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Vibration-Induced Shift of the Subjective Visual Horizontal
A Sign of Unilateral Vestibular Deficit
Mikael Karlberg, MD, PhD;
Swee T. Aw, MBBS, PhD;
G. Michael Halmagyi, MD, FRACP;
Ross A. Black, M Biomed E
Arch Otolaryngol Head Neck Surg. 2002;128:21-27.
ABSTRACT
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Background Vibration to the head or neck excites vestibular and neck muscle spindle
afferents. Can such vibrations improve the sensitivity of the subjective visual
horizontal (SVH) test to chronic unilateral deficit of the vestibular system?
Design Controlled experimental study.
Setting Tertiary referral center.
Patients and Controls Thirteen healthy subjects and 23 patients with chronic unilateral vestibular
deficits after vestibular neurectomy or neurolabyrinthitis. Results of head-impulse
test showed unilateral loss of function of all 3 semicircular canals in 14
patients and loss of anterior and lateral semicircular canals in 9 patients.
Intervention Unilateral vibration (92 Hz; 0.6-mm amplitude) applied to sternocleidomastoid
muscle (SCM) or mastoid bone.
Main Outcome Measure Results of SVH test (in degrees).
Results Without vibration, 13 of 23 patients and all healthy subjects had SVH
of less than 3° (sensitivity, 43%; specificity, 100%). During vibration
to the ipsilesional SCM, SVH increased to greater than 3° in 21 of 23
patients but in only 1 of 13 healthy subjects (sensitivity, 91%; specificity,
92%). The patient group had significantly greater SVH shifts to the ipsilesional
side than did healthy subjects in response to SCM and mastoid bone vibration
on either side. The SVH shift during vibration to the ipsilesional SCM was
significantly greater than that during vibration to the contralesional muscle
(P<.001) or to the mastoid bone on either side
(P<.05). The vibration-induced SVH shift was significantly
greater in those patients with loss of 3 semicircular canals than in those
with loss of 2 (P<.01).
Conclusions The sensitivity of the SVH test to chronic unilateral vestibular deficits
can be improved by applying vibration to the SCM. The magnitude of vibratory
SVH shift is related to the extent of unilateral deficit of the otolithic
organs, vertical canals, or both.
INTRODUCTION
THE SUBJECTIVE visual horizontal (SVH) (or vertical) is tested by asking
a subject seated in a totally dark room to set a dim light bar to the imagined
gravitational horizontal or vertical. After acute total unilateral vestibular
deafferentation (uVD), the SVH (or subjective visual vertical) is invariably
offset, always to the ipsilesional side by 20° or more.1-4
The SVH test can also give useful information about patients with suspected
peripheral or central vestibular lesions.5-8
In peripheral vestibular lesions at least, the offset of the SVH is due to
a tonic offset of torsional eye position and as such is an indirect measurement
of utricular function.2, 7 The
SVH invariably returns to normal or near normal, ie, 3° or less, within
a few weeks after uVD, owing to central compensation.2, 4
In other words, a small ipsilesional offset of the SVH, just within or just
outside the reference range, is often found in patients with chronic compensated
uVD.
We asked whether there was a simple, reliable way of accentuating such
a borderline or minimal offset of the SVH to produce a clearer result in a
patient suspected of having lost utricular function on one side. Others have
asked this question before us. For example, performing the SVH test with the
subject in a tilting chair or lying on one side has not distinguished patients
with longstanding unilateral vestibular deficits from healthy subjects.3, 9 In contrast, testing the SVH during
high-speed off-axis yaw rotation might accentuate the offset of the SVH in
patients with chronic uVD.1, 10
Vibration applied to the neck or head can induce illusions of movement
of a fixated visual target11-14
and small eye movements13-16
in subjects with normal vestibular function. In most patients with uVD, vibration
applied to neck muscles or to the mastoid bone induces nystagmus.17-19 Vibration has been
shown to excite semicircular canal (SCC) and otolith afferents in different
animal species.20-22
Consequently, the perceptual and ocular motor effects have been attributed
to a direct vibratory stimulation of intact vestibular receptors.14, 18-19 However, vibration
also increases the firing in muscle spindle afferents,23
and others have attributed the vibratory effects to an interaction between
neck proprioceptors and the vestibular system.11, 13, 15-16
Unilateral vibration to the sternocleidomastoid muscle (SCM) has no
effect on the SVH in healthy subjects. However, in a small series of patients
with uVD, vibration to the ipsilesional, but not the contralesional, SCM induced
a shift of the SVH.24 We set out to study how
vibration applied to the SCM or to the mastoid bone on one side affected the
SVH in patients with well-defined unilateral vestibular deficits. All patients
underwent head-impulse testing to assess the function of the 6 individual
SCCs,25-26 to determine whether
the magnitude of SVH response to vibration was related to a total or partial
unilateral lesion of the vestibular system.
SUBJECTS AND METHODS
PATIENTS AND CONTROL SUBJECTS
We studied 23 patients (12 men and 11 women; mean age, 53.6 years; range,
25-73 years) with well-defined unilateral vestibular deficits. They were recruited
from the outpatient clinic at the Department of Neuro-otology, Royal Prince
Alfred Hospital, Sydney, Australia, or from among patients in our clinical
database. Head impulses in the planes of the 3 pairs of SCCs were studied
in all patients to disclose the function of the 6 individual SCCs (Figure 1). Detailed descriptions of the equipment
and the procedures of head-impulse testing have been presented elsewhere.25-26 Eleven patients, 8 with vestibular
schwannoma and 3 with Meniere disease, had undergone unilateral vestibular
neurectomy. They had unilateral loss of function of all 3 SCCs. Twelve patients
had permanent unilateral peripheral loss of vestibular function after vestibular
neurolabyrinthitis, and all had a unilateral canal paresis found on results
of caloric testing. Of these 12 patients, 3 had lost function of all 3 SCCs,
and 9 had lost function of the anterior and lateral SCCs (ie, "superior vestibular
neuritis").27 The average time since the vestibular
lesion occurred was 35 months (range, 1-144 months). The clinical data of
the patients are presented in Table 1.
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Figure 1. Recordings of position and velocity
of the head and the left eye (eye recordings inverted for simplicity) from
patient 14. During a head-impulse directed toward the right posterior semicircular
canal (SCC), eye velocity matches head velocity perfectly; consequently eye
position also matches head position perfectly. In contrast, during head impulses
directed toward the right lateral SCC or the right anterior SCC, eye velocity
reaches less than half of head velocity, ie, vestibulo-ocular reflex gain
is less than 0.5°. This results in a large eye position error, which is
corrected with a series of saccades, the first of which is shown. The patient
thus had a right-sided lesion of the anterior and lateral SCCs, ie, superior
vestibular neuritis.
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Table 1. Summary of the Patients' Clinical Data and SVH Results*
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We also studied 13 healthy subjects (7 men, 6 women; mean age, 32 years;
range, 19-66 years) who were recruited from among the hospital and laboratory
staff. None of the subjects had any history of cochlear, vestibular, central
nervous system, or neck disorders. All subjects gave their written informed
consent after being briefed about the examination. The local ethics committee
approved the experimental procedures. All experiments were performed in accordance
with the Helsinki II Declaration.
VIBRATORY STIMULUS
We used a battery-powered, handheld vibrator (Mini Vibrator NC70209;
North Coast Medical, Inc, San Jose, Calif) with a frequency of 92 Hz and an
amplitude of 0.6 mm. The frequency did not change with increased pressure
to the neck or skull, as tested in a separate experiment on 3 healthy subjects.
The vibrating silicon tip was semispherical, with a radius of 8 mm. For head
vibrations, the tip of the vibrator was positioned perpendicular to the skin
overlying the mastoid bone behind the external ear canal and held in position
by hand. For vibrations applied to the neck muscles, we chose to vibrate the
SCM, as it is more superficial and easier to locate than the posterior neck
muscles. To standardize the site of vibration, the belly of the SCM and the
mastoid bone were palpated during active muscle contraction, and a point on
the muscle belly 20 mm below the tip of the mastoid bone was marked with a
pen. The vibrator was positioned on the marked spot, perpendicular to the
skin and held in position by hand (Figure
2A). We did not change the position of the vibrator until an illusion
of visual target movement was evoked as in previous studies.11-13,16
The same examiner (M.K.) delivered the vibrations to all subjects to reduce
the variability of the stimulus.
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Figure 2. A, Measurement of the subjective
visual horizontal during vibration to the left sternocleidomastoid muscle.
B, The middle bar is set to the true gravitational horizontal. The left bar
is set to the left (counterclockwise), which is seen after left-sided vestibular
loss of function. The right bar is set to the right (clockwise), which indicates
right-sided vestibular loss.
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MEASUREMENT OF THE SVH
The subject sat upright in a dark room with the head immobilized using
a head holder. This consisted of a molded neck rest that covered the back
of the head and neck and kept the head horizontal. The neck rest could be
adjusted in the vertical and anterior-posterior directions to fit every subject.
The subject's head was firmly held in the neck rest by a forehead holder with
3 padded clamps that could be individually adjusted. In front of the subject
at a distance of 1.3 m was a dim light bar, 2 mm wide and 120 mm long. It
could be rotated about its midpoint by means of an electric motor and a remote-control
device. The task for the subject was to adjust the bar to parallel alignment
with the perceived gravitational horizon. Owing to ocular torsion toward the
side of vestibular loss, a patient with a unilateral vestibular lesion will,
in the absence of other visual cues, perceive a truly horizontal line as being
tilted to the intact side. The same subject will set the light bar tilted
to the side of the vestibular lesion when asked to set it to the horizon (Figure 2B). During each test, subjects performed
10 settings of the light bar with both eyes open. The average of the 10 settings
was used as the measure of SVH. There was no time limit for performing the
test. The time to complete 1 set of 10 settings ranged from 60 to 120 seconds
across the subjects. Each subject first performed the SVH test without vibration
(baseline), then while vibration was applied to the right- and left-sided
SCMs and the right- and left-sided mastoid bones. The same test sequence was
used for all subjects. Between each test, the subjects rested for at least
1 minute.
STATISTICAL ANALYSIS
To enable the recordings from all patients to be used for statistical
analysis, individual data of SVH were pooled as if all patients had right-sided
vestibular lesions. A 2-tailed t test for paired
or unpaired observations was used to evaluate differences within the patient
group and between patients and healthy subjects. A difference of P<.05 was considered statistically significant.
RESULTS
All healthy subjects and 13 of the 23 patients had SVH within ±3°
without vibration (Table 1). This
yields a sensitivity of the SVH test to chronic unilateral vestibular deficits
of 43% and a specificity of 100%. During vibration to the ipsilesional SCM,
SVH increased to greater than 3° in 21 of the 23 patients (Table 1 and Figure 3).
Vibration applied to the mastoid bone or to the SCM of the healthy subjects
had small and inconsistent effects (Figure
3, Figure 4, and Figure 5 and Table 2). Only 1 of these subjects increased his SVH to more than
3° during SCM vibration. Thus, although the sensitivity of the SVH test
increased from 43% to 91%, the specificity decreased slightly from 100% to
92% during SCM vibration (Figure 3).
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Figure 3. Each line shows subjective visual
horizontal (SVH) at baseline and during vibration to the ipsilesional sternocleidomastoid
muscle (SCM) for individual patients with unilateral vestibular deafferentation
(uVD) (left) and healthy subjects (right). The shaded area indicates a ±3°
limit of SVH reference range. Without vibration, 13 of 23 patients and all
13 healthy subjects had SVH values within the reference range. During vibration,
SVH became abnormal in 21 of 23 patients and 1 of 13 healthy subjects.
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Figure 4. Subjective visual horizontal (SVH)
at baseline and during vibration to the sternocleidomastoid muscles (SCMs)
in a healthy subject (A), and patient 10 with right-sided (unilateral) vestibular
deafferentation (uVD) (B), and patient 7 with left-sided uVD (C). Baseline
SVHs were within the reference range. Vibration to the SCMs induced a small
shift of SVH to the vibrated side in the healthy subject. In the patients,
vibration to the SCM on either side shifted the SVH to the ipsilesional side.
CW indicates clockwise tilt (as seen in B); CCW, counterclockwise tilt (as
seen in C). Vibration to the ipsilesional muscle induced the largest shift.
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Figure 5. Subjective visual horizontal (SVH)
shift from baseline during vibration to the sternocleidomastoid muscles (SCMs)
(A) and to the mastoid bones (B) in healthy subjects (n = 13) and patients
with unilateral vestibular deafferentation (n = 23; mastoid bone vibration,
n = 21). In all patients except patient 23, the largest SVH shift was toward
the ipsilesional side, irrespective of the side of vibration. Other abbreviations
are defined in the legend to Figure 4.
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Table 2. Baseline and Vibration-Induced Shifts in SVH in Healthy Subjects
and Patients With uVD*
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The average baseline SVH was significantly larger in patients than in
healthy subjects (P<.001) (Table 1 and Table 2).
Mastoid bone and SCM vibration shifted the SVH to the ipsilesional side, irrespective
of the side vibrated, ie, clockwise (to the right side) in patients with right-sided
vestibular lesions and counterclockwise (to the left side) in patients with
left-sided lesions, except for patients 13 and 23 (Figure 4 and Figure 5).
The maximal SVH shift was 13.5° during mastoid bone vibration and 11.5°
during SCM vibration (Figure 5).
The vibration-induced shifts in SVH were significantly larger in patients
than in healthy subjects (P<.001) (Table 2).
Vibration to the ipsilesional SCM shifted the SVH significantly more
than did vibration to the contralesional side (P<.001)
or vibration to the mastoid bones on either side (P<.05).
No significant differences between the shifts of the SVH were found during
vibration to the contralesional SCM and vibration to the mastoid bone on either
side (P = .34) or between vibration to the mastoid
bone on either side (P = .20) (Table 2).
There was no difference in the baseline SVH between patients with unilateral
loss of 3 SCCs and those with loss of 2 SCCs (P =
.25). The patients with loss of 3 SCCs showed significantly larger SVH shifts
than patients with loss of 2 SCCs did in response to SCM vibration (P<.05) and a tendency to larger shifts during mastoid
bone vibration (P = .10) (Table 2). If SVH results from mastoid bone vibration to the ipsilesional
and contralesional sides were pooled together, patients with loss of 3 SCCs
had significantly larger SVH shifts (mean, 3.8°; 95% confidence interval
[CI], 1.4°-6.2°) than patients with loss of 2 SCCs (mean, 1.9°;
95% CI, 1.1°-2.6°; P<.05). Pooled data
from SCM vibration to both sides showed that the patients with loss of 3 SCCs
had significantly larger SVH shifts (mean, 4.4°; 95% CI, 2.6°-6.2°)
than patients with loss of 2 SCCs (mean, 2.3°; 95% CI, 1.4°-3.2°; P<.01).
COMMENT
Comparison of the vibration-induced effects on the SVH with an independent
test of otolith function would be ideal. Unfortunately, we have no direct
test of utricular function. Ipsilateral myogenic potentials can be recorded
from tonically activated SCMs during repeated monaural auditory stimulation
(vestibular evoked myogenic potentials [VEMPs]) and probably reflect saccule
function.28 In 6 of the 9 patients with loss
of 2 SCCs, we had recordings of VEMPs. No differences were found in baseline
SVH or in vibration-induced shift of the SVH between the 3 patients with loss
of VEMPs on the ipsilesional side and the 3 patients with preserved VEMPs.
Thus, we had to rely on results of head-impulse testing of the SCCs to get
a reliable measurement of the extent (total or partial loss) of the vestibular
lesion.
A high correlation between SVH and static torsional eye position has
been reported after uVD.2, 7 In
patients with vestibular neuritis, a high correlation was found between the
shifts in horizontal eye position and subjective straight-ahead position induced
by neck vibration.13 Head or neck vibration
can induce nystagmus with torsional components in patients with uVD.17-19 Whether head or neck
vibration also induces the sort of tonic torsional eye position shifts in
patients with uVD that could cause the vibration-induced SVH shift shown herein
remains to be investigated.
Vibration to the mastoid bone or SCMs on either side induced a shift
of the SVH toward the ipsilesional side in our patients. To our knowledge,
this is the first time that vibration to the mastoid bone or contralesional
SCM has been shown to shift the SVH in patients with uVD. The net effect of
an oscillating mechanical stimulus delivered to the hair bundle of a vestibular
receptor cell is excitatory.29 Vibrations with
frequencies above 80 Hz delivered to the heads of squirrel monkeys have been
shown to excite SCC and otolith afferents.20
Thus, a possible explanation of our results is that vibration to the mastoid
bone or to the SCMs results in a direct vibratory stimulation of the intact
vestibular receptors. However, we found that the shift of the SVH induced
by ipsilesional SCM vibration was significantly larger than that induced by
contralesional vibration or by vibration to the mastoid bone on either side.
This is in accord with previous reports of changes in visual perception in
yaw13 and roll24
induced by neck muscle vibration and might represent an increased central
weighting of somatosensory neck information from the side with the lesion,
which substitutes for missing vestibular input.13
The neck muscle vibrations of previous studies were standardized by
adjusting the position of the vibrator until the subject perceived an illusion
of movement of a stationary visual target.11-13,16
This position dependency has been used as an argument against vibratory stimulation
of vestibular receptors.11 However, the positioning
of the vibrator when it is applied to the head also affects the direction
of perceptual illusions. Vibration to the top of the head induces illusions
of vertical target movement, and vibration to the mastoid bone induces illusions
of horizontal movement.14 Vibration applied
to the mastoid bone might also propagate to neck muscles and thus stimulate
the neck proprioceptors. However, propagation of vibration from the skull
is probably not confined to those neck muscles that induce movements in a
certain plane. The direction of illusions of movement during vibration to
a muscle depends on the natural action of the vibrated muscle.30
The SCMs are contracted or stretched during head rotations about the naso-occipital
axis,31 and perceptual effects induced by SCM
vibration might thus be presumed to be in the roll plane. A possible way to
differentiate the effects of vestibular stimulation vs neck muscle afference
might be to stimulate both SCMs simultaneously. As the afferent information
from the muscle spindles then would signal neck extension (bilateral lengthening)
instead of roll tilt (unilateral lengthening), any effects on the SVH would
probably be due to stimulation of intact vestibular receptors.
Muscle spindle primary endings (type Ia) increase their firing harmonically
in response to vibrations up to about 80 Hz, but at higher frequencies they
start to fire in subharmonic patterns.23 Thus,
92 Hz, as used in our study, is an adequate frequency for stimulating muscle
afferents. After a 30-second vibration, 40 seconds are required for the spindles
of lower leg muscles in humans to return to normal resting activity and stretch
sensitivity.32 In our study, the subjects rested
at least 1 minute between the different vibrations. However, it is not known
whether neck muscle spindles manifest the same adaptive behavior or whether
there is central adaptation. Although there was no obvious order effect, a
larger variability of the SVH shifts was found in response to mastoid bone
vibration, which was always performed last in our test sequence. As the same
stimulus sequence was used for all tested subjects, adaptation or fatigue
might have accounted for this result.
During head tilt to one side, the SVH shifts to the opposite side, which
is the so-called E-effect.24 If the pressure
of the vibrator induced head tilts, we would expect an effect dependent on
which side was vibrated. We did not find this. The effect of vibration was
instead related to the side on which the vestibular lesion was located. Tactile
information regarding earth horizontal might be conveyed to the subject undergoing
testing by pressure from the chair and the head holder. This information remains
unchanged during the test, and we believe that it did not influence the results.
To sum up, the results show that vibration applied to the head or neck
is a simple way to increase the sensitivity of the SVH test to chronic unilateral
vestibular deficits. During vibration to the SCM, the sensitivity of the test
increased from 43% to 91%, whereas the specificity only decreased marginally
from 100% to 92%. Patients with unilateral loss of all 3 SCCs showed larger
vibration-induced shifts of SVH than did patients with loss of only the anterior
and lateral SCCs. This indicates that the magnitude of the vibration-induced
shifts in SVH reflects the extent of unilateral vertical SCC deficit or otolithic
deficit or both, but not the extent of the lateral canal deficit. The test
results thus give information that cannot be gained from the caloric test
results.
AUTHOR INFORMATION
Accepted for publication August 16, 2001.
This study was supported by the National Health and Medical Research
Council of Australia, Canberra; the Garnett Passe and Rodney Williams Memorial
Foundation, Melbourne, Australia; the trustees of the Department of Neurology
of the Royal Prince Alfred Hospital; the Swedish Medical Research Council,
the Wenner-Gren Foundations, and the Swedish Medical Association, Stockholm;
and the Maggie Stephens Foundation, Lund, Sweden.
Corresponding author: Mikael Karlberg, MD, PhD, Department of Oto-rhino-laryngology,
Lund University Hospital, SE-221 85 Lund, Sweden (e-mail: mikael.karlberg{at}onh.lu.se). Reprints: G. Michael Halmagyi, MD, FRACP, Department of Neuro-otology,
Royal Prince Alfred Hospital, Camperdown, Sydney, 2050 New South Wales, Australia
(e-mail: michael{at}icn.usyd.edu.au).
From the Department of Neuro-otology, Royal Prince Alfred Hospital,
Sydney, Australia (Drs Karlberg, Aw, Halmagyi, and Black); and the Department
of Oto-rhino-laryngology, Lund University Hospital, Lund, Sweden (Dr Karlberg).
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