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Optokinetic Nystagmus in Strabismus: Are Asymmetries

Related to Binocularity?
Christophe Valmaggia,1 Frank Proudlock,2 and Irene Gottlob2

PURPOSE. Strabismus may be associated with an asymmetry of temporal to nasal (TN) stimulus motion compared with nasal to
monocular horizontal optokinetic nystagmus (OKN). It is un- temporal (NT) stimulus motion when the stimulation is applied
clear whether OKN asymmetries are associated with deficiency monocularly.8 Hoffmann9 hypothesized that horizontal TN
in binocular and/or stereovision. In the current study, patients OKN present early in life is mediated entirely by subcortical
with different degrees of binocularity were investigated. projections to the pretectal nucleus of the optic tract (NOT)
METHODS. OKN was examined in the dominant and nondomi- and the dorsal terminal nucleus (DTN) of the accessory optic
nant eyes of four groups of patients: (1) no measurable binoc- system. Cortical projections to NOT-DTN develop later, and,
ularity (NB), (2) poor binocularity (PB)—that is, showing bin- once established, the subcortical projections lose influence
ocularity on the Bagolini Test and/or rudimentary stereovision, over NOT-DTN cells. Thus, the increasing dominance of the
(3) good binocularity (GB) with good stereoacuity after squint cortex allows the development of the symmetrical OKN re-
surgery, and (4) a control group. Monocular OKN was elicited sponse in normal subjects. OKN symmetry and binocular vi-
with black-and-white stripes moving temporally to nasally (TN) sion in infants develop simultaneously.3,4 If binocular vision is
or nasally to temporally (NT) at velocities of 15, 30, 45, and 60 disrupted, it is likely that subcortical pathways, which favor
deg/s. Eye movements were recorded with infrared oculogra- nasalward motion, will dominate.
phy. It has been reported that the OKN deficit is more prevalent
when strabismus manifests itself early, between the first 6 and
RESULTS. Only subjects in the NB group showed a significant 24 months of life.5,10 –16 However, it is usually difficult to know
OKN asymmetry, with preference for TN stimulation in dom- the exact time of onset. Most studies have examined older
inant and nondominant eyes. Subjects with PB did not have subjects, in whom the onset of strabismus was evaluated ret-
significant OKN asymmetries but reduced OKN gains in both rospectively, without clinical examination data available from
stimulus directions. Subjects with GB had normal mean OKN the time of onset. Only a few studies have investigated the
gains without asymmetry. Larger OKN asymmetries were cor- relationship of binocular function and OKN asymmetry, and
related with younger age at detection of strabismus if NB and these have suggested that there is no correlation.12,17–19 One
GB were grouped together, but not if each group was analyzed study, however, showed a relationship between stereopsis and
separately. symmetry of OKN gain.20
CONCLUSIONS. For the first time, a large groups of patients In this study, our purpose was to investigate the relation
classified by level of binocular vision has been investigated. between horizontal OKN asymmetries and clinical characteris-
The results show that OKN gain and asymmetry are associated tics such as binocular- and stereovision, visual acuity or age of
with the development of binocular vision. OKN investigation the onset of squint. OKN was examined in four groups of
may be helpful to identify patients with binocularity or binoc- subjects divided according to binocular vision: (1) no measur-
ular potential in strabismus. (Invest Ophthalmol Vis Sci. 2003; able binocular vision (NB); (2) poor binocularity (PB) when
44:5142–5150) DOI:10.1167/iovs.03-0322 tested on the Bagolini Test and/or gross stereopsis; (3) good
binocular vision (GB) with a normal or almost normal level of

O KN is a rhythmic involuntary eye movement elicited by


large moving patterns.1 It consists of a slow component
with eye movements in the same direction as the movement of
postoperative stereoacuity; and (4) normal subjects. In the NB
and GB groups, we selected only subjects for whom the age of
onset of strabismus had been documented in our department.
a target and a fast component with saccadic eye movements in
the opposite direction.2 OKN can be quantified by measuring
the gain, which corresponds to the ratio of slow-phase eye METHODS
velocity and stimulus velocity.
Patients
Horizontal OKN asymmetry is evident in early normal in-
fancy,3,4 and in patients who have normal visual development The ethics committee of the Kantonsspital St. Gallen approved the
disrupted by unequal visual inputs from the two eyes due to study. Informed consent was obtained from all subjects after explana-
strabismus,5 amblyopia,6 or unilateral congenital cataracts.7 tion of the nature of the investigation. The study was performed in
This asymmetry of OKN is due to a larger gain elicited by accordance with the tenets of the Declaration of Helsinki.
Patients were recruited from the Department of Strabismology and
Neuroophthalmology of the Kantonsspital St. Gallen. At the time of
From the 1Department of Ophthalmology, Kantonsspital, St. OKN examination, all subjects were old enough to cooperate easily
Gallen, Switzerland; and the 2Department of Ophthalmology, Univer- with all tests. The subjects had no ophthalmic abnormalities other than
sity of Leicester, Leicester, United Kingdom. squint or amblyopia and were otherwise healthy. A full ophthalmic
Submitted for publication March 28, 2003; revised July 13, 2003; examination, including visual acuity, binocular function (Bagolini test),
accepted August 5, 2003. stereoacuity (TNO test [Richmond Products, Boca Raton, FL)]and Tit-
Disclosure: C. Valmaggia, None; F. Proudlock, None; I. Gott- mus fly for gross stereopsis of 3000 seconds of arc), ocular motility,
lob, None
cover test, slit lamp examination, funduscopy, and cycloplegic refrac-
The publication costs of this article were defrayed in part by page
charge payment. This article must therefore be marked “advertise- tion, was performed in all subjects. Patients with latent nystagmus
ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact. were excluded from the study because this form of nystagmus interacts
Corresponding author: Christophe Valmaggia, Department of with OKN, slowing down the NT slow phase and speeding up the TN
Ophthalmology, Kantonsspital, CH-9007 St. Gallen, Switzerland; slow phase.21
christophe.valmaggia@kssg.ch. Four different groups of subjects were examined:

Investigative Ophthalmology & Visual Science, December 2003, Vol. 44, No. 12
5142 Copyright © Association for Research in Vision and Ophthalmology
IOVS, December 2003, Vol. 44, No. 12 OKN and Strabismus 5143

1. Twenty patients with no measurable binocularity (NB; 8 males, measuring the position of the corneal reflex with respect to the center
12 females; mean age at time of OKN examination: 17.5 ⫾ 13 of the pupil. The investigation was independent of head movements. A
years; SD). Strabismus was documented before or at 18 months near infrared illumination of the eye (880 nm) was used to produce the
of age in all patients in this group. Twelve patients had disso- corneal reflex and the pupil image. The system operated with a sam-
ciated vertical deviation (DVD), and 16 had occlusion therapy pling rate of 60 Hz and achieved a resolution of 10 minutes of arc. The
for amblyopia. All subjects underwent strabismus surgery be- slope of the best-fit regression line plotted across the sample points of
fore OKN examination. After surgical correction of squint, ste- the OKN slow phases was used to estimate the slow phase velocity.
reopsis (measured using the Titmus fly) or binocular vision Precision was no greater than 5%. The noise of the velocity measure-
(measured by absence of suppression of the nondominant eye ment was approximately 0.3 deg/s root mean square (RMS; manufac-
on the Bagolini test) was not detectable in any of the subjects of turer’s specifications). In the different strabismus groups, OKN gains of
this group. Details of patients with NB are listed in Table 1. the dominant and nondominant eyes were assessed. In the control
2. Twenty patients with poor binocular vision (PB; 10 males, 10 group, the mean OKN gain of the right eye was measured. Each eye
females; mean age at time of OKN examination: 15.6 ⫾ 13.9 was investigated with the different stimulus velocities and directions,
years; SD)—that is, with peripheral fusion on Bagolini test with with a time interval of 2 minutes between the trials. To record stare
central scotoma and/or stereopsis measured with the Titmus fly OKN, subjects were instructed not to follow individual stripes across
(15 subjects). None of the patients with PB demonstrated ste- the screen but to fixate stripes as they passed in the center of the
reopsis when examined with the TNO test. At the time of screen.
examination, they all had small squint angles, which corre- Eye movement analysis included the detection of OKN slow and
sponded either to primary or secondary postoperative micro- fast phases and calculation of the average velocity for the slow phases.
tropia. Ten of these patients had a history of sudden increase of The mean velocity of consecutive slow phases was measured from 5
squint angle when they first were examined in our department. seconds after the stimulus onset, for a period of 10 seconds, at each
Photographs of the patient before onset of strabismus con- stimulus velocity and stimulus direction. Other investigators observed
firmed this, although the photographs did not exclude micro- that the early OKN is dominant in humans and has a stable velocity
tropia. These patients underwent squint surgery and achieved after a time of approximately 0.5 seconds.8 Accordingly, the OKN slow
rudimentary binocular vision after surgery. Because of the small phases had reached a stable velocity over the time period that was
squint angle in the PB group, strabismus was most frequently analyzed in our experiment.
detected after the screening tests for amblyopia or because of Eye movement recordings were numbered, and analysis was per-
the sudden development of a large strabismus (with possible formed without knowledge of the clinical data of the patients. The
preexistence of microtropia). Therefore, it was unlikely that the OKN gain, defined as the ratio of slow-phase velocity to stimulus
time of first examination in our department had any correlation velocity, was measured for TN and NT stimulus directions. An OKN
with time of onset of squint in this group. In the PB group 10 asymmetry factor was calculated from the OKN gains by dividing the
patients had occlusion therapy for amblyopia. None of the TN gains by the sum of the TN and NT gains (TN/TN ⫹ NT) for each
subjects in this group had DVD. Details of patients with PB are velocity and for each examined eye. Asymmetry factors above 0.5
listed in Table 2. indicate a larger gain for TN stimulation, whereas asymmetry factors
3. Fifteen patients (seven males, eight females; mean age at time of below 0.5 correspond to a larger gain for NT stimulation. For each
OKN examination: 10.2 ⫾ 3.1 years; SD) who achieved binoc- group of patients the percentage of subjects outside of the 2 SD of the
ular vision on the Bagolini test and good levels of stereovision normal subjects was calculated for the OKN gain and asymmetry index.
on the TNO test (15–240 seconds of arc) at the time of exam- Analysis of variance was used to compare gains of different groups and
ination (GB). All had late-onset strabismus and had a well- was corrected for multiple comparisons by Student-Newman-Keuls
documented sudden onset of strabismus between 18 and 36 test. Correlations coefficients were calculated between age of detec-
months of age. History and/or examination revealed that, tion of strabismus and asymmetry factor. Differences were considered
shortly after onset of squint, all had diplopia or signs indicating as significant for P ⬍ 0.05.
diplopia, such as frequently closing one eye. Two patients in
the GB group had eyes patched for amblyopia. None of them
had DVD. All had undergone strabismus surgery and had no RESULTS
postoperative manifest squint. In Table 3 further details of
patients with GB are listed. Eye movement recordings are shown in Figure 1 in response to
4. Twenty control subjects (8 males, 12 females; mean age 14.8 ⫾ stimuli moving at 45 deg/s in TN and NT directions from a
7.2 years; SD) without squint or history of squint surgery, with representative subject in each group. Whereas the NT re-
visual acuity of 1.0 or better in each eye, and stereoacuity sponse was clearly reduced in the subject with NB (Fig. 1A),
between 15 and 120 seconds of arc on the TNO test. there was no clear difference between NT and TN responses in
the patient with PB. However, the gain appeared slightly lower
In the NB and GB groups, only patients who had been examined in our
in the patient with PB for both stimulation directions (Fig. 1B).
department and had well-documented clinical notes from the age of
OKN recordings of the subject with GB (Fig. 1C) were similar
diagnoses of squint were included in the study.
to those of the control subject (Fig. 1D).
In Table 4, the percentage of subjects with gains that de-
Methods clined to below the 95% confidence interval of the gain for
OKN stimulation, eye movement recordings and analysis were per- control subjects are listed for dominant and nondominant eyes
formed with the vision monitor equipment (Metrovision, Perenchies, at the four stimulus velocities. Whereas most patients in the NB
France).22,23 Visual stimuli were generated on a monitor, measuring 51 group had normal TN gains and abnormal NT gains, in the PB
cm in diagonal, placed 40 cm away from the patients with a frame rate group, the gain abnormality was similar for TN and NT stimu-
of 120 Hz. The patient’s head was stabilized with a head-chin rest. The lation. More patients showed reduced OKN gains in the PB
screen covered a visual field of 54° horizontally and 41° vertically. group than in the GB group.
OKN was elicited with alternating white (luminance, 70 cd/m2) and Figure 2 represents the mean OKN gains for dominant and
black (luminance, ⬍1 cd/m2) vertical stripes. Each stripe covered 2° of nondominant eyes, at different stimulation velocities, in each
visual angle (equivalent to a visual acuity of 20/2400). Stripes moved in group of subjects. In the NB group, OKN gains for NT stimu-
random order at a constant velocity of 15, 30, 45, or 60 deg/s, either in lation were significantly lower than in the control group, at
TN or NT direction for 40 seconds. Eye movements were recorded by each velocity in the deviating and the nondeviating eye (P ⬍
5144
Valmaggia et al.

TABLE 1. Details of Patients with No Measurable Binocularity

First First
Age at Measured Measured Strabismus SA at Age at VA at Time of VA at Time of Strabismus SA at Time of
Diagnosis VA VA Form at Presentation Occlusion OKN Test OKN Test OKN Test Form at Time OKN Test
Patient (mo) (DE) (NDE) Presentation (Degrees) DVD Therapy (y) (DE) (NDE) of OKN Test (Degrees)

1 14 0.8 0.6 R eso 11.4 N Y 9 1.0 1.0 Rexo 8.0


2 18 0.8 0.6 L exo 11.4 N Y 48 1.0 1.0 L eso 21.3
3 8 0.6 0.8 R eso 16.7 Y Y 7 1.0 0.6 Rexo 1.2
4 5 1.25 1.0 L exo 22.3 N N 33 1.25 0.8 L exo 8.0
5 3 0.5 0.4 L eso 19.3 Y Y 11 1.0 1.0 L eso 21.3
6 16 0.6 0.4 R eso 19.3 N Y 40 1.25 1.0 Rexo 8.0
7 4 0.8 0.6 L eso 11.4 Y Y 37 0.9 1.0 L exo 6.3
8 2 0.8 0.3 R eso 19.3 Y Y 14 1.0 0.6 R eso 12.5
9 4 1.25 0.1 L eso 19.3 Y Y 10 0.9 0.8 L eso 22.3
10 6 0.5 0.4 L eso 14.1 Y Y 13 1.0 0.9 L eso 8.0
11 12 1.0 0.8 L eso 23.4 N N 14 1.0 1.25 L eso 7.0
12 18 1.25 1.0 Rexo 14.1 Y N 9 1.0 1.0 Rexo 12.5
13 2 0.6 0.6 R eso 24.0 Y Y 6 0.9 0.7 Rexo 12.5
14 3 1.0 0.8 L exo 9.1 Y Y 10 1.0 0.9 L exo 2.3
15 2 0.8 0.5 R eso 24.0 N Y 36 0.6 0.6 R eso 20.0
16 1 0.5 0.3 L eso 40.0 Y Y 5 0.9 0.6 L eso 12.5
17 5 0.6 0.5 R eso 19.3 N Y 9 0.9 0.8 R eso 12.5
18 12 0.5 0.1 R eso 22.0 Y Y 9 0.6 0.6 R eso 21.8
19 16 1.0 0.5 R eso 19.3 N Y 8 1.0 0.8 R eso 15.7
20 1 1.0 0.4 L exo 14.1 Y N 22 1.0 1.0 L eso 12.5

DE, dominant eye; NDE, nondominant eye; SA, squint angle; R, right; L, left; eso, esotropia; exo, exotropia; y, yes; n, no.
IOVS, December 2003, Vol. 44, No. 12
TABLE 2. Details of Patients with Poor Binocularity

First First
IOVS, December 2003, Vol. 44, No. 12

Age at Measured Measured Strabismus SA at Age at VA at Time of VA at Time of Strabismus SA at Time of


Diagnosis VA VA Form at Presentation Occlusion OKN Test OKN Test OKN Test Form at Time OKN Test Titmus
Patient (mo) (DE) (NDE) Presentation (Degrees) Therapy Surgery (y) (DE) (NDE) of OKN Test (Degrees) Fly

1 46 1.25 0.1 R eso 4.6 Y N 7 1.0 0.8 R eso 4.6 Pos


2 44 1.25 0.8 Rexo 19.3 Y Y 8 1.0 0.8 R exo 3.5 Pos
3 56 1.25 1.0 L eso 16.7 N Y 12 1.0 1.0 L eso 4.6 Neg
4 73 1.0 1.0 L eso 23.8 N Y 14 1.0 1.0 L eso 4.6 Neg
5 56 0.8 1.25 L eso 19.3 N Y 9 1.0 1.0 L eso 4.6 Pos
6 66 1.0 0.6 R eso 16.7 Y Y 12 1.0 1.0 R eso 3.5 Pos
7 64 1.0 0.5 R eso 4.5 Y N 11 1.0 1.0 R eso 4.6 Neg
8 54 1.25 0.5 L eso 4.5 N N 12 1.25 0.6 L eso 0.6 Pos
9 48 1.25 1.25 R eso 14.1 N Y 9 1.25 1.25 R eso 4.6 Pos
10 51 0.9 0.4 L eso 16.3 Y Y 8 1.0 1.0 L eso 2.3 Neg
11 43 1.2 0.2 L eso 4.5 Y N 13 1.0 0.6 L eso 2.3 Pos
12 43 1.25 0.6 R eso 16.7 N Y 20 1.0 1.0 R eso 4.6 Pos
13 67 0.8 0.6 L eso 5.0 Y N 8 0.8 0.8 L eso 4.6 Pos
14 82 0.9 0.2 R eso 16.7 N Y 54 1.0 0.8 R eso 2.3 Pos
15 34 1.0 0.5 R eso 4.6 Y N 10 1.0 0.6 R eso 4.6 Pos
16 67 1.0 0.5 R eso 4.6 N N 5 1.0 1.0 R eso 1.2 Neg
17 81 0.6 1.0 L eso 3.5 N N 37 1.0 0.6 L eso 3.5 Pos
18 34 1.25 1.0 R eso 23.8 N Y 50 1.0 0.6 R eso 4.6 Pos
19 43 1.0 0.1 L eso 2.0 Y N 6 1.0 0.6 L exo 0.6 Pos
20 89 1.0 0.5 L eso 4.6 Y N 7 0.8 0.8 L eso 3.2 Pos

DE, dominant eye; NDE, nondominant eye; SA, squint angle; R, right; L, left; eso, esotropia; exo, exotropia; y, yes; n, no; pos, positive; neg, negative.
OKN and Strabismus
5145
5146 Valmaggia et al. IOVS, December 2003, Vol. 44, No. 12

(seconds of arc)
Stereoacuity
TNO Test

240
60
120
60
60
120
240
60
240
60
60
120
60
60
15
VA at Time of
OKN Test
(NDE)

1.00
1.00
1.00
1.25
1.00
1.00
1.25
1.25
1.00
1.25
1.25
1.00
1.00
1.00
1.00
VA at Time of
OKN Test
(DE)

1.00
1.00
1.00
1.25
1.00
1.00
1.25
1.25
0.90
1.25
1.25
1.00
1.00
0.90
0.90
OKN Test
Age at

(y)

6
11
14
10
8
6
6
16
10
11
6
12
14
9
13

DE, dominant eye; NDE, nondominant eye; SA, squint angle; R, right; L, left; Alt, alternating; eso, esotropia; y, yes; n, no.
Occlusion
Therapy

FIGURE 1. Original eye movement recordings during monocular TN


N
N
N
N
N
N
N
N
N
N
N
N
N
Y
Y

and NT stimulation at a velocity of 45 deg/s of the right eyes of (A)


patient 14 with NB, (B) patient 1 with PB, (C) patient 8 with GB, and
(D) a normal 22-year-old subject.
Presentation
(Degrees)
SA at

19.3
21.9
20.9
15.2
26.7
15.2
19.3
16.7
19.3
28.0
15.2
16.7
19.3
20.0
16.7

0.05). In contrast, no difference was present for TN stimula-


tion. In the PB group, OKN gains were lower than in the
control group in both directions, for the deviating and the
nondeviating eye. This difference increased with increasing
stimulus velocity and was significant for TN and NT stimulation
at 60 deg/s in both eyes (P ⬍ 0.05). No significant differences
Presentation
Strabismus

were found between TN and NT asymmetry. In the GB group,


Form at

R eso
L eso
R eso
R eso
Alteso
L eso
R eso
R eso
L eso
Alteso
Alteso
Alteso
Alteso
R eso
R eso

there were no significant differences compared with the con-


trol group.
The percentages of subjects falling outside of the 95% con-
fidence interval of the asymmetry index for control subjects are
listed in Table 5, for dominant and nondominant eyes at the
four stimulus velocities. A large percentage of subjects in the
Measured

(NDE)
First

1.00
0.50
1.25
0.80
1.00
0.30
0.90
1.00
0.80
1.00
0.63
0.90

0.50
0.80
VA

1.0
TABLE 3. Details of Patients with Good Binocularity

TABLE 4. The Percentage of Patients with OKN Gain Below Normal


95% Confidence Interval

TN (deg/s) NT (deg/s)
Measured

(DE)
First

1.00
0.50
1.25
0.80
1.00
0.30
0.90
0.80
0.80
1.00
0.63
0.90
0.80
0.50
0.80
VA

15 30 45 60 15 30 45 60

No binocularity
DE 0.0 5.0 10.0 0.0 60.0 55.0 60.0 60.0
NDE 0.0 0.0 0.0 0.0 80.0 60.0 70.0 55.0
Diagnosis

Poor binocularity
Age at

(mo)

24
32
28
36
19
35
27
36
29
18
32
27
22
29
34

DE 5.0 10.0 20.0 10.0 25.0 10.0 10.0 5.0


NDE 15.0 20.0 25.0 10.0 25.0 25.0 15.0 20.0
Good
binocularity
DE 0.0 0.0 13.3 0.0 13.3 0.0 6.7 0.0
Patient

NDE 6.7 0.0 6.7 0.0 0.0 0.0 6.7 0.0


10
11
12
13
14
15
1
2
3
4
5
6
7
8
9

DE, dominant eye; NDE, nondominant eye.


IOVS, December 2003, Vol. 44, No. 12 OKN and Strabismus 5147

significant correlation was found between the age of detection


of strabismus and OKN asymmetry at the four stimulus veloc-
ities for dominant eyes (P ⬍ 0.05 for 15 and 30 deg/s, P ⬍
0.005 for 45 deg/s, and P ⬍ 0.0005 for 60 deg/s) and nondomi-
nant eyes (P ⬍ 0.01 for 15 and 30 deg/s, P ⬍ 0.001 for 45
deg/s, and P ⬍ 0.0001 for 60 deg/s). However, when the
correlation between age and asymmetry factor was analyzed
within groups (i.e., NB and GB separately), there was no
significant correlation.
In the NB group, at higher stimulus velocities, patients with
DVD showed larger OKN asymmetry than patients without
DVD, in dominant and nondominant eyes, but differences were
not significant (Fig. 4). No correlation was found between
OKN asymmetry and visual acuity at the time of onset or of
OKN measurement.

DISCUSSION
In summary, we found that only subjects with NB showed
significant OKN asymmetry with preference for TN stimulation
rather than NT stimulation, in dominant and nondominant
eyes. Asymmetries were more frequent in nondominant eyes.
Subjects with PB did not have a significant preference for TN
stimulation, although the OKN gain of these subjects was
reduced for both stimulus directions and in both eyes. Subjects
with GB had normal mean OKN gains and showed no signifi-
cant preference in either stimulation direction. Larger asym-
metry factors were correlated with younger age at detection of
strabismus only if NB and GB were grouped together.
In the literature, OKN asymmetries have usually been ana-
lyzed in relation to onset of strabismus by comparing subjects
with early-onset with those with late-onset strabismus. The age
limit used to define early-onset strabismus varies in different
reports from 6 months,12 to 12 months,13 and up to 24
months.14 Several studies5,10 –14 have found a greater preva-
lence of asymmetry with earlier onset of strabismus. In all these
studies, asymmetries were present in the dominant eyes, but
were less common than in the nondominant eyes. Schor et al.5
found that monocular OKN asymmetries could be used to
predict whether esotropia had occurred before or after the first
FIGURE 2. Mean ⫾ SD of gains for the four different groups of subjects
at (A) 15, (B) 30, (C) 45, and (D) 60 deg/s for nondominant and
year of life. In our study, we found asymmetry in 75% to 85%
dominant eyes. For control subjects, gains of the right eyes are plotted of the nondominant eyes and in 50% to 65% of the dominant
in both the left and right columns. eyes in the NB group, depending on stimulation velocity.
Strabismus onset was documented as occurring before or at 18
months of age. In the PB group, up to 30% of subjects had
asymmetrical OKN with TN preference; however, some sub-
NB group showed significant asymmetries, with preference for jects also showed NT preference, reflecting a wider variation of
TN stimuli rather than NT stimuli. This TN preference was data. Consequently, only the NB group showed significantly
more frequently seen in the nondominant than in the dominant
eye at all velocities. In the PB group, the asymmetry factor was
also outside normal limits more frequently in the nondominant TABLE 5. The Percentage of Patients with Asymmetric OKN
than in the dominant eye. However, asymmetries were ob-
served with preference to both TN and NT directions. Asym- TN>NT (deg/s) NT>TN (deg/s)
metries also occurred in both directions (TN and NT) for
dominant and nondominant eyes in GB. This pattern of asym- 15 30 45 60 15 30 45 60
metry factors falling on both sides of the normal confidence
interval reflect the wider variation of the data in the patients No binocularity
with PB and GB than in the control subjects. DE 65.0 55.0 50.0 55.0 0.0 0.0 5.0 10.0
The PB group was divided into patients who had no surgery NDE 80.0 85.0 75.0 80.0 0.0 0.0 0.0 0.0
and those who had surgery. No significant differences in gain Poor binocularity
or asymmetry factors were found between the two subgroups. DE 15.0 5.0 5.0 5.0 0.0 0.0 5.0 25.0
NDE 20.0 30.0 10.0 25.0 10.0 10.0 5.0 25.0
Figure 3 represents the relationship between the age when Good
strabismus was detected and the asymmetry index for the NB binocularity
and GB groups at different stimulation velocities. The PB group DE 33.3 13.3 6.7 6.7 13.3 26.7 6.7 26.7
was not included in this analysis, because the detection of NDE 26.7 20.0 6.7 20.0 20.0 6.7 6.7 26.7
strabismus was unlikely to correlate with the time of onset of
squint, because of the small squint angle in these subjects. A DE, dominant eye; NDE, non-dominant eye.
5148 Valmaggia et al. IOVS, December 2003, Vol. 44, No. 12

FIGURE 3. Asymmetry index of non-


dominant and dominant eyes versus
age of detection of strabismus for pa-
tients with NB and those with GB at
the four stimulus velocities. An asym-
metry factor of 0.5 corresponds to
equal gain for TN and NT stimula-
tion. Larger asymmetry factors reflect
TN preference and smaller ones NT
preference.

asymmetrical OKN as a group. Most studies have used ages observers with strabismus at an older age, as in our study,
estimated retrospectively for onset of strabismus. However, it may help differentiate between the normal maturation pro-
is impossible to determine the exact time of onset of strabis- cesses for OKN symmetry, and its alteration by strabismus.
mus by these means, because onset may remain long undetec- Our data were similar to those of Steeves et al.14 who
ted by lay people before clinical examination. Also, a slow investigated patients older than 8 years with early-onset
increase in squint angle may lead to a wrong assumption of the strabismus.
time of onset. The difficulty in determining the exact time of Westall et al.17 found no clear relation between stereop-
onset of strabismus retrospectively may explain discrepancies sis and OKN deficits. Wright18 and Aiello et al.19 examined
between findings. three children who underwent unusual early surgery for
We found that OKN asymmetries were consistently but not esotropia at 3 and 4 months of age. Although these children
significantly larger in patients with DVD than in subjects with- eventually had normal stereoacuity, they had asymmetrical
out DVD (probably due to the small sample size within the NB OKN. In contrast to these findings, van Hof-van Duin et al.20
group) and appeared to increase with increasing stimulus ve- measured OKN in six normal, six stereodeficient, and six
locities. Because DVD is a strong indicator of early-onset stra- stereoblind subjects. OKN was clearly asymmetric in pa-
bismus5 this may also indicate a relation between earlier onset tients with no stereovision, but symmetric in subjects with
of strabismus and asymmetric OKN. rudimentary stereovision. This is in agreement with our
OKN responses have been reported as asymmetrical in study. Patients with PB in our study had peripheral fusion
normal children between 3 and 24 months of age3,24,25 (Roy and/or stereopsis, but central scotomas in the nondominant
MS, et al. IOVS 1987;28:ARVO Abstract 18; Lewis TL, et al. eye when tested binocularly with the Bagolini test. They had
IOVS 1991;32:ARVO Abstract 1437). Consequently, testing small squint angles, which should easily be fused if normal
IOVS, December 2003, Vol. 44, No. 12 OKN and Strabismus 5149

Visual acuities, measured at the time of strabismus detection


or at the time of OKN measurement, were not correlated to
OKN asymmetries. At the time of OKN measurement, most of
our patients had relatively good visual acuity, some after oc-
clusion therapy.
Patients in the GB group had the potential of stereovi-
sion, but had strabismus associated with diplopia, or signs of
diplopia. Their mean OKN gain was similar to normal sub-
jects. The only difference was that more subjects had an
asymmetry factor out of normal range favoring either TN or
NT stimulation. Larger OKN variability reflects a less precise
OKN generation in the GB group. This may be associated
with a less robust binocular system, causing sudden onset
of strabismus at a later age, although binocular vision has
developed.
In conclusion, our study shows that OKN gain and asym-
metry are associated with the development of binocular vision.
OKN investigation may be helpful to identify patients with
binocularity or binocular potential in strabismus.

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