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Comparison of Head Thrust Test With Head Autorotation Test Reveals That the Vestibulo-ocular Reflex Is Enhanced During Voluntary Head Movements
Charles C. Della Santina, PhD, MD;
Phillip D. Cremer, MBBS, PhD;
John P. Carey, MD;
Lloyd B. Minor, MD
Arch Otolaryngol Head Neck Surg. 2002;128:1044-1054.
ABSTRACT
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Objectives To compare 2 clinical tests of vestibular function, the head autorotation
test (HART) and the head thrust test (HTT), and to determine why they give
disparate results in patients with known unilateral vestibular deficiency
(UVD) due to labyrinthectomy.
Methods We used scleral coils to measure the horizontal (yaw) vestibulo-ocular
reflex (VOR) in 5 healthy human subjects and in 11 patients who underwent
labyrinthectomy. We used 2 paradigms. Using HART, subjects visually fixated
a target during self-generated, swept-frequency, sinusoidal, horizontal head
rotations. Using HTT, patients fixated the target during horizontal head thrusts
delivered randomly in direction and time.
Results In subjects without UVD, eye movements were almost perfectly compensatory
for both paradigms. In subjects with UVD, VOR gain for ipsilesional head thrusts
was low for both paradigms, but significantly (P<.001) higher
(less abnormal) for HART (0.60 ± 0.13) than for HTT (0.14 ±
0.13). Contralesional gain was reduced for both, to 0.64 ± 0.20 for
HART and to 0.57 ± 0.17 for HTT. Because ipsilesional and contralesional
gains were not statistically different for HART (P
= .69), comparison of VOR gains for half-cycle responses to the HART stimulus
could not reliably identify the side of the known lesion. In contrast, HTT
consistently identified the side of the lesion for all subjects with UVD.
To investigate whether preprogramming contributes to the boost in VOR as measured
by HART, we compared the gain and response delay of eye movements during actively
self-generated and passively received head thrusts. For subjects without UVD,
response delays were shorter for active (6 ± 1 milliseconds) than for
passive (12 ± 1 milliseconds) HTT. For ipsilesional rotations of subjects
with UVD, active HTT yielded a significantly higher gain (0.44 ± 0.20)
(P<.001) and a shorter delay (15 ± 6 milliseconds)
(P<.001) than did passive HTT (0.14 ± 0.13
and 37 ± 15 milliseconds, respectively). Contralesional test results
revealed a similar performance boost for active head movements. Data are given
as mean ± SD.
Conclusion When comparison of half-cycle gains is used to identify the lesion side,
self-generated predictable head movement paradigms, such as HART and active
HTT, are less accurate than passive HTT in the characterization of UVD, in
part because preprogramming can augment the VOR during voluntary head movements.
INTRODUCTION
DIZZINESS IS the ninth most common reason adults visit a primary care
physician, and it affects approximately 90 million Americans.1-4
Identification of the side, affected semicircular canals, and degree of unilateral
vestibular deficiency (UVD) is an important goal in the examination of patients
experiencing dizziness.
Two high-frequency rotational stimulus paradigms—the head thrust
test (HTT) and the head autorotation test (HART)—are in wide use for
assessing angular vestibulo-ocular reflex (VOR) function, yet have not been
directly compared.
Researchers5-8
have advocated HTT, in which high-acceleration impulsive head rotations are
delivered in the plane of one pair of semicircular canals while a subject
attempts to maintain visual fixation on a distant target. Implied by the second
law of Ewald,9 such head rotations elicit an
asymmetric response in patients with UVD by maximally stimulating the neural
pathway arising from one semicircular canal crista while maximally inhibiting
or silencing the pathway from the coplanar canal. The approach has proved
sensitive for the detection of vestibular dysfunction in subjects with known
UVD.6, 10
A second paradigm, HART, uses self-generated, swept-frequency, sinusoidal
head rotations performed while the subject visually fixates a distant earth-fixed
target. Fourier analysis of system gain and phase, along with formulaic measures
of response asymmetry, are applied to the measured head and eye movements.
Researchers11-16
have reported extensively on this approach, and several commercially available
vestibular testing systems are based on this paradigm.
We sought to compare the ability of HTT with that of HART to identify
dysfunction in subjects with known UVD after surgical labyrinthectomy. There
are 3 differences between these 2 stimulus paradigms that could contribute
to a difference in measured VOR for a given patient. First, HTT stimuli are
passive (ie, delivered by the examiner), while during HART, the head movement
is active (ie, self-generated). Second, HTT stimuli are presented unpredictably
in time and direction, while the sinusoidal frequency–sweep head movement
during HART is predictable cycle by cycle. Third, HTT stimuli are often of
higher acceleration and wider spectral bandwidth than are HART stimuli, because
of some subjects' inability to make rapid, self-generated, sinusoidal head
movements.
We hypothesized that during active predictable head movements, subjects
with UVD can augment apparent VOR performance by using information about the
intended/expected head movement to complement deficient vestibular function
and guide compensatory eye movements. Such an effect would be expected to
reduce the sensitivity of tests like HART that rely on self-generated head
movement stimuli for detecting vestibular hypofunction. We tested these predictions
by comparing VOR gains measured for subjects with and without UVD during HART
and HTT, and by comparing subjects' responses to active and passive impulsive
head rotations.
METHODS
SUBJECTS
We studied 5 human subjects without UVD and 11 with UVD due to labyrinthectomy.
Subjects without UVD ranged in age from 32 to 55 years and were free of vestibular
and ocular disease, except for wearing corrective lenses. Subjects with UVD
ranged in age from 48 to 72 years, and the time from labyrinthectomy ranged
from 3 to 120 months. All had undergone vestibular rehabilitation therapy
postoperatively. The indication for labyrinthectomy was vestibular schwannoma
or meningioma in 6 subjects and unilateral Meniere disease in 5. The side
of labyrinthectomy was the left for 6 subjects with UVD and the right for
5. All subjects gave written informed consent, and the experimental procedures
were approved by the Joint Committee on Clinical Investigation, The Johns
Hopkins University School of Medicine, Baltimore, Md.
EXPERIMENTAL TECHNIQUE
Head and eye movements were recorded in 3 dimensions using magnetic
search coils embedded in contact lenses and in a bite block. The instrumentation
and technique have been described in detail elsewhere.17
Eye and bite block angular positions were sampled at 500 Hz. The resulting
signals were low-pass filtered with a single-pole analog filter with a 3-dB
bandwidth of 100 Hz. Each subject was tested while seated upright and centered
within a uniform magnetic field, with the interpupillary line parallel to
the horizon and the Frankfort line (from the top of the tragus to the infraorbital
foramen) in the plane of head rotation. All rotational stimuli were in the
horizontal (yaw) plane. During each trial, the room was completely dark except
for a target light-emitting diode positioned 1.24 m anterior to the center
of the head, at the same elevation as the pupils. All subjects were tested
more than 20 minutes after removal of eyeglasses.
Each experiment began with the subject's head held rigidly at the starting
position via connection of the bite block to a bar, while the subject performed
calibration tasks. The bar was then removed, and all subsequent trials were
performed with the head free to move during a stimulus, then returning to
the starting position.
For HART, subjects attempted to visually fixate the target while sinusoidally
shaking their heads horizontally (ie, rotating about an earth-vertical axis
through the center of the cervical spine) at maximum tolerated velocity in
time with a metronome swept logarithmically in frequency from 1 to 6 Hz for
20 seconds. Results from 3 trials were averaged.
For HTT, subjects fixated the same target during brief (100-200–millisecond)
rotations in the earth-horizontal plane, at high acceleration (3000°-5000°/s2) starting from a complete stop. Head velocity reached 25° to 75°/s
at 40 milliseconds into the movement and 150° to 300°/s peak velocity
by 100 to 120 milliseconds. The final position was 10° to 15° from
center. For passive HTT (pHTT), stimuli were delivered manually at an unpredictable
onset time and in a randomly varied direction, starting from center. The subject
received no cues about the direction or time of an impending passive head
thrust. For active HTT (aHTT), the subject generated the head thrust voluntarily.
Only head movements reaching greater than 100°/s within the first 60 milliseconds
were included in the analysis. A typical trial lasted about 3 minutes and
included about 20 to 40 head thrusts to each side.
ANALYSIS
To facilitate comparison between eye and head angular velocities, both
were analyzed in 3 dimensions in the head frame of reference. Horizontal rotational
components were extracted and compared.18 All
results reported are for the horizontal components of rotation only. Angular
velocity and acceleration were computed from angular position signals using
a 30-Hz, band-limited, 10-element, linear phase differentiating digital filter
designed using computer software (MATLAB; The Mathworks, Inc, Cambridge, Mass)
and applied in zero-delay fashion.
We quantified the eye movement responses in terms of velocity gain and
response delay. Gain was defined as the angular velocity of the eye divided
by the angular velocity of the head at the instant head velocity crossed to
above 120°/s, with the eye velocity inverted so that a gain of +1.0 denotes
an ideal compensatory response. Using the method of Tabak et al,7
we defined response delay as the time between the onsets of head and eye movements,
where onset was defined as the time at which velocity crossed a threshold
set at 2°/s plus 8 times the root-mean-square velocity in the 100 milliseconds
preceding the stimulus.8 We used 1- or 2-tailed t tests to compare gain and response delay distributions
between experimental groups, with P<.05 considered
significant. Data are given as mean ± SD unless otherwise indicated.
RESULTS
HEAD AUTOROTATION TESTING
Figure 1 shows HART results
for a healthy 33-year-old man without UVD. In the trial shown, head velocity
ranged from 40°/s at 1 Hz to approximately 180°/s at 6 to 8 Hz (Figure 1A). Eye velocity traces (inverted
for comparison with head velocity) are nearly identical to head velocity traces,
to within less than the 4°/s of retinal image slip for which visual acuity
begins to degrade (Figure 1B).19 When plotted as eye velocity vs head velocity, these
data lie almost exactly along a y = -x line, consistent with a nearly perfect VOR (Figure 1C). This subject without UVD has
rightward and leftward VOR velocity gains of 1.0 ± 0.05 and 1.0 ±
0.02, respectively.
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Figure 1. Horizontal head autorotation test
results of a 33-year-old man without a unilateral vestibular deficiency. A,
Head and eye velocity vs time, with the eye trace inverted for comparison
with the head trace. (All similar figures use the same convention.) The eye
velocity trace overlies the head trace almost exactly. In the trial shown,
head velocity ranged from 40°/s at 1 Hz to 180°/s at 6 to 8 Hz. B,
Expanded view of a portion of the trial. Eye velocity traces are nearly identical
to head velocity traces. C, Eye velocity vs head velocity after removal of
saccades. Data lie almost exactly along a y = -x line, consistent with a nearly perfect vestibulo-ocular reflex.
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Figure 2 shows HART results
for a symptomatically well-compensated 63-year-old man who had undergone right
translabyrinthine vestibular schwannoma resection and postoperative vestibular
rehabilitation 5 months before testing. For this subject, the response during
head turns toward the contralesional left side (Figure 2A and B) is somewhat degraded, but not significantly (P = .07) different from normal (gain, 0.87 ± 0.13).
During rightward head turns, there is a significantly (P<.001) abnormal response, with a velocity gain of 0.43 ±
0.19 and retinal slip errors of up to 100°/s. Retinal slip not only degrades
foveal visual acuity but also accrues to cause the subject to lose target
fixation, eliciting large saccadelike corrective eye movements to reacquire
the visual target. For this subject, HART results clearly reveal an asymmetry.
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Figure 2. Head autorotation test results
of a 63-year-old man 5 months after right translabyrinthine vestibular schwannoma
resection. A, Head and eye (inverted) velocity vs time. B, Expanded view of
a portion of the trial. C, Eye velocity vs head velocity. Contralesional (leftward)
head turns elicit a moderately degraded response, with a gain of 0.87 ±
0.13 (mean ± SD). Ipsilesional responses are more abnormal, with decreased
velocity gain, increased retinal slip errors of up to 100°/s, and large-amplitude
saccadelike catch-up eye movements.
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Such asymmetries between responses to ipsilesional and contralesional
head rotations were not always apparent. Figure 3 presents the HART responses from a 68-year-old man tested
38 months after undergoing surgery resulting in left UVD. At maximum effort,
this patient achieved slower peak head velocity than the subject shown in Figure 2. The slow-phase components of the
response to ipsilesional rotations were not markedly different from those
observed in the contralesional half cycles. However, a gaze-correcting saccadic
eye movement was often observed in the ipsilesional responses.
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Figure 3. Head autorotation test results
of a 68-year-old man 38 months after surgery for a left unilateral vestibular
deficiency. A, Head and eye (inverted) velocity vs time. B, Expanded view
of a portion of the trial. C, Eye velocity vs head velocity after saccade
removal. Saccadelike catch-up eye movements are directed toward the lesion
side, but slow-phase eye movements show little asymmetry.
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Figure 4A and B shows a summary
of VOR gains measured using HART in 5 healthy subjects and in 11 subjects
with UVD, respectively. The VOR gains for subjects without UVD are segregated
into rightward and leftward head movements and illustrated separately as a
check of test reliability. The VOR gains for subjects without UVD are 0.95
± 0.13 and 1.03 ± 0.11 for rightward and leftward head rotations,
respectively. There was no significant difference between right and left VOR
gains (P = .13), and the combined data set was insignificantly
different from 1.0 (P = .64) (95% confidence interval,
0.93-1.05). The HART gains for subjects with UVD were segregated into ipsilesional
and contralesional directions. Four findings were notable. First, the ipsilesional
gain of 0.60 ± 0.13 was significantly lower than normal (P<.001). Second, there was a wide distribution of ipsilesional gains
for this sample population, ranging from 0.2 to 1.0. Third, the contralesional
gain of 0.64 ± 0.20 was also significantly decreased from normal (P<.001). Finally, HART gains were not significantly
different for ipsilesional and contralesional rotations in these subjects
with UVD and, therefore, could not reliably indicate the side of the known
lesion (P = .69).
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Figure 4. The head autorotation test (HART)
gains measured in 5 healthy subjects (A) and in 11 subjects with unilateral
vestibular deficiency (UVD) (B) are shown. A, The mean vestibulo-ocular reflex
(VOR) gain for subjects without UVD is not significantly (P =
.64) different from 1.0 for rightward and leftward head rotations. B, For
this population of subjects with UVD, ipsilesional and contralesional HART
gain distributions were not significantly different from each other (P = .69). The VOR gains for passive head thrust test (pHTT)
in 4 subjects without UVD (C) and in 11 subjects with UVD (D) are also shown.
C, Right and left pHTT gains of subjects without UVD are close to 1.0 and
not significantly different from each other (P =
.27). D, The gains of subjects with UVD were decreased for ipsilesional and
contralesional head rotations, with a marked asymmetry between ipsilesional
and contralesional gains for every patient tested. For A and C, the key provides
subject age (in years)/sex (M indicates male; F, female); for B and D, subject
age (in years)/sex/side (R indicates right; L, left)/time since labyrinthectomy
(in months). Bars represent mean ± SD.
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PASSIVE HTT
Passive HTT was performed on 4 of the subjects without UVD and on all
11 subjects with UVD who had been studied using HART. Figure 5A shows head velocity and concurrent eye velocity traces
for 2 representative head thrusts from the same subject without UVD who was
described in Figure 1. The high-acceleration
head rotation transients reach a peak velocity of greater than 200°/s
within 80 to 100 milliseconds and are tracked accurately by compensatory eye
movements, with a slight overshoot following the peak of head velocity. Figure 5B shows multiple head thrust stimuli
and the corresponding eye movement responses for the first 80 milliseconds
of each. Peak head accelerations ranged from approximately 3000° to 5000°/s2. Although there is a slight early mismatch of eye and head traces
because of VOR latency, retinal slip is kept below 5°/s throughout most
of each trace. In Figure 5C, a plot
of eye velocity vs head velocity reveals that all traces lie close to a y = -x line, corresponding
to nearly perfect performance. Rightward and leftward gains for this subject
were 1.00 ± 0.04 and 0.99 ± 0.06, respectively. Subjects without
UVD never complained of losing sight of the target during testing.
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Figure 5. Passive head thrust test results
for a healthy subject without a unilateral vestibular deficiency (UVD) (same
subject as in Figure 1). A, Head and eye (inverted) velocities during passive
head thrusts to the right, then to the left (after returning to center [not
shown]). This subject has nearly perfect overlap of head and eye traces. B,
Head and eye (inverted) velocities during the first 80 milliseconds of multiple
passive head thrust trials. Traces nearly overlie each other for this subject
without UVD. C, Eye velocity vs head velocity. Data lie closely along a y = -x line, consistent with a near-perfect
vestibulo-ocular reflex.
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In contrast, Figure 6 shows
pHTT responses for the 68-year-old man with left UVD for whom HART data were
described in Figure 3. In Figure 6A, a rightward head thrust is tracked
fairly well by the eye, although the VOR gain is less than normal and a small
catch-up saccadelike movement is required to correct the final eye position
after the head movement ends. For a leftward head thrust, the VOR response
decrease is more pronounced, as are the prominent catch-up eye movements.
The second and third catch-up movements occur after the head stops moving;
these are the corrective eye movements an observer can detect when using HTT
as part of the physical examination. Figure
6B shows the first 80 milliseconds of multiple stimuli for this
subject. For rightward head rotations, the eye tracks the head fairly well;
however, the initial VOR-mediated eye movement response for leftward head
thrusts is of low amplitude. Figure 6C
reveals an asymmetry in the eye movement responses to contralesional and ipsilesional
head thrusts, corresponding to the measured VOR gains of 0.50 ± 0.15
and 0.06 ± 0.09, respectively.
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Figure 6. Passive head thrust test results
in a subject with a unilateral vestibular deficiency (UVD) (same subject as
in Figure 3). A, Head and eye (inverted) velocities during passive head thrusts
to the right, then to the left (after returning to center [not shown]). This
subject with a left UVD follows rightward head movement moderately well, but
tracks leftward head thrusts poorly. B, Head and eye (inverted) velocities
during the first 80 milliseconds of multiple passive head thrust trials. Response
is delayed and of decreased magnitude, mildly for rightward head movements
and dramatically for head movements toward the lesion side. C, Eye velocity
vs head velocity for the first 80 milliseconds of responses.
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Figure 4C and D shows a summary
of pHTT VOR gains for 4 subjects without UVD and 11 subjects with UVD, respectively.
(The same subjects were used for pHTT and HART, except for 1 subject without
UVD who was tested only with HART.) Right and left pHTT responses of subjects
without UVD are shown separately in Figure
4C. Rightward (0.94 ± 0.04) and leftward (0.90 ± 0.05)
pHTT gains were not significantly different (P =
.27) for subjects without UVD. For subjects with UVD (Figure 4D), gains were decreased for ipsilesional and contralesional
head rotations. In contrast to the HART VOR gains for the same population
of subjects, there was a marked asymmetry between ipsilesional (0.14 ±
0.13) and contralesional (0.58 ± 0.17) gains. For every patient with
UVD tested, ipsilateral gains were significantly lower than contralesional
gains (P<.001). Ipsilesional and contralesional
gains were each significantly different from normal (P<.001).
Comparison of HART and pHTT results reveals that although the ipsilateral
VOR gains are reduced for the HART paradigm applied to subjects with UVD,
a similar reduction in contralesional gains was such that HART could not reliably
distinguish the side of the known lesion. In contrast, there was a marked
and consistent asymmetry in the VOR gains of subjects with UVD measured using
the pHTT paradigm, with the ipsilateral gains close to 0 and the contralesional
gains close to gains measured using HART.
aHTT VS pHTT
Gain
To better identify why the VOR is apparently enhanced when measured
by the HART paradigm, we compared VOR gains measured in subjects with and
without UVD using head thrusts that were either passively and unpredictably
received by the subjects as in the usual application of the test (pHTT) or
actively generated by the subjects (aHTT). Analysis was limited to active
and passive head movements that were similar in mean peak velocity, peak acceleration,
and spectral content.
Figure 7 shows the first 80
milliseconds of head movements and corresponding eye movement responses to
aHTT for the subject with left UVD shown in Figure 3 and Figure 6.
Whereas the ipsilesional pHTT response was essentially nonexistent for the
first 80 milliseconds after stimulus onset (Figure 6B), the aHTT response VOR gain is enhanced, to 0.34 ±
0.06, from 0.06 ± 0.09 (Figure 7A).
The contralesional VOR gain is also increased, to 0.74 ± 0.05, from
0.50 ± 0.15. Similarly, the time from stimulus onset to threshold response
is shorter for aHTT than for pHTT.
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Figure 7. Active head thrust test results
in a subject with a left unilateral vestibular deficiency (same subject for
whom passive data are shown in Figure 6). A, Head and eye (inverted) velocities
during the first 80 milliseconds of multiple active head thrust trials. B,
Eye velocity vs head velocity. Although still not normal, the active eye movement
response is significantly better than for passive trials, with shorter response
delay and higher gains.
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Figure 8 shows pHTT and aHTT
VOR gains for 3 subjects without UVD and 10 subjects with UVD (the same subjects
used for HART except for those who did not generate aHTT head movements similar
to those of pHTT). For subjects without UVD (Figure 8A), responses to aHTT and pHTT were not significantly different
from each other or from 1.00 (P>.05 for all). For
subjects with UVD, there was a significant (P<.001)
increase in apparent ipsilesional VOR gain when measured using the aHTT paradigm,
to 0.44 ± 0.20 (from 0.14 ± 0.13 for pHTT) (Figure 8B). The contralesional VOR gain also increased significantly
(P = .004) under aHTT conditions, to 0.81 ±
0.14 (from 0.58 ± 0.17 for pHTT) (Figure 8C). This level was not significantly different from the
VOR gains measured in subjects without UVD using pHTT (P = .08).
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Figure 8. The vestibulo-ocular reflex (VOR)
gains for passive and active head thrust test (HTT) of 3 subjects without
unilateral vestibular deficiency (UVD) (A) and 10 subjects with UVD (B and
C). The keys in Figure 4 provide characteristics of each subject. In A, lowercase
letters indicate leftward thrusts; uppercase letters, rightward thrusts. For
healthy subjects without UVD, responses to active and passive HTT were not
significantly different from each other or from 1.00 (P>.05 for
all). In B, active HTT ipsilesional VOR gain is significantly (P<.001) higher than for passive HTT. In C, contralesional UVD VOR
gain is also significantly (P = .004) closer to normal
for active than for passive HTT. Bars represent mean ± SD.
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Response Delay
To obtain a measure of response timing, we used the method of Tabak
et al8 to define stimulus and response onset
and to compute a response delay. Figure 9 shows pHTT and aHTT VOR response delays for 4 subjects without
UVD and 11 subjects with UVD. For subjects without UVD (Figure 9A), the response delay was 11.0 ± 3.3 milliseconds
for pHTT and slightly, but significantly, lower at 5.0 ± 1.8 milliseconds
for aHTT (P = .006). For subjects with UVD, the response
delay for ipsilesional head thrusts was significantly shorter for aHTT (19
± 16 milliseconds) than for pHTT (42 ± 17 milliseconds) (P = .006) (Figure 9B). The response delay in subjects with UVD for contralesional head thrusts was
also shorter for aHTT (11.0 ± 5.1 milliseconds) than for pHTT (15.0
± 4.5 milliseconds), but the difference was not significant (P = .07) (Figure 9C).
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Figure 9. The response delays for passive
and active head thrust test (HTT) of 3 subjects without unilateral vestibular
deficiency (UVD) (A) and 10 subjects with UVD (B and C). The keys in Figure
4 provide characteristics of each subject. In A, lowercase letters indicate
leftward thrusts; uppercase letters, rightward thrusts. For subjects without
UVD, the response delay was shorter for active than for passive HTT (P = .006. In B, for ipsilesional stimuli, response delay was significantly
shorter for active HTT than for passive HTT (P =
.006). In C, the response delay for contralesional stimuli was not significantly
different (P = .07) between passive and active HTT.
Bars represent mean ± SD.
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COMMENT
CLINICAL TESTS FOR IDENTIFICATION OF UVD
Traditional caloric and rotary chair tests for the identification of
UVD fail to test the vestibular system using physiologically appropriate stimuli
over the range of frequencies and accelerations for which the system apparently
evolved. Caloric testing has the advantage of being strictly unilateral, but
uses an unnatural stimulus (a thermal gradient) that, as measured by the eye
movements it elicits, is the equivalent of a low frequency (0.025 Hz) and
low amplitude (approximately 50°/s) head rotation. The caloric response
can be altered by anatomic changes in the external ear canal and by individual
variation in temporal bone anatomic features, and it only evaluates 1 of the
5 vestibular receptors (the lateral semicircular canal). Rotary chair vestibular
testing is more physiologic; however, at the lower frequencies and velocities
typically used in clinical vestibular laboratories, rotary chair tests are
insensitive in the identification of chronic total unilateral vestibular hypofunction.20-21 The sensitivity of rotary chair testing
can be improved by comparison of responses to steps of acceleration with the
head up and head down.22
In contrast, high-frequency and high-acceleration rotational stimuli
unmask the inherent asymmetry in the vestibular system, as described by the
second law of Ewald9—that the excitatory
responses of vestibular pathway neurons encode motion over a larger dynamic
range than do inhibitory responses. The eye movements elicited by such stimuli
are principally due to excitation of the vestibular pathway arising from the
canal ipsilateral to the direction of head acceleration and are, therefore,
sensitive to a unilateral peripheral vestibular loss in that canal.
There are 2 high-frequency rotational stimuli in clinical use, pHTT
and HART. The main objective of this study was to compare these 2 stimuli
for the identification of unilateral vestibular hypofunction. The pHTT is
a single, passive (operator delivered), unpredictable, high-acceleration (2000°-4000°/s2), low amplitude (15°-30°) head rotation in the direction of
a single semicircular canal. The HART is a continuous, active (self-generated),
sinusoidal head rotation that begins slowly and becomes faster, covering a
frequency range of about 1 to 6 Hz. During each test, subjects are required
to fixate a visual target in front of them, and their ability to maintain
visual fixation is accepted as a measure of VOR function. However, because
HART is actively generated, non-VOR processes, such as predictive eye movements
driven by an "efference copy" neural representation of the intended head movement,
could contribute to maintaining gaze stability. As a result, VOR function
could seem artificially enhanced, making HART a less sensitive and less accurate
test of UVD.
We tested 11 patients who had undergone surgical labyrinthectomy and
compared their responses with those of 5 subjects without UVD. The VOR gains
for subjects without UVD using pHTT were insignificantly different from an
ideal gain of 1.0, consistent with findings from previous studies.23 For subjects with UVD, the VOR gains of 0.14 ±
0.13 for ipsilesional head thrusts and 0.58 ± 0.17 for contralesional
head thrusts were significantly different, and the side with the lesion was
clearly identified by pHTT in each patient, consistent with previous studies.6, 24 For HART, the VOR gain in subjects
without UVD was essentially perfect, as one would expect. Surprisingly, however,
although some subjects with UVD showed obvious asymmetry of VOR half-cycle
gains on HART, there was no significant difference between the ipsilesional
and contralesional VOR gains over the population with UVD (P = .69).
Other features of the response to the actively generated HART stimulus
did provide an indication of the side of unilateral vestibular hypofunction.
The occurrence of rapid, gaze-correcting, saccadic eye movements during head
movements toward the side of the lesion, when they occur, is a reliable indication
of the side of UVD. A bias velocity in the eye movement response during the
HART stimulus (a direct current shift in the eye velocity trace toward the
side of the lesion) provides another such indication. Head autorotation is,
therefore, a useful paradigm, but comparison of VOR gains from half-cycle
analysis of HART responses is not reliable for the identification of the side
of UVD.
MECHANISMS FOR IMPROVED RESPONSES TO ACTIVE HEAD ROTATIONS
There are 2 main differences between HART and pHTT stimuli that might
explain the improvement in VOR gain of patients with UVD for ipsilesional
head movements during HART. First, the peak velocities and accelerations generated
by the examiner in pHTT are greater than those that some patients are able
to generate during HART. This constraint on stimulus intensity may limit HART's
ability to discern unilateral weakness in such patients. In contrast, the
stimulus used for pHTT is generated by the examiner and reaches a peak acceleration
of 3000°/s2 and a peak velocity of 250°/s. Although these
head movements have low amplitude in displacement (10°-15°) and are
well tolerated by patients, they are sufficient to elicit excitation-inhibition
asymmetry and, thus, selectively probe the function of the excited canal.
A second difference is that the pHTT is passive, transient, and unpredictable,
whereas the HART is a self-generated, sinusoidal, predictable stimulus. Self-generated,
sinusoidal, steady-state rotations could allow for nonvestibular eye movement
systems (eg, predictive eye movements, efference copy, and visual-following
mechanisms) to contribute to the response. The existence of predictive mechanisms
in augmenting vestibular responses is suggested by measures of visual acuity
during head movement. Visual acuity is improved during active compared with
passive head movements.25-26 To
further investigate these potential effects of self-generated stimuli, we
asked patients to perform the HTT themselves, aiming to mimic the speed and
amplitude of the operator-delivered head thrusts. Although patients had some
difficulty reaching the top speed of operator-delivered stimuli (about 300°/s),
they did reach speeds of approximately 200°/s, and we compared responses
for active and passive head thrusts of similar peak velocity and acceleration.
In subjects without UVD, the VOR gain was already insignificantly different
from 1.00 for pHTT, so no significant change was observed for aHTT. For subjects
with UVD, however, there was a marked improvement in VOR gain during active
head movements, and the boost in VOR gain during active thrusts occurred from
the onset of the head thrust, during the initial 20 to 40 milliseconds. The
only 2 oculomotor systems with a latency of less than 40 milliseconds are
the direct VOR and predictive eye movements. Saccades, the cervico-ocular
reflex, and visual-following mechanisms, such as smooth pursuit, all have
latencies that are 70 to 150 milliseconds.27
From previous studies,6, 10 it
has been shown that the 3-neuron VOR arc generates the response to pHTT, so
the boost in gain during aHTT is, therefore, likely to be a result of predictive
eye movements.
To study the effect of prediction, we measured the time between the
onset of head rotation and the onset of eye rotation for active and passive
head thrusts. We used manually applied passive head thrusts to approximate
the usual clinical application of pHTT and the movements our subjects made
during aHTT. Manual thrusts do not have an onset sharp enough or an acceleration
constant enough to precisely measure VOR latency (estimated at 8.6 milliseconds
in subjects without UVD by Collewijn and co-workers28-29
using a torque-applying helmet in an HTT-type paradigm). To obtain a measure
of response timing, we used the method of Tabak et al8
to define stimulus and response onset times (at which head and eye velocities
cross set thresholds) and compute a response delay. This response delay probably
does not precisely equal the true synaptic and axonal conduction delay of
the VOR, because the finite rate of change of acceleration for manually applied
stimuli and responses reduces the precision with which onset times for head
and eye movements can be measured. However, this response delay provides a
useful measure for comparison of responses to passive and active head thrusts.
For subjects without UVD, the response delay was shorter for active
than for passive head thrusts. For subjects with UVD, the response delay during
ipsilesional head thrusts was significantly longer for passive thrusts than
for active thrusts. A similarly prolonged response delay for passive ipsilesional
head rotations has been reported by Tabak et al.8
The apparent reduction in the response delay to aHTT might be further evidence
of preprogrammed eye rotation. Alternatively, some of the apparent difference
in response delay may be due to a difference in VOR gain for the first 40
milliseconds of the response. The initial low velocity eye rotation makes
it difficult to precisely define the onset of the eye rotation, and could
give the appearance of a delayed onset.
TIMING OF CORRECTIVE EYE MOVEMENTS
Further evidence for preprogramming of eye rotations during active head
thrusts was the reduced latency of rapid corrective eye movements during active
compared with passive head thrusts. To compensate for a deficient VOR, patients
with UVD used rapid eye movements to correct accrued gaze error and reacquire
visual fixation of the target. During active head thrusts, these corrective
movements occurred as early as 60 milliseconds after the onset of the head
rotation, significantly earlier than during passive head thrusts (Figure 10). Under normal circumstances,
the latency of voluntary true saccadic eye movements is 200 milliseconds.25 This latency can be reduced to 100 milliseconds if
the subject is trained in a specific task (so-called express saccades30). Tian et al25 have
shown that under pHTT conditions, these rapid eye movements have latencies
shorter than those of express saccades. Our data indicate that these latencies
can be reduced even further under conditions of active head movement.
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Figure 10. Corrective rapid eye movements
during passive (A) and active (B) ipsilesional head thrust testing (HTT) in
a 48-year-old subject with a unilateral vestibular deficiency 120 months after
left labyrinthectomy (subject R shown in Figure 4, Figure 8, and Figure 9).
Head and eye (inverted) velocities are shown. The response to active HTT has
a higher initial vestibulo-ocular reflex gain (arrows) and earlier rapid compensatory
eye movements (dashed lines).
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CONCLUSIONS
Gain asymmetries on the pHTT reliably detected the presence of known
unilateral vestibular lesions in all patients with UVD tested, whereas the
half-cycle gains measured from HART did not. Relative to pHTT, HART gains
overestimated ipsilesional vestibular function and were, therefore, a less
accurate indicator of unilateral hypofunction.
For subjects with UVD who are unable to generate high-acceleration sinusoidal
head movements, HART may underestimate hypofunction simply because it relies
on stimulus accelerations inadequate to silence inhibitory pathways arising
in the intact ear. In contrast, the high-acceleration movements of pHTT reliably
identify response asymmetry by more selectively probing the function of the
excited canal. However, even for head movements of similar acceleration and
time course, the measured VOR during self-generated head rotations (aHTT)
has significantly higher gain and shorter response delay than does the VOR
to passive unpredictable stimuli (pHTT).
Subjects with UVD may use a variety of strategies for improving visual
fixation, including preprogrammed eye movements designed to augment the deficient
VOR and to compensate for a planned or anticipated head movement. Tests using
passive high-acceleration head thrusts delivered unpredictably in time and
direction should, therefore, be more sensitive for discerning VOR hypofunction
than tests using active and/or predictable stimuli.
AUTHOR INFORMATION
Accepted for publication February 18, 2002.
This study was supported by the Garnett Passe and Rodney Williams Memorial
Foundation, Parkville, Australia (Dr Cremer); the Royal Australasian College
of Physicians, Sydney, New South Wales (Dr Cremer); grants K23 DC00196 (Dr
Carey) and R01 DC02390 (Dr Minor) from the National Institutes of Health,
Bethesda, Md; and a Johns Hopkins Clinician-Scientist Award (Dr Carey).
We thank Grace C. Y. Peng, PhD, David S. Zee, MD, Adrian G. Lasker,
MS, and Dale C. Roberts, MS, for their assistance with data acquisition; and
John K. Niparko, MD, and Howard W. Francis, MD, for their referral of subjects.
Corresponding author and reprints: Lloyd B. Minor, MD, Department
of Otolaryngology–Head & Neck Surgery, The Johns Hopkins Medical
Institutions, 601 N Caroline St, Baltimore, MD 21287-0910 (e-mail: lminor{at}bme.jhu.edu).
From the Department of Otolaryngology–Head & Neck Surgery,
The Johns Hopkins Medical Institutions, Baltimore, Md (Drs Della Santina,
Carey, and Minor); and the Eye and Ear Research Unit, Institute of Clinical
Neurosciences, Royal Prince Alfred Hospital, Sydney, Australia (Dr Cremer).
REFERENCES
1. Hoffman RM, Einstadter D, Kroenke K. Evaluating dizziness. Am J Med. 1999;107:468-478.
FULL TEXT
| PUBMED
2. Kroenke K, Arrington ME, Manglesdorff AD. The prevalence of symptoms in medical outpatients and the adequacy
of therapy. Arch Intern Med. 1990;150:1685-1689.
ABSTRACT
3. Cypress BK. Patterns of ambulatory care in internal medicine: the National Ambulatory
Medical Care Survey. Vital Health Stat 13. 1984;(80):1-69.
4. Kroenke K, Hoffman R, Einstadter D. How common are various causes of dizziness? a critical review. South Med J. 2000;93:160-167. |
