(Investigative Ophthalmology and Visual Science. 2001;42:2826-2830.)
© 2001
by The Association for Research in Vision and Ophthalmology, Inc.
Reduced Binocular Beat Visual Evoked Responses and Stereoacuity in Patients with Duane Syndrome
John J. Sloper1,
Carolyn Garnham2,
Petrous Gous3,
Roger Dyason3 and
Deborah Plunkett4
1 From the Moorfields Eye Hospital, London, United Kingdom
2 Departments of Medical Physics,
3 Ophthalmology, and
4 Orthoptics, University Hospital, Nottingham, United Kingdom.
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Abstract
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PURPOSE. To study the effects that the abnormal eye movements of patients with
Duane retraction syndrome have on the development of binocular
function.
METHODS. Pattern reversal visual evoked responses (VEPs) to 15-minutes-of-arc
and 60-minutes-of-arc checks and binocular beat VEPs to diffuse
sinusoidally modulated 18- and 20-Hz stimuli were recorded in 10
patients with Duane retraction syndrome who maintain binocular function
by using an abnormal head posture. Visual acuity, stereoacuity, and eye
movements were measured. The results have been compared to those from
10 normal subjects.
RESULTS. The patients with Duane retraction syndrome had reduced stereoacuity
compared to the normal control group (TNO mean, 82.5 seconds of arc
compared to 37.5 seconds of arc; Titmus mean, 143 seconds of arc
compared to 44 seconds of arc). The binocular beat VEPs showed a
significantly reduced difference beat response at 2 Hz in the patients
with Duane syndrome compared to normal subjects (mean signal-to-noise
ratio 2.40 ± 1.05 compared to 4.30 ± 2.66; t
= 2.21, df = 18, P < 0.05).
Binocular enhancement of the P100 pattern reversal amplitude to
15-minute checks was increased in these patients, because of a
reduction of the monocular P100 amplitudes compared to the normal
group.
CONCLUSIONS. Patients with Duane syndrome who maintain binocular function using an
abnormal head posture have reduced stereoacuity and show
electrophysiological evidence of reduced cortical binocular
interaction.
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Introduction
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Most patients with Duane retraction syndrome maintain
binocular single vision by using an abnormal head posture to compensate
for their restricted ocular motility.1
2
3
4
However, their
stereoacuity is reduced compared to normal subjects of a similar
age5
and it has been suggested that this is due to the
intermittent misalignment of their eyes during visual
development.6
In a study reported in a companion article
in this issue of IOVS,7
it has been shown that
such patients demonstrate an increase in binocular enhancement of
contrast sensitivity, and it has been suggested that the combination of
this with reduced stereoacuity may be explained by a partial loss of
binocularly driven cortical neurons. In the present study, we
investigated binocular function electrophysiologically in a further
group of patients with Duane syndrome, by using pattern reversal and
binocular beat VEPs.
Some of the data in this study have been presented
earlier.8
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Subjects and Methods
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Ten patients with Duane syndrome, aged between 11 and 19 years,
were studied and compared to 10 normal subjects of similar ages.
Patients were recruited either during a clinic visit or were contacted
from clinic records and were the first 10 patients with Duane syndrome
and binocular single vision who were willing to participate in the
study. Ocular motility was examined clinically. All patients with Duane
syndrome showed failure of abduction of one or both eyes, together with
retraction on attempted adduction of the eye.9
10
11
Three
had had previous squint surgery. With their head postures, nine had
bifoveal binocular single vision with no movement on the cover–uncover
test and a normal result in the Worth 4-dot test indicating no central
suppression. The remaining patient had binocular single vision with
microtropia. Visual acuity was measured using
a standard Snellen chart and the appropriate spectacle correction (Table 1)
. All had Snellen acuity of at least 6/9 in each eye with the
exception of one bifoveal patient who was 6/18 in the affected eye
after patching for anisometropic amblyopia. All normal subjects had
normal cover tests and ocular movements (Table 2)
. Stereoacuity was measured with the Titmus and TNO stereotests at a
standard distance in patients wearing their normal spectacle
corrections, if any. Patients were allowed time to find the optimum
head posture for these tests.
Pattern reversal VEPs were recorded by standard methods in patients
wearing their distance spectacle corrections, if any. No patient had
difficulty in maintaining fixation monocularly with either eye during
recording; this was confirmed by observation of the subjects. Pattern
reversal VEPs were recorded to black-and-white checks subtending 15
minutes of arc or 60 minutes of arc of the visual angle, with a midline
occipital electrode at Oz and an earlobe reference. Patients who were
binocular with an abnormal head posture used it during binocular
recording. Amplitude and latency of the peak of the P100 response were
measured. Binocular enhancement was calculated as the binocular P100
amplitude divided by the mean of the monocular P100 amplitudes or by
the greater monocular amplitude. Delay was calculated as the P100
latency from the affected or more affected eye minus the P100 latency
from the fellow eye.
Binocular beat VEPs were recorded using the same recording arrangements
as used for pattern reversal VEPs. The stimulus was produced by
custom-built goggles with red LEDs producing a large diffuse field,
with luminance modulated sinusoidally at 18 Hz for one eye and 20 Hz
for the other eye. For each subject, two runs of approximately 4
minutes each were recorded at a mean luminance of 40 candelas
(cd)/m2 and two at 20
cd/m2, both with a modulation depth of 100%.
Responses were analyzed by fast Fourier transform. Signal-to-noise
ratio was measured at the difference frequency of 2 Hz, using the
average of the 0.5-, 1-, 1.5-, 2.5-, 3-, and 3.5-Hz bins to calculate
the noise level for that frequency and at the input frequencies of 18
and 20 Hz, using the average of the 15-, 17-, 19-, 21-, and 23-Hz bins
to calculate the noise level for those frequencies.
Statistical comparisons of electrophysiological data between Duane
syndrome and control groups were made using Student’s
t-test for independent groups; comparisons between eyes
within groups were made using paired t-tests. Stereoacuity
results were analyzed using the Mann-Whitney test corrected for tied
values.
This research conformed with the tenets of the Helsinki Declaration.
Informed consent was obtained from all subjects and their parents, if
appropriate, after the nature and possible consequences of the study
were explained. The research was approved by the hospital ethics
committee.
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Results
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Clinical data for the Duane patients and normal control subjects
are shown in Tables 1
and 2
. All subjects in both groups had corrected
acuity of 6/9 or better, with the exception of one eye in a patient
with Duane syndrome who had undergone patching for anisometropic
amblyopia.
The patients with Duane syndrome had reduced stereoacuity compared to
the normal group (TNO mean excluding two negative subjects,
82.5 seconds of arc compared to 37.5 seconds of arc, P < 0.001; Titmus mean, 143 seconds of arc compared to 44 seconds of
arc, P < 0.001; both Mann-Whitney test; n =
10).
Binocular Beat VEPs
Averaged binocular beat waveforms in a patient with Duane syndrome
are shown in Figure 1A
and in a normal subject in Figure 1B
. Although present, the 2-Hz
component of the waveform was less consistent in the subject with Duane
syndrome than in the control subject. Fourier analyses of these
waveforms is shown in Figures 1C
and 1D . These confirm the reduced 2-Hz
component in the patient with Duane syndrome. Overall the difference
beat response at 2 Hz was significantly reduced in the patients with
Duane syndrome compared to the normal age-matched group (Fig. 2A)
, with the mean 2-Hz signal-to-noise ratio for the Duane patients being
2.40 ± 1.05 compared to 4.30 ± 2.66 for the control
subjects (t = 2.21, df = 18, P <
0.05). To show that this reduction was specific for the 2-Hz difference
frequency the results were also calculated as the ratio of the 2-Hz
signal-to-noise ratio divided by the mean of the 18- and 20-Hz
signal-to-noise ratios for each subject (Fig. 2B)
. This ratio was also
significantly reduced in the patients with Duane syndrome compared to
the normal control subjects (ratio in the Duane group 0.58 ± 0.28
compared to 1.14 ± 0.72 in the control group; t =
2.44, df = 18, P < 0.05). This shows that
the reduction of the response in the patients with Duane syndrome was
specific for the difference frequency in relation to the input
frequencies.
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Figure 1. (A) Binocular beat VEP recorded from a patient with Duane
syndrome. Although present, the 2-Hz component was not as strong as in
the normal subject. (B) Binocular beat VEP recorded from a
normal subject. A strong 2-Hz component was present. (C)
Fast Fourier analysis of the waveform of (A) of a patient
with Duane syndrome. The input frequencies were at 18 and 20 Hz, with a
weak difference beat response at 2 Hz. (D) Fast Fourier
analysis of the waveform of (B) of a normal subject. The
components at the input frequencies of 18 and 20 Hz were similar to
those in (C), but the difference beat response at 2 Hz was
much more prominent.
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Figure 2. Comparison of (A) signal-to-noise ratios at the difference
beat frequency of 2 Hz and (B) the ratio of signal-to-noise
ratios at 2 Hz to those at the input frequencies of 18 and 20 Hz in 10
patients with Duane syndrome and 10 normal subjects.
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Pattern Reversal VEPs
The amplitude of the P100 response to 15-minute checks was greater
under binocular than monocular conditions in patients with Duane
syndrome and in normal subjects (Fig. 3)
. The binocular enhancement to the mean monocular amplitude for
15-minute checks was significantly greater in the patients with Duane
syndrome than in normal subjects (Table 3)
. This was because the mean P100 amplitudes of the monocular responses
were significantly smaller in the Duane group than in the normal group,
whereas the amplitude of the binocular responses was similar in both
groups. A comparable difference was not seen with the 60-minute check
size. The binocular enhancement to the larger monocular amplitude was
also greater with 15-minute checks in patients with Duane syndrome than
in normal subjects (mean, 1.78 ± 0.4 compared to 1.09 ±
0.2; P < 0.001), but not with 60-minute checks (mean,
1.29 ± 0.3 compared to 1.24 ± 0.3; P =
0.74).
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Figure 3. Pattern reversal VEP to 15-minute checks from a patient with Duane
syndrome. The P100 amplitude was larger with binocular than with
monocular stimulation.
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There was no significant difference in the P100 latency between fellow
and affected eyes of the patients with Duane syndrome for either check
size (Table 4)
. The binocular P100 latency was significantly shorter than the mean
monocular latency for normal subjects for both 15-minute checks (118.9
compared to 121.6 msec; t = 2.70, df = 9,
P < 0.05) and 60-minute checks (114.0 compared to
120.3 msec; t = 3.36, df = 10, P < 0.01). For the Duane patients the difference was significant for
60-minute checks (114.0 compared to 118.0 msec; t = 2.51,
df = 10, P < 0.05) but not for the
15-minute checks (118.0 compared to 119.7 msec; t = 1.25
df = 9, P = 0.24).
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Discussion
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In the companion article7
it was shown that patients
with Duane syndrome have reduced stereoacuity but increased binocular
enhancement of their contrast sensitivity. It was suggested that these
abnormalities arise because of intermittent ocular misalignment during
the early years of life, leading to the loss of a proportion of
binocularly driven cortical cells, and a model of how this could lead
to the apparently paradoxical combination of reduced stereoacuity and
increased binocular enhancement was proposed. The present study, using
electrophysiological techniques, has demonstrated a reduction of the
binocular beat VEP but increased binocular enhancement of the P100
response of the pattern reversal VEP to small checks. These
electrophysiological abnormalities show striking parallels to the
psychophysical findings.
A binocular beat VEP is produced by stimulating each eye with a diffuse
sinusoidally modulated stimulus at a slightly different frequency for
each eye. In addition to the stimulating frequencies, the beat VEP
normally contains new beat frequencies generated by the nonlinear
addition of the input frequencies by binocularly driven cortical
cells.12
It has been shown that these beat frequencies are
reduced or absent in both animals and patients with abnormal or absent
binocularity.13
14
The reduced difference beat responses
seen in patients with Duane syndrome thus indicate that they have a
reduced population of binocular cells in the cortex, as proposed in the
companion article.7
Binocular enhancement of the pattern reversal VEP has been suggested as
a measure of binocularity in patients with squints.15
16
17
18
19
20
However, no correlation between stereoacuity and binocular enhancement
has been shown in a previous study of normal development in humans
which showed that binocular enhancement to small checks decreases with
age, whereas stereoacuity increases.21
A subsequent study
of binocular patients with Duane syndrome showed that they also
demonstrated binocular enhancement, but that this did not reduce
significantly with age.6
Patients in the present study are
older that those in this previous study and show that the failure of
reduction of binocular enhancement during development produces a
greater than normal enhancement to small checks in this older group.
This is an interesting parallel to the greater than normal binocular
enhancement of contrast sensitivity described in patients with Duane
syndrome.7
In both instances the increased enhancement
occurs because monocular responses are reduced, whereas the binocular
response is normal. The P100 amplitude probably reflects the response
of both monocular and binocular cells. It is proposed that the number
of cells available to each eye is reduced, because cells that were
previously binocular are lost to the other eye, but this increased
population of cells driven only by the other eye is then recruited
under binocular conditions and gives an enhanced response, as with the
contrast sensitivity.7
However, even a total loss of
binocular cells can account for a binocular enhancement ratio of only
two, and it is likely that other mechanisms are also involved. In
particular, many patients with Duane syndrome show interocular
suppression under nonbinocular conditions, and this may also contribute
to reduced monocular responses.
Because the underlying motor pathophysiology is reasonably well
understood, patients with Duane syndrome provide an interesting model
in which to study the effects of intermittent motor misalignment on
sensory visual development. The disruption of binocular function seen
in Duane syndrome is usually relatively minor and generally stays
stable into adult life, probably because of the way the patients are
able to maintain ocular alignment by using anomalous head postures. The
minority of patients who lose binocular function completely and develop
a constant squint usually have a second abnormality, such as
anisometropia6
and patients with Duane syndrome are
particularly sensitive to disruption of binocularity by refractive
abnormalities. It appears that binocular function in Duane syndrome is
surprisingly resistant to intermittent ocular misalignment, but that
different anomalies can have an additive affect in the disruption of
binocularity. This may be important in understanding the deterioration
in control seen in some children with intermittent squints. These
findings are likely to be of relevance to other forms of intermittent
squint, such as intermittent exotropias, congenital fourth nerve
palsies, and convergence excess esotropias. If a similar loss of
binocularly driven cells is present in these other intermittent
squints, studying them may lead to an understanding of why binocular
function breaks down in some patients and not in others.
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Footnotes
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The study was conducted at the University Hospital, Nottingham, United
Kingdom.
Submitted for publication February 2, 2001; revised June 12, 2001;
accepted July, 3, 2001.
Commercial relationships policy: N.
The publication costs of this article were defrayed in part by page
charge payment. This article must therefore be marked
"advertisement" in accordance with 18 U.S.C. 
1734
solely to indicate this fact.
Corresponding author: John J. Sloper, Moorfields Eye Hospital, City
Road, London EC1V 2PD, UK.
john.sloper{at}dial.pipex.com
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W. E. Marshman, E. Dawson, M. M. Neveu, M. J. Morgan, and J. J. Sloper
Increased Binocular Enhancement of Contrast Sensitivity and Reduced Stereoacuity in Duane Syndrome
Invest. Ophthalmol. Vis. Sci.,
November 1, 2001;
42(12):
2821 - 2825.
[Abstract]
[Full Text]
[PDF]
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Abstract
Introduction
