acting upon the body in mediolateral (x), anteroposterior (y) planes were measured from 0 to 450 ms post stimulus onset. The magnitude and direction of their vector sum (horizontal force response) was calculated. The position of the point of application of the ground reaction force in the horizontal plane (centre of pressure; CoP) was calculated.
The 3-dimensional position and velocity of an infrared marker attached to the prominence overlying the C7 spinous process was measured at 200 Hz using a CODA mpx 30 motion detection system (Charnwood Dynamics, Rothley, UK). For the final study, additional markers were placed at other sites on the body (see experiment 4 below). The magnitude and direction of the peak velocity of the C7 marker between 0.75 s and 2 s from stimulus onset was measured. The magnitude and direction of position change of the C7 marker in the horizontal plane was measured at a fixed interval of 0–2 s from stimulus commencement.
For single-trial analysis, we estimated the magnitude of response displacement in each individual trial by measuring the component of body displacement that occurred in the direction of the subject's mean response, normalized to the magnitude of the mean response. Thus, if in a single trial the subject swayed in the same direction and by an equal amount as her mean response, the single-trial response would be assigned a value of one. If she swayed by the same amount at either 90 or 180 deg to the mean angle, the single-trial response would be assigned values of 0 and –1, respectively. This method was chosen to take into account both the magnitude and direction of movement.
Experimental protocols
Experiment 1. Baseline study. Ten subjects stood facing forwards and were randomly presented with a right mastoid, left mastoid or a null stimulus. Sixty responses (20 per condition) were recorded and averaged separately for each of the three (left, right, null) conditions.
Experiment 2. Comparison of muscle vibration with mastoid vibration. Sixteen subjects were studied facing forwards. One bone conductor was placed over the left mastoid (standard location/control stimulus). The second one was placed in 1 of 5 alternative locations on the left side: the upper 1/3 of the sternocleidomastoid muscle (SCM) overlying the tendon; the middle 1/3 of the SCM overlying the muscle belly; the lower 1/3 of the SCM over it's clavicular head; on the posterior neck muscles, lateral to the superior part of trapezius; over the temporal fossa 4 cm directly above the external acoustic meatus. This experiment was conducted in five blocks. During each block, 40 stimuli were randomly delivered at one every 60 s over the standard or alternative locations. Between blocks the stimulators were removed from the head and subjects were allowed to sit down and rest for a minimum duration of 10 min.
Experiment 3. Effect of head yaw position. Eight subjects participated in this study. Their naso-occipital axes were approximately aligned to each of the five following directions presented in random order: 90 deg to the left, 45 deg to the left, directly forwards, 45 deg to the right, 90 deg to the right. The feet were always aligned to the sagittal plane. The head position was recorded, using infrared markers attached to symmetrical sites over both tragii. Left or right mastoid stimuli were presented randomly with 40 trials recorded for each head yaw angle.
Experiment 4. Comparison of galvanic vestibular stimulation and vibration. Ten subjects were studied, using 3 s, 136 dB FL, 500 Hz tones delivered over the left temporal fossa or 3 s, 1 mA GVS delivered over the left mastoid. This study also enabled us to observe the effects of a longer duration stimulus. The order of stimulus presentation was randomised. Twenty stimuli were delivered for each condition. Displacement of markers placed over the occiput, C7, T7 and L3 spinous processes, ground reaction forces and centre of pressure (CoP) displacement were measured.
Statistical methods
Measures of magnitude. The parameters measured (magnitude of force, velocity, position) were analysed using repeated measures ANOVA (version 11, SPSS Inc., Chicago, IL, USA). Planned contrasts were used for comparison between levels. When required, further post hoc comparisons were performed using paired t tests. Significance was taken as P < 0.05. The descriptive data are given as mean ± S.E.M. unless otherwise specified.
Measures of direction. Although linear statistical methods can be applied to directional data when the values are closely clustered, angular measures that are widely separated cannot be treated statistically as linear data. This is true for descriptive statistics as well as inferential statistics.
Conventions used to describe angles. All directional data were expressed as angles ranging from 0 to ±180 deg using the convention of 0 deg pointing forward and horizontally in the mid-sagittal plane, with directions to the left of zero being positive and directions to the right being negative (Fig. 1A).
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1, 2, ...
n, would thus have a series of x and y coordinates x1, x2, ...
xn and y1, y2, ...
yn. The mean x- and y-values can be calculated as follows:
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can now be calculated as follows:
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represents the direction of the mean vector of the sample 1, 2, ...
n.
The length of the mean vector (r) is equal to the resultant vector (of all the x and y coordinates) R divided by n (sample size). For a series of angles 1, 2, ...
n the resultant vector is calculated as follows: the x coordinate of the resultant vector is the sum of all the x coordinates for 1, 2, ...
n, or (
sin ). Its y coordinate is the sum of all the y coordinates for 1, 2, ...
n (cos ). The resultant of the summed x and y coordinates is then calculated.
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Tests of significant clustering of angles. For each sample of angular data we used the Rayleigh test (using r as the test statistic) to check whether there was statistical evidence of ‘directedness’ (i.e. whether the population from which the angles are drawn differ significantly from randomness). When r is large (i.e. close to 1), the null hypothesis of randomness can be rejected in favour of directedness (Batschelet et al. 1981). The critical level of r for a sample varies with its size. We used a significance level of 0.05. Examples of a significantly clustered group of angles and a randomly distributed group are given in Fig. 1B.
Pair-wise comparisons.
To examine differences between paired angular observations (1, ß1;
2, ß2 . . . n, ßn) we used Moore's modification of Rayleighs test, a non-parametric method of pair-wise comparison (Moore, 1980; Zar, 1999; Sparto & Schor, 2004) using the following steps:
= sin ; Xß
= sin ß; Y
= cos ; Yß
= cos ß); |
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,ß)2
+ (Y,ß)2]1/2 
= tan–1
=
X,ß/Y,ß |
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The test statistic R' is then calculated as in eqn (5) and compared against critical values provided by Moore (1980).
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Correlations.
When examining correlations between two sets of angular data (1, ß1;
2, ß2 . . . n, ßn), we first used conventional linear scatterplots and linear regressions. Conventions of –360 to +360 deg were used to avoid discontinuity between data points that lay close to each other but across the ±180 deg line. However, this sometimes required subjective assessment of where a data point should lie. Therefore, we performed a more rigorous parametric circular–circular correlation using a modified correlation coefficient R2 (Batschelet, 1981; Mardia & Jupp, 2000) with angles within ±180 deg. This modified coefficient incorporates the following six correlation coefficients and is computed using eqn (6):
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n, ßn is rejected for large values of R2. Under independence, nR2
=
2 (Batschelet, 1981). |
Results |
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Whole-body response characteristics
With the subject facing forward and eyes closed, 500 Hz vibration applied unilaterally to the mastoid process produced a consistent whole-body response. In single trials the response was superimposed on the random body sway of bipedal stance. Stimulus-locked averaging of 20 trials largely cancelled out the random spontaneous sway to reveal the mean stimulus-evoked response. In our recordings the earliest manifestation of the response was a force impulse between the feet and ground. It began 
250 ms after stimulus onset and peaked at 450 ms (Fig. 2A). On average, it caused the body to sway in an anterolateral direction away from the stimulated mastoid (Fig. 3A). The magnitude of body velocity peaked around 0.75–1.5 s after stimulus onset (Fig. 2B). Displacement of the body began at 400 ms. By the end of the 2 s stimulus the body had moved to a new position relative to its start position, maximal displacement being achieved some 400–500 ms later (Fig. 2C). Following stimulus cessation, a similar but oppositely directed sequence of events returned the body approximately to its start position. We measured the magnitude and direction of three variables (initial force, peak velocity, position change) to define the average on-response at different stages of its development.
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To investigate the possibility of response habituation, we analysed data on an individual trial basis from the baseline study (experiment 1) in which each subject was stimulated 40 times. Figure 4C shows the trial-by-trial normalized displacement for a single subject and the mean normalized displacement for all 10 subjects. Linear regression of the normalized displacement against trial number gave an r value of 0.17 (P = 0.3) and no evidence of response habituation.
Comparison with direct neck muscle vibration
The mean sway paths to vibration delivered at five different sites over the skull or neck muscles together with the standard mastoid site are shown in Fig. 5A. In this experiment mastoid vibration trials were randomly interleaved with vibration at one other site in five blocks of trials. However, for the purpose of statistical analyses we have taken the mastoid response as the average of all mastoid trials.
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For all three SCM sites there were no consistent directions of response within the group (see Table 2 and Fig. 5C) and so were not analysed further. For the posterior neck muscle site there was significant clustering of force and position directions (r = 0.49, 0.68; P = 0.022, P < 0.001, respectively), but the mean directions (force: 27.3 deg; position: 6.05 deg) were significantly different to the mastoid site (P < 0.001 for both). For the temporal fossa site there was significant clustering of force, velocity and position directions (r = 0.61, 0.75, 0.78; P < 0.002, P < 0.001, P < 0.001, respectively). In this case the mean directions (force: –85.2 deg; velocity: –61.6 deg, position: –67.57 deg) were not significantly different to the mastoid site (P > 0.1 for all 3).
Effect of head yaw position
Figure 6A illustrates the effect of five head yaw angles (+ 90, +45, 0, –45, –90 deg) on the mean sway paths in eight subjects. It shows that response direction was not fixed in body or room coordinates but was a function of head angle. The scatter plot shown in Fig. 6B suggests there was a linear relationship between sway direction and head yaw angle. Statistically, the direction of the initial force (F), the direction of body motion at peak velocity (V) and the direction of displacement (P) were significantly correlated with head yaw angle (H). Thus, the circular–circular correlations between F, V, and P with H for left mastoid stimulation yielded modified correlation coefficients (Mardia & Jupp, 2000) of 0.79, 0.92 and 1.2, respectively (corresponding values for nr2 = 31.6, 36.9, 48.0; probability of independence < 0.001 for all 3). For right mastoid stimulation, the modified coefficients for F, V and P were 0.83, 0.49, 0.75 (nr2 = 33.2, 19.6, 30.0; P < 0.001 for all 3). The slopes of the relationships obtained from linear regression were close to unity (1.01, 1.07 and 0.98, respectively, for F, V and P) suggesting the response was organized in a craniocentric reference frame. The response magnitudes were unaffected by head yaw angle (F4,56 = 2.1, 0.362, 0.89, P = 0.08, 0.83, 0.48 for F, V and P, respectively) (Fig. 6C).
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There were a number of similarities between the responses to unilateral bone-conducted sound and unilateral GVS (cathodal), as shown in Fig. 7. Both caused the body to sway away from the side of stimulation with a similar time course and similar kinematic profile. Thus, higher body markers displaced further than lower sites and there was an overall shift in the centre of pressure (CoP) of the ground reaction force, which when the body is in a quasi-static state reflects displacement of the body's centre of mass (CoM). This pattern suggests that for both stimuli a major component of the response consisted of body sway about the feet and ankle joints.
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The major distinguishing feature between the two stimuli was in the direction of the evoked response (Fig. 7B). The mean directions of the on-response initial force, peak velocity and position were significantly clustered for both vibration (force: –56.7 deg., r = 0.89, P < 0.001; velocity: 47.1 deg, r = 0.93, P < 0.001; position: 52.7 deg., r = 0.94, P < 0.001) and GVS (force: –86.6 deg, r = 0.97, P < 0.001; velocity: –78.3 deg, r = 0.98, P < 0.001; position: –79.3 deg., r = 0.97, P < 0.001) For all three measures the mean response directions were significantly different for the two stimuli (force: P < 0.01; velocity: P < 0.001; position: P < 0.005; Moore's method of comparing paired angular data). The linearity of the mean sway path also appeared to differ for the two responses with GVS producing a more curved path (Fig. 7B). However, this may have been a consequence of the difference in response directions. The sway vector to GVS was such that subjects' CoM moved further laterally taking them to a position of greater instability. This would have been signalled by other sensory systems, e.g. proprioceptors, which are known to modify the developing GVS-evoked response (Day & Cole, 2002), causing the sway path to be modified.
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Discussion |
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Other investigators have reported that, although neck muscle vibration evokes measurable sway, mastoid vibration does not (Andersson & Magnusson, 2002; Magnusson et al. 2004). Our stimulus differed from their's in that it was generated by a different stimulus source with a higher stimulus frequency. Stimuli used in these previous studies had a frequency of 120 Hz or less. For myogenic potentials evoked by bone-conducted tones, well-formed responses are obtained using stimuli of 250–1000 Hz (Welgampola et al. 2003) with maximal amplitudes at 200–400 Hz (Sheykholeslami et al. 2001). Vibration at 500 Hz has been shown to be an effective stimulus for activating vestibular afferents in guinea pig (Curthoys et al. 2006). Our choice of stimulus frequency was governed by these observations and by the output of our stimulator, which is maximal at 500 Hz. Was our stimulus source better suited to evoke a sway response since it generated a signal that is more lateralized? Using the vestibular-evoked myogenic potential as a marker of vestibular input, we suspect that vibration delivered via a bone conductor is also transmitted bilaterally but not symmetrically since the response is 30% larger ipsilaterally (Welgampola et al. 2003). Our measures of head acceleration also indicate asymmetrical stimulation.
Does muscle spindle input contribute to the response?
It is well established that vibration of posterior neck muscles can evoke a forward whole-body sway response in standing subjects (Gregoric et al. 1978; Lund, 1980). Furthermore, the sway response direction changes with head yaw position indicating organization in a craniocentric reference frame (Ivanenko et al. 1999). The vibration frequencies used in their experiments were an order of magnitude lower than the frequency used in the present study, but we were able to replicate forward sway behaviour using 500 Hz vibration applied directly to posterior neck muscles. The precise mechanisms underlying the whole-body sway responses to posterior neck muscle vibration are not clear. Responses are either abolished or dramatically reduced in subjects with bilateral loss of vestibular function (Lekhel et al. 1997). In subjects with unilateral vestibular lesions the sway response is smaller and in a different direction compared with normal (Popov et al. 1996; Lekhel et al. 1998). A simple explanation for the absence or reduction of sway in these lesions would be that vibration-evoked vestibular input normally contributes to the sway response. An alternative explanation, and one that is favoured by Lekhel et al. (1998) and Popov et al. (1996), is that the sway response is driven exclusively by vibration-evoked muscle spindle input but modified by concurrent vestibular information. Their argument is that the change in muscle spindle input generated by vibration mimics a stretch of the posterior neck muscle, as though the neck were flexed, but the vestibular system signals that the head has remained upright. The brain therefore interprets the situation as a backward lean of the body together with a neck flexion that keeps the head upright. The apparent unplanned backward lean of the body is compensated by a forward directed whole-body sway.
Could our mastoid sway response have this mechanism? Mastoid vibration could potentially be transmitted to nearby anterior or posterior neck muscles. The sternocleidomastoid (SCM), which inserts over the mastoid process, contributes to contralateral rotation of the head, ipsilateral lateral flexion and forward flexion of the neck. The splenius, which also inserts over the mastoid, contributes to ipsilateral rotation of the head, ipsilateral lateral flexion and extension of the neck (Gray, 1918). If SCM and splenius were activated together then most of these actions would cancel out to leave lateral neck flexion. Vibration-evoked muscle spindle input from both muscles would therefore mimic the muscle lengthening associated with contralateral lateral neck flexion. Using the argument outlined above, this would be interpreted as an unplanned ipsilateral lean of the body demanding a body sway away from the stimulated side. This is close to the observed behaviour. The additional forward component of the observed sway response could be simply explained by an asymmetrical signal from the two muscles with splenius providing the stronger input.
The evidence that favours more a vestibular rather than muscle spindle origin of the mastoid response comes from the results of stimulating at other sites. When the stimulator was moved off the bone and placed directly on the SCM muscle its spindle input should have increased. The direction of the response might be expected to change since the posterior neck muscles would contribute less to the input, but the direction should be just as consistent between subjects. However, we found this was not the case. The response magnitude became smaller and the response direction lost its consistency as the stimulator was moved further from the mastoid. Presumably by stimulating the soft tissue of muscle there was less transmission of vibration to the vestibular organs. In contrast, when we moved the stimulator off the mastoid to a point 4 cm above the external acoustic meatus the response was unchanged. The natural action of the nearby muscles (auricularis superior and temporalis) do not involve head or neck movements, therefore activation of their primary afferents should not evoke a sway response. A transmitted response by propagation of the signal to the posterior neck muscles is possible, but not likely to be the dominant mechanism since the average magnitude of displacement evoked by temporal fossa vibration was twice the displacement evoked by posterior neck vibration. The temporal fossa location, by its ability to generate well-formed vestibular-evoked myogenic potentials (Welgampola et al. 2003) has been shown to be an optimal site (as is the mastoid process) for vestibular activation by bone-conducted sound in humans. The sway responses evoked by temporal or mastoid stimulation are therefore likely to be predominantly vestibular in origin.
Does cochlear stimulation contribute to the response?
Bone-conducted sound activates both vestibular and cochlear afferents. The dependency of sway upon head orientation and the similarity of the initial rapid force responses observed at the onset and offset of GVS and vibration may be more indicative of a vestibular-evoked response. However, a cochlear contribution to the vibration-evoked sway response cannot be excluded until similar responses are recorded from subjects with isolated profound hearing loss.
Comparison with sway evoked by air-conducted sound
Lower limb EMG responses and sway evoked by air-conducted sound have been described by Dieterich et al. (1989) in a subject presenting with the Tullio phenomenon. They reported anterolateral displacement of the body towards the stimulus. Russolo et al. (2002) also reported mediolateral sway towards the stimulated ear in response to air-conducted tone bursts of 500 Hz in healthy subjects. These findings differ from ours and raise the possibility that sway responses to long duration air- and bone-conducted sound may differ in direction, thus implying activation of different vestibular afferents. However, the studies performed by Watson & Colebatch (1998), who reported soleus EMG responses evoked by intense auditory clicks, are contrary to these findings. The soleus EMG responses to monaural clicks were of similar polarity to soleus EMG responses evoked by monopolar cathodal stimulation and consisted of an initial short latency component and an oppositely directed medium latency component. Since the direction of the medium latency component in galvanic-evoked soleus EMG responses usually reflects the direction of sway (away from the cathodal ear), the findings of Watson and Colebatch can be extrapolated to suggest that air-conducted sound also evokes sway away from the stimulated ear. This question is best resolved by studies using air- and bone-conducted stimuli of similar intensity and duration in the same subjects.
Origin of bone-conducted sway
Cathers et al. (2005) suggested that the whole-body sway response evoked by bilateral bipolar GVS consists of a small otolith-mediated component plus a larger and more dominant semicircular canal-mediated component. The semicircular canal input produced by unilateral cathodal GVS used in the present study can be calculated from the model proposed by Fitzpatrick & Day (2004) using known canal coordinates (Blanks et al. 1975) and the assumption that afferents from all three semicircular canals are equally weighted and equally activated by GVS. This calculation yields an expected sway direction of –79 deg in response to a left-sided cathodal stimulus. This predicted sway direction agrees well with the measured sway direction (–79.3 deg for the position response) and suggests that the GVS-evoked response is indeed dominated by inputs from the semicircular canals. The bone-conducted sway response was not in the same direction as the GVS response implying that the afferent input was different for the two types of stimulation. This is in agreement with the recent work of Curthoys et al. (2006) who showed that the dominant response to bone-conducted sound in the guinea pig comes from the otoliths, with little if any response from the semicircular canals.
Vestibular-evoked myogenic potentials (VEMPs) generated by air-conducted clicks and tones (Colebatch et al. 1994) are thought to represent sacculocollic pathways (McCue & Guinan, 1994, 1997). VEMPs evoked by bone-conducted tones demonstrate partial phase cancellation by air-conducted tones, indicating that the two stimuli may activate common receptors (Welgampola et al. 2003). Loss of VEMPs evoked by both air- and bone-conducted sound following inferior vestibular nerve section (Brantberg & Mathieson, 2004) also points to significant saccular activation by both stimuli. However, it is unlikely that our whole-body responses to bone-conducted tones arise from a pure saccular input. The saccular maculae lie predominantly in the sagittal plane and so a pure saccular stimulus should result in a whole-body response also predominantly in the sagittal plane. If our sway responses are mediated exclusively by otolith afferent input, the lateral component of sway direction suggests there is likely to be a significant utricular component to the input, which is consistent with the afferent responses recorded in guinea pig (Curthoys et al. 2006). If the response is otolith mediated it is not clear why bone vibration transmitted to the saccular and utricular maculae, with their multidirectionally aligned hair cells, would produce such a consistent sway response direction. Although there was appreciable inter- and sometimes intrasubject variability, the response was far from being randomly represented in all possible directions. Even when the stimulation site was moved from the mastoid to the temporal fossa a similar mean sway direction was obtained. One explanation could be that non-specific activation of the total population of unilateral otolith afferents (plus possibly a weaker but similar contribution from the opposite side) is equivalent to a consistently directed linear acceleration through vector summation of the individual hair cells' preferred directions. Alternatively, there could be a specific activation of otolith hair cells with a preferred orientation with respect to the axis of the applied vibratory stimulus.
In summary, bone-conducted sound evokes consistent craniocentric whole-body responses in standing subjects. The characteristics of the response are compatible with it being mediated by vestibular input, although the sway direction is different to that evoked by galvanic vestibular stimulation. This suggests that different patterns of input are produced by the two types of stimulation, possibly involving different proportions of afferents from the otoliths and semicircular canals. If so, bone-conducted sound, used either in isolation or in combination with GVS, may enable investigation of hitherto unexplored aspects of vestibular function in intact freely behaving human subjects.
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