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Role of Central Preprogramming in Dynamic Visual Acuity With Vestibular Loss
Susan J. Herdman, PT, PhD;
Michael C. Schubert, PT, MS;
Ronald J. Tusa, MD, PhD
Arch Otolaryngol Head Neck Surg. 2001;127:1205-1210.
ABSTRACT
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Objective To determine the contribution of central preprogramming of eye movements
to dynamic visual acuity (DVA) during head movement in patients with vestibular
hypofunction.
Study Design Prospective, clinical study.
Setting Tertiary care, academic hospitals.
Participants Twenty-six healthy subjects and 20 patients with unilateral (UVL) and
7 with bilateral vestibular loss (BVL) (age range, 20-86 years).
Interventions Diagnostic interventions, including caloric and rotational chair testing.
Main Outcome Measure Measurements of DVA during predictable (DVA-predictable) and unpredictable
(DVA-unpredictable) head movements using a computerized test.
Results There was a difference between DVA-predictable and DVA-unpredictable
scores in all groups (P<.02). The difference between
DVA-predictable and DVA-unpredictable scores for the BVL group was significantly
greater than that for the other groups (P<.005).
Age was a significant factor in DVA-unpredictable scores for the healthy subjects
(P<.001) and UVL group (P<.02).
Comparisons of DVA between groups were significant (P<.03),
with the following exceptions: UVL group for head movements toward the unaffected
side for DVA-predictable and DVA-unpredictable scores, compared with healthy
subjects, and UVL group for head movements toward the affected side for DVA-predictable
scores, compared with the BVL group.
Conclusions Unpredictable head movements cause a greater decrement in visual acuity
than do predictable head movements. This suggests that central programming
of eye movements and/or efference copy contributes to gaze stability during
predictable head movements in healthy subjects and patients with vestibular
hypofunction. Patients with BVL use central programming of eye movements to
maintain gaze stability more than do healthy subjects or patients with UVL.
INTRODUCTION
MOVEMENT of the head can cause significant retinal slip. When retinal
slip exceeds 2°/s, degradation of visual acuity occurs.1-3
Various mechanisms that may augment the vestibulo-ocular reflex (VOR) include
the pursuit/optokinetic system, the cervico-ocular reflex (COR), efference
copy, central programming of eye movements, and anticipatory intent.4-11
The contribution of these mechanisms to gaze stability was studied primarily
by comparing the gain of the compensatory eye movements during active and
passive head movements in which the direction, amplitude, and temporal quality
of head movement were predictable.3, 6, 12-14
Other studies have shown that there is little difference of the gain of the
VOR in the light (visual-VOR) under conditions in which the active and passive
head movements are predictable.3, 15
We chose to examine the role of central programming of eye movements
and efference copy in maintaining gaze stability using a functional measure,
ie, dynamic visual acuity (DVA). We examined the ability of these compensatory
mechanisms to augment the VOR by comparing visual acuity during predictable
(active) and unpredictable (passive) head rotation. We hypothesized the following:
(1) visual acuity during head rotations in which the direction and timing
of the head movement was unpredictable (DVA-unpredictable) would be significantly
worse than visual acuity when the head movement was predictable (DVA-predictable)
for healthy subjects, patients with unilateral vestibular loss (UVL), and
patients with bilateral vestibular loss (BVL); (2) patients with BVL would
have a significantly greater decrement in DVA-unpredictable scores compared
with all other groups; and (3) age would be a factor in DVA-unpredictable
scores as it was for DVA-predictable scores.16
SUBJECTS AND METHODS
SUBJECTS
Healthy subjects were recruited from among laboratory personnel and
family members of patients at 2 tertiary care academic hospitals. Informed
consent was obtained in compliance with the institutional review board protocols
of the University of Miami, Miami, Fla, and Emory University, Atlanta, Ga.
Patients included in the study had been referred to the laboratory for assessment
from the clinical practice of 2 of the investigators (S.J.H. and R.J.T.).
Vestibular function was assessed in these subjects using caloric and vertical-axis
rotational chair tests.17-18 Subjects
were excluded from the healthy group if they had abnormal results of vestibular
function tests or a history of vertigo. Bilateral and unilateral vestibular
deficits were identified based on the clinical evidence of an abnormal vestibular
response (positive findings of the head-thrust test)19
and the results of vestibular testing (rotational chair or caloric tests).17-18 For the head-thrust test, the patient's
head was first pitched forward approximately 30°, and the patient was
asked to fixate on a stationary target. The patient's head was moved through
a small amplitude, first slowly and then rapidly, in the yaw plane. The direction
of the rapid head impulses was randomized to be unpredictable. Patients underwent
testing using a near and a far target with appropriate visual correction.
When the head thrust resulted in a corrective saccade to refixate the target,
the test result was considered positive for the side of the head thrust (indicating
vestibular hypofunction). We used step-velocity rotational chair testing at
rotations of 60°/s and 240°/s with electronystagmography. Unilateral
vestibular deficits were defined by at least a 25% difference in slow-phase
eye velocity between right and left sides during the caloric or rotational
chair test (at a chair speed of 240°/s). Bilateral vestibular loss was
defined as less than 5° of slow-phase eye velocity in response to bithermal
caloric tests, including ice water, and a gain (peak slow-phase eye velocity/chair
velocity) of less than 0.2 on results of rotational chair testing. We defined
no response to ice water irrigation unilaterally or bilaterally as a complete
loss of vestibular function unilaterally or bilaterally, respectively, recognizing
that this represents no function in the horizontal canals, as it is not possible
to measure function of the remainder of the labyrinth by using caloric irrigation.
INSTRUMENTATION
An optotype (the letter E) is displayed on
the monitor when the subject's head velocity ranges from 120°/s to 180°/s.
A computer-generated program alters the orientation of the E randomly. The computer can be set so the letter appears during only
the rightward or leftward portion of a horizontal head movement. There are
5 trials at each acuity level. The optotype size is changed decrementally
so changes in visual acuity from line to line are equivalent to 0.1 logarithm
of the minimal angle of resolution (LogMAR).20
When the subject indicated the direction of orientation of the E, the subject's response was recorded, and the next trial was begun.
The trial was scored as an error if the subject incorrectly identified the
direction of the orientation of the E or if the subject
did not know the orientation after viewing the optotype 5 times. When the
subject incorrectly identified the orientation of the E for all optotypes presented at a particular acuity level, the test
was stopped. Data are the number of errors in identifying the orientation
of the optotype. Details of the test procedure have been reported previously.16
TEST PROTOCOL
The test was performed first with the subject's head stationary. The
series of optotypes was displayed and scored. The rate sensor was then placed
on the subject's forehead and oriented to detect horizontal movement of the
head. All subjects then performed a practice trial in which optotypes were
presented during active head movements to the right, to familiarize the subjects
with the test and to minimize a learning effect before data were collected.
Data were then collected separately for display of the optotype during active
rightward and leftward head movements (DVA-predictable). For DVA during unpredictable
head movements, subjects then performed a practice trial in which their heads
were moved by one of the investigators (M.C.S.) to the right and left in a
random order. The optotype was displayed only when the subject's head velocity
ranged from 120°/s to 180°/s. After the practice trial, data were
collected separately for display of the optotype during rightward (leftward
head movements did not result in display of the optotype) and leftward (rightward
head movements did not result in display of the optotype) head movements (DVA-unpredictable).
Dynamic visual acuity was calculated by counting the total number of errors
in identifying the orientation of the optotype and subtracting that value
from the static visual acuity. Raw scores were then converted to a LogMAR
score.
STATISTICAL ANALYSES
Comparison of DVA-predictable and DVA-unpredictable scores within each
group was examined using the t test. The relationship
of age to DVA scores in healthy subjects and in subjects with vestibular deficits
and the relationship of time from onset to DVA scores in the patient groups
were determined using regression analysis. Correlation of degree of deficit
to DVA scores in patients with UVL was determined using point-biserial correlation.
Between-group comparisons were performed using analysis of covariance with
least squares difference post hoc testing. Level of significance for all analyses
was P<.05. Data for age and time from onset are
presented as mean ± 1 SD; for DVA, mean ± 2 SD.
RESULTS
HEALTHY SUBJECTS
Twenty-six healthy subjects (mean age, 39.6 ± 15.5 years; range,
20-69 years) were studied. Mean DVA-predictable score was 0.030 ± 0.027
LogMAR; mean DVA-unpredictable score, 0.045 ± 0.044 LogMAR. The difference
between DVA-predictable and DVA-unpredictable scores was significant at P = .02.
Regression analysis showed a significant relationship between age and
DVA-unpredictable score (F = 15.18; P<.001) (Figure 1). Results indicated that 40% of
the variance of DVA-unpredictable score could be accounted for by age. The
relationship of age to DVA-predictable score approached significance (F =
3.59; P = .07).
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Figure 1. There was a significant relationship
between age and scores for dynamic visual acuity (DVA) during predictable
(DVA-predictable) and unpredictable (DVA-unpredictable) head movements, shown
here as binned data. Data are given as mean ± 2 SD; trend lines are
shown. LogMAR indicates logarithm of the minimal angle of resolution.
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PATIENTS WITH VESTIBULAR DEFICITS
UVL Group
Twenty patients with UVL were studied (mean age, 66.7 ± 13.1
years; range, 33-86 years). Table 1
gives the characteristics of the subjects with UVL. Mean time from onset was
7.3 ± 8.0 months. Only 3 of the patients were less than 1.5 months
from onset at the time of the study. In 1 patient, caloric testing could not
be performed because of a tympanic membrane perforation. Time from onset was
not a significant factor for DVA-predictable or DVA-unpredictable scores (Table 1). There was no correlation between
degree of deficit and DVA scores (Table
1). There was a significant difference between DVA-predictable and
DVA-unpredictable scores for head movements toward the affected and unaffected
sides (Table 2).
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Table 1. Subject Characteristics*
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Table 2. Factors Affecting DVA*
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BVL Group
Seven patients with BVL were studied (mean age, 63.4 ± 12.7 years;
range, 43-75 years) (Table 1).
Mean time from onset was 30.6 ± 38.5 months. Time from onset and degree
of deficit were not significant factors in DVA in this small group. There
was a significant difference between DVA-predictable and DVA-unpredictable
scores (t test, P = .004)
for patients with BVL (Table 2).
Effect of Age on DVA Score
We examined the possible relationship between DVA score and age in patients
with UVL and BVL separately (Table 2).
Regression analysis showed a significant relationship between age and DVA-predictable
and DVA-unpredictable scores for patients with UVL for head movements toward
the unaffected and affected sides (Figure
2). The relationship between age and DVA score was not significant
for patients with BVL.
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Figure 2. There was a significant relationship
between age and scores for dynamic visual acuity (DVA) during predictable
(DVA-predictable) and unpredictable (DVA-unpredictable) head movements toward
(A) and away from (B) the affected side in patients with unilateral vestibular
loss (UVL). No relationship was found between age and DVA in patients with
bilateral vestibular loss (BVL) (C). Trend lines are shown. LogMAR indicates
logarithm of the minimal angle of resolution.
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Differentiation Among Groups
Because age was a factor in DVA for the healthy subjects and for patients
with UVL, an analysis of covariance was used to compare DVA-predictable and
DVA-unpredictable scores across groups. For DVA-predictable scores, all pairwise
comparisons were significant (P<.03) except for
healthy subjects compared with the UVL group on movements toward the unaffected
side and the BVL group compared with the UVL group on movements toward the
affected side. For DVA-unpredictable scores, all pairwise comparisons were
significant (P<.01) except for healthy subjects
compared with the UVL group on movements toward the unaffected side. Comparison
of the difference between DVA-predictable and DVA-unpredictable scores across
groups showed that the BVL group differed from all other groups (P<.005) (Figure 3).
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Figure 3. Difference between scores for
dynamic visual acuity (DVA) during predictable (DVA-predictable) and unpredictable
(DVA-unpredictable) head movements for healthy subjects, for patients with
unilateral vestibular loss (UVL) for head movements toward the unaffected
and affected sides, and for patients with bilateral vestibular loss (BVL).
The BVL group differed significantly from all other groups (P<.005). Data are given as mean ± 2 SD. LogMAR indicates
logarithm of the minimal angle of resolution.
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COMMENT
Several studies have shown that there is little difference in visual-VOR
gain during active and passive head rotations in healthy subjects.3, 15 In contrast, our results show a significant
difference between DVA-predictable and DVA-unpredictable scores in healthy
subjects and in patients with UVL and BVL, with poorer acuity during DVA-unpredictable
movements. The most likely explanation for the differences between our findings
on DVA and those of other studies on visual-VOR gain is that the active and
the passive head rotations used in earlier studies were predictable in direction
and tempo.3, 15 This means that
the subjects could augment the VOR using other mechanisms for gaze stability.
We compared DVA during predictable head movements with DVA during unpredictable
head movements. This is a crucial consideration because in normal daily activities,
head movements do not always occur in a predictable manner but are random.1, 14, 21-22 It
is important, therefore, to examine gaze stability using unpredictable passive
head movements to establish the functional degradation of visual acuity that
may happen in a natural environment.
MECHANISM UNDERLYING DIFFERENCE IN DVA-PREDICTABLE AND DVA-UNPREDICTABLE
SCORES ACROSS GROUPS
Although the VOR is the primary reflex that stabilizes the eyes during
head movement, several other mechanisms have the potential to contribute to
gaze stability. These mechanisms may also contribute to gaze stability when
there is loss of vestibular function. When the head moves slowly or at low
frequencies, the pursuit/optokinetic system may be sufficient to maintain
gaze stability.4-5 Another mechanism
that may contribute to gaze stability during low-frequency head movements
is the COR. The COR is a compensatory eye movement that parallels the VOR
but is generated by inputs from receptors in ligaments and joints in the upper
cervical region.23 In healthy individuals,
the COR may not be present. Even when present, COR gain is unremarkable, ranging
from 0.07 to 0.20 at 0.1 Hz.7-9
We do not believe that the pursuit/optokinetic system or the COR contributed
to gaze stability in our patients during predictable or unpredictable head
rotations. In the paradigm we use, the velocity of head movement when the
target optotype is displayed (120°/s-180°/s) exceeds the ability of
these mechanisms to contribute to gaze stability.
During active head movements, efference copy, in which the motor commands
that produce 1 movement, eg, movement of the head, would also produce compensatory
eye movement, can contribute to gaze stability.11
During active or passive head movements, in which the direction and temporal
qualities of the head movement are predictable, central programming of appropriate
compensatory eye movement can contribute to gaze stability.6
Mechanisms such as efference copy and the central programming of eye movements
may have contributed to gaze stability during active head rotations (which
are also predictable) but would not have contributed to gaze stability during
the unpredictable passive head rotations. We think these later 2 mechanisms
account for the difference between DVA-predictable and DVA-unpredictable scores
that we found in all groups.
RELATIVE CONTRIBUTION OF CENTRAL PROGRAMMING TO DVA ACROSS GROUPS
We found that for healthy subjects and patients with UVL, head movements
toward the affected and unaffected sides had the same difference between DVA-predictable
and DVA-unpredictable scores (Figure 3).
For patients with BVL, however, the difference between DVA-predictable and
DVA-unpredictable scores was significantly larger compared with all other
groups. This may be due to the superior use of central programming of eye
movements and efference copy by the patients with BVL compared with the other
groups. Another possibility is that patients with BVL differed from the other
groups because the deficit in the patients with BVL was so much greater.
DISTINGUISHING AMONG GROUPS
Our results differ from those of a study by Tian et al24
that failed to demonstrate significant differences in DVA between healthy
subjects and patients with UVL or a difference between DVA for head movements
toward the affected and unaffected sides in UVL. One explanation for the disparity
between the studies is the velocity of head rotation used. We required head
velocities to range from 120°/s to 180°/s before the target letter
would appear. At those velocities, the eye movement generated by inhibition
of the intact labyrinth during head movements toward the affected labyrinth
would not be sufficient to produce gaze stability. In contrast, Tian et al24 displayed the target at head velocities ranging from
50°/s to 75°/s, which would be within the effective range of the intact
labyrinth to produce appropriate compensatory eye movements during head rotations
toward the affected side. Using higher velocities of head movement is clearly
necessary to reveal the difference in DVA between healthy subjects and patients
with UVL as well as the difference between affected and unaffected sides in
patients with UVL.
Unlike a previous report from our laboratory,16
in the present study we found no difference in DVA-predictable scores between
healthy subjects and patients with UVL during head movements toward the unaffected
side. One possibility is that the UVL group in the present study had compensated
more for the effect of the vestibular loss than did the patients with UVL
in the previous study. Another possibility is that there is a difference in
the degree of vestibular loss between the 2 groups. Finally, patients with
UVL in the present study were older (mean age, 66.7 ± 13.1 years) than
those in the previous study group (mean age, 51.7 ± 14.6 years), and
this difference may have been a factor.
EFFECT OF AGE ON DVA
In general, older subjects had poorer visual acuity during head movement
than did younger subjects. This was true for DVA-predictable and DVA-unpredictable
scores across all groups. This general trend is similar to earlier results
from our laboratory with DVA-predictable scores.16
In part, this may be related to changes in the vestibular system with increasing
age.25 Baloh et al25
found that at high-velocity head movements (in the range used in our study),
older subjects (aged >75 years) had lower visual-VOR gain compared with younger
subjects (aged 19-39 years). This decrease in visual-VOR gain with age would
result in greater retinal slip and therefore in a decrement in dynamic visual
acuity.
We found that, for healthy subjects and for the UVL group for head movements
toward the unaffected side, the difference between DVA-predictable and DVA-unpredictable
scores increased with increasing age (differences in the slopes of the trend
lines for DVA-predictable and DVA-unpredictable scores are seen in Figure 1 and Figure 2B). This suggests that age has a greater effect on DVA in
subjects who are older compared with younger subjects. This was not true for
patients with UVL for head movements toward the affected side, or for patients
with BVL, suggesting that the loss of vestibular function, with the resultant
increase in retinal slip during head movement, has a far greater impact on
DVA than has age.
CONCLUSIONS
The difference between DVA-predictable and DVA-unpredictable scores
suggests the degree to which subjects are able to use mechanisms such as the
central programming of eye movements and efference copy to enhance gaze stability.
Patients with BVL appear to use these compensatory mechanisms to a greater
extent than do patients with UVL or healthy subjects. Although visual acuity
during unpredictable head movements is poorer than during active (predictable)
head movements, both tests distinguish patients with UVL and BVL from healthy
subjects. The presence of a vestibular deficit has a greater effect on DVA
than has age.
AUTHOR INFORMATION
Accepted for publication May 17, 2001.
Supported by grant 03196 from the National Institute on Deafness and
Other Communication Disorders, Bethesda, Md (Drs Herdman and Tusa), and by
the Foundation for Physical Therapy, Alexandria, Va (Mr Schubert).
Corresponding author and reprints: Susan J. Herdman, PT, PhD, Department
of Rehabilitation Medicine, Emory University, 1441 Clifton Rd NE, Atlanta,
GA 30322 (e-mail: sherdma{at}emory.edu).
From the the Department of Rehabilitation Medicine (Dr Herdman and
Mr Schubert), the Department of Neurology (Dr Tusa), and Yerkes Research Center
(Dr Tusa), Emory University, Atlanta, Ga.
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