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C L I N I C A L A N D E X P E R I M E N T A L

OPTOMETRY
cxo_753 410..420

RESEARCH PAPER

A novel apparatus for interocular interaction evaluation in


children with and without anisometropic amblyopia

Clin Exp Optom 2012; 95: 410–420 DOI:10.1111/j.1444-0938.2012.00753.x

Xin Jie (Angela) Lai*§ PhD MOptom Background: Dichoptic visual stimulation may be achieved using shutter goggles and
Jack Alexander* PhD FAAO mirror systems. These methods vary in their feasibility for use in children. This study
Ming Guang He† MD PhD aims to investigate the feasibility of use of a simple trial frame-based system to evaluate
Zhi Kuan Yang†¶ MD PhD interactions in children.
Catherine Suttle* PhD MCOptom Methods: Low contrast acuity, contrast sensitivity and alignment sensitivity were mea-
* School of Optometry and Vision sured in the non-dominant eye of 10 normally-sighted children, 14 anisometropic
Science, The University of New South children without amblyopia and 14 anisometropic amblyopic children (aged
Wales, Sydney, Australia 5–11 years) using goggles and a trial frame apparatus (TFA). The dominant eye was

Zhongshan Ophthalmic Centre, either fully or partially occluded. The difference in visual functions in the non-dominant
Guangzhou, China eye between the full and partial occlusion conditions was termed the ‘interaction index’.
§
Smith-Kettlewell Eye Research Institute, Agreement between the TFA and goggles in terms of visual functions and interactions
San Francisco, CA, USA was assessed in anisometropic children with and without amblyopia using the Bland-

Changsha Aier Eye Hospital, Hunan, Altman method and t-test. Training sessions allowed subjects to become accustomed to
China the systems and tasks. The duration of training, the number of breaks requested by
E-mail: xinjie.lai@gmail.com subjects and their willingness to attend further experiments were recorded in 10 sub-
jects from each group and were compared between groups and between systems.
Results: Both Bland-Altman and t-test methods indicated acceptable agreement between
the TFA and goggles in visual function and interaction measures (p > 0.05), except for
contrast sensitivity measured in anisometropic children without amblyopia (p = 0.042).
For all subject groups, contrast sensitivity training was significantly longer using goggles
than using the TFA (p ⱕ 0.001). Significantly more breaks were requested in acuity and
contrast sensitivity testing, when goggles were used than when the TFA was used (p <
Submitted: 26 March 2011 0.045). Anisometropic children without amblyopia showed a significantly greater willing-
Revised: 8 January 2012 ness to attend more experiments using the TFA than using goggles (p = 0.025).
Accepted for publication: 18 January Conclusion: The TFA may be a useful tool in studies of interactions in amblyopes,
2012 particularly in studies of children’s vision.

Key words: amblyopia, children, contrast sensitivity, vision, visual acuity

Dichoptic visual masking occurs when a light’, ‘masking a pattern by light’ and and the mask are processed binocularly
target is presented to one eye and a mask ‘masking a pattern by a pattern’.1 The and the mask can affect the perception of
is presented to the fellow eye. The stimu- mask may be presented either coincident the target, resulting in an increment or a
lus and masking configurations may take with or adjacent to the stimulus.2–10 In decrement in visual function thresholds of
various forms, including ‘masking light by the normal visual system, the target the tested eye.2,3,8–10 These masking effects

Clinical and Experimental Optometry 95.4 July 2012 © 2012 The Authors
410 Clinical and Experimental Optometry © 2012 Optometrists Association Australia
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

in humans, about one-third of cases of


amblyopia are caused by anisometropia,
one-third by strabismus and one-third by a
combination of both.18,19 Deprivation due
to conditions such as congenital cataracts
can also lead to amblyopia.20
Numerous studies have demonstrated
that interocular interactions differ be-
tween amblyopic and normal observers.
For example, binocular summation is
reduced or absent in amblyopes.21,22 Hol-
opigian, Blake and Greenwald23 found that
stereoacuity and binocular summation are
absent at high spatial frequencies only,
while Hood and Morrison24 found a higher
level of binocular contrast summation in
amblyopes with binocular single vision
than in normal observers, for both low and
high spatial frequencies. Baker and col-
leagues25 found that binocular contrast
summation is normal in amblyopes when
contrast sensitivity is normalised across the
amblyopic and the fellow eyes. Studies by
Sengpiel and Blakemore26, and Smith and
colleagues27 have demonstrated inhibitory
interaction in animals with amblyopia and
Figure 1. The trial frame apparatus (TFA), 1.0 mm pinhole, opaque
Vedamurthy and colleagues2 found signifi-
occluder and the star-shaped occluder used with the TFA. The
cant inhibitory interaction in anisome-
star-shaped occluder was made using a +5.00 DS trial lens with four
tropic amblyopic adults.2 Most of these
strips of 5.0 mm wide black masking tape. The opaque occlusion at
findings suggest that abnormal interac-
the centre of the star-shaped occluder was 13 mm in diameter.
tions occur in anisometropic amblyopia.
Studying interactions in anisometropic
amblyopes may provide information on
are underpinned by interactions in the pinhole aperture (1.0 mm in diameter) visual processing in these subjects and the
visual system that take place between placed in front of the tested eye and a mechanisms underlying this disorder.
signals from the two eyes, known as partial occluder placed in front of the Comparison between interactions in
interocular interactions. In dichoptic non-tested eye. The occluder was made anisometropes with and without amblyo-
masking studies, the impact of the using a +5.00 DS trial lens, on which four pia may be informative because both
masking stimulus on perception of the test strips of 5.0 mm wide opaque black groups have significant differences in
stimulus is assessed. Comparison between masking tape were placed to form a refractive error between eyes but only one
visual functions measured under dichop- ‘star-shaped’ occlusion (Figure 1). Visual of these groups has developed amblyopia.
tic and monocular viewing conditions function and interocular interaction mea- The aim of this study is to investigate the
allows the nature and the strength of surements made using this method were feasibility of use of the TFA as a means of
interocular interactions to be investigated. found to agree with those made using studying interocular interactions in chil-
Mirror or prism devices and shutter shutter goggles in children and adults with dren with and without anisometropic
goggles have been used in dichoptic normal vision.14 amblyopia. Specifically, to investigate:
masking studies;3,11–13 however, equipment Amblyopia is often known as ‘lazy eye’. 1. Agreement in visual function and
of this kind may not be feasible for use in It refers to a disorder of the visual system interocular interaction measures
some populations.14 For this reason, a that is characterised by unilateral or between the TFA and shutter goggles
simple and portable viewing system, a ‘trial bilateral loss of visual acuity without in anisometropic children with and
frame apparatus’ (TFA) was designed and pathology.15 Anisometropia, which has a without amblyopia and
validated in a previous study.14 The TFA prevalence of two to six per cent in school 2. The feasibility of use of the TFA as a
consisted of a trial frame adjusted to children,16,17 is one of the major causes of viewing system to evaluate interactions
the individual’s interpupillary distance, a amblyopia. Previous studies indicate that in children.

© 2012 The Authors Clinical and Experimental Optometry 95.4 July 2012
Clinical and Experimental Optometry © 2012 Optometrists Association Australia 411
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

(a) Anisometropic amblyopic children


Subject Sex Age Prescription VA (logMAR) IDVA Stereoacuity
(years) (logMAR) (arcsec)
Right eye Left eye DE NDE

1 M 6.4 plano +3.00 -0.2 0.1 0.3 50


2 M 6.5 +0.25 +6.50/-2.00 ¥ 180 -0.1 0.5 0.6 400
3 M 7.4 +6.25 +7.00 0.1 0.3 0.2 400
4 F 8.3 0/-1.75 ¥ 95 -1.00 0 0.1 0.1 30
5 F 8.4 +2.25/-0.50 ¥ 170 +0.50/-1.00 ¥ 10 -0.2 0.2 0.4 70
6 M 8.4 -4.00/-2.25 ¥ 50 -2.50/-0.50 ¥ 170 0 0.15 0.15 50
7 F 8.5 +0.75/-0.50 ¥ 130 +3.75 0 0.5 0.5 100
8 F 8.6 +4.25/-0.50 ¥ 155 +0.25/-0.50 ¥ 15 -0.1 0.3 0.4 70
9 F 9.1 +4.50/-1.00 ¥ 160 plano -0.1 0.2 0.3 50
10 M 9.2 +0.50 +7.00/-2.00 ¥ 45 -0.2 0.2 0.4 400
11 F 9.3 -4.50/-1.50 ¥ 10 -1.25 -0.2 0.4 0.6 50
12 M 9.5 -3.25/-0.75 ¥ 170 plano 0 0.15 0.15 30
13 M 9.8 -6.00/-1.75 ¥ 40 -4.25/-1.00 ¥ 130 0 0.1 0.1 40
14 M 10.1 +2.50/-2.50 ¥ 180 +4.50/-2.50 ¥ 180 0 1.0 1.0 400

(b) Anisometropic children without amblyopia


Subject Sex Age Prescription VA (logMAR) Stereoacuity
(years) (arcsec)
Right eye Left eye DE NDE

1 M 7.1 -1.75 -1.75/-1.00 ¥ 85 0 0 40


2 F 7.2 0/-3.25 ¥ 175 0/-2.25 ¥ 5 0 0 70
3 F 8.3 -2.50 -2.75/-1.25 ¥ 165 -0.1 -0.1 40
4 M 8.3 -2.25 -1.00 -0.2 -0.2 30
5 F 8.8 -4.75/-0.50 ¥ 180 -3.25/-0.50 ¥ 170 0 0 30
6 F 8.9 -0.25 -1.50 0 0 30
7 M 9.0 -6.50 -4.75/-0.50 ¥ 30 0 0 30
8 F 9.3 -5.00/-1.50 ¥ 35 -6.25/-2.00 ¥ 150 0 0 40
9 F 9.3 +0.50 +1.25/-0.75 ¥ 155 -0.1 -0.1 30
10 F 9.3 +1.00/-1.00 ¥ 165 +2.00/-2.25 ¥ 175 -0.2 -0.2 140
11 F 9.6 -12.50 -10.50 0 0 30
12 F 9.7 -4.50 -4.50/-1.00 ¥ 160 0 0 40
13 F 9.8 +3.00/-0.75 ¥ 180 -1.00/-0.50 ¥ 175 0 0 140
14 M 9.8 -3.75 -2.25/-0.75 ¥ 160 0 0 30

Table 1 Clinical characteristics of anisometropic children with [a] and without [b] amblyopia. VA, visual acuity measured in the
screening program (using a high contrast E chart); DE, dominant eye; NDE, non-dominant eye; IDVA, interocular difference in high
contrast acuity. No monocular suppression or diplopia was reported in any of these subjects (Worth four dot test).

⫾ 1.5 years; seven male, three female), 14 three subject groups are referred to as
METHODS
anisometropic children without amblyo- ‘controls’, ‘anisometropes’ and ‘ambly-
pia (mean age: 8.8 ⫾ 0.8 years; six male, opes’, respectively. All subjects were
Subjects eight female) and 14 anisometropic recruited through a school-based screen-
Subjects were 5–11 years old, including 10 amblyopic children (mean age: 8.8 ⫾ ing program in Huadu, China. Table 1
normally sighted children (mean age: 9.2 1.0 years; eight male, six female). These shows the clinical characteristics of the

Clinical and Experimental Optometry 95.4 July 2012 © 2012 The Authors
412 Clinical and Experimental Optometry © 2012 Optometrists Association Australia
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

anisometropes and amblyopes. Ethical 2. visual acuity for amblyopes: 0.1 logMAR cover the non-tested eye, with a trial frame
approval for the present study was or worse in one eye and 0.1 logMAR holding the subject’s refractive correction
obtained from the Human Research or better in the other eye, with an over it (if needed) and with the shutter
Ethics Committee of the University of New interocular difference of 0.1 logMAR goggles outermost. In the partial occlu-
South Wales in Australia and the ethics or more sion condition, subjects wore a trial frame
committee of the Zhongshan Ophthalmic 3. interocular difference in spherical with refractive correction (if needed) and
Center in China. Written, informed refractive error of 0.75 DS or more for the goggles, with no eye-patch.
consent was obtained before recruitment hyperopic children, 1.25 DS or more
from parents of all subjects. Assent was for myopic children and cylindrical TRIAL FRAME APPARATUS
obtained from each subject. This study refractive error of 1.00 DC or more for The design and validation of the TFA
adhered to the tenets of the Declaration of children with astigmatism (refractive (Figure 1) are described elsewhere.14 In
Helsinki. errors were defined using negative both full and partial occlusion, a pinhole
A series of vision screening tests was cylinder).32 aperture (1.0 mm in diameter) was placed
conducted as part of the screening in front of the tested eye. The non-tested
program, including a clinical acuity test Apparatus eye was covered using the star-shaped
for distance (a high-contrast E chart at Visual stimuli were generated using a VSG occluder in the partial occlusion condi-
5 m), cover test for distance and near 2/5 graphics card (Cambridge Research tion and using an opaque cover for full
(with refractive correction if needed; Systems, Rochester, UK) externally con- occlusion. The star-shaped occluder con-
correction was prescribed by one of the nected to an HP 8530P laptop computer sisted of one opaque black masking tape at
authors [XJL] based on both cycloplegic and were displayed on a gamma-corrected horizontal, one at vertical and the other
[1% cyclopentolate] and non-cycloplegic 21-inch Trinitron Sony GDM-F520 cathode two at 45° and 135°. Depending on the
refractions28,29 and was applied through- ray tube monitor. The refresh rate was vertex distance, the opaque occlusion at
out this study), binocularity (Worth four 120 Hz. The mean room illuminance was the centre of the star-shaped occluder
dot test at 6 m), stereopsis (Randot stere- 4.78 ⫾ 2.76 Lux (Konica Minolta T-10 illu- blocked out between 22° and 24° of the
oacuity test at 40 cm), sighting dominance minance meter). Three visual functions central visual field of the non-tested eye
test30,31 and fundus examination, includ- were measured in each subject, namely, but light transmission from the periphery
ing assessment of central fixation (direct low contrast acuity (-0.20 Weber contrast), was allowed.14 The pinhole transmits
ophthalmoscopy). No ocular deviation or contrast sensitivity and alignment sensitiv- approximately 10° of central field to the
eccentric fixation was found in any of the ity. Two viewing systems were used, namely, tested eye and the field more peripheral to
subjects. ferro-electric shutter goggles (FE-1, Cam- this was vignetted. Thus, in partial occlu-
Subjects were included only if they had bridge Research Systems) and the TFA. sion, the view consists of the target pre-
no history of ocular trauma and/or ocular Using each of these viewing systems, each sented to the tested eye coincident with
pathology, no systemic disease (by self- visual function was measured under both the central occlusion of the non-tested
report), no strabismus (based on cover full and partial occlusion conditions (see eye. While the experiments were con-
test), no previous or current treatment of below). For anisometropes and amblyopes, ducted in a darkened room, even with a
anisometropia and/or amblyopia (refrac- refractive error was always corrected using pupil diameter of 8.0 mm, the field of view
tive correction or occlusion), no eccentric trial lenses. through the pinhole remained below 20°
fixation and they met the following and always below the peripheral field
criteria: SHUTTER GOGGLES angle of the star-shaped occluder.
The shutter goggles were synchronised
CONTROLS with the monitor so that alternate frames Stimuli and experimental tasks
1. Uncorrected vision of 0.0 logMAR or were presented to each eye (for example, A training session was conducted for each
better in each eye, with an interocular odd-numbered frames to right eye, even- subject before the main experiments, to
difference of less than 0.1 logMAR numbered frames to left eye). Thus, each allow the subject to become accustomed to
2. spherical and cylindrical refractive eye viewed the stimuli at a refresh rate of the tasks with each viewing system. The
error of 0.50 D or less for distance 60 Hz. The background luminance of the stimuli and tasks described here apply to
3. stereopsis of equal to or better than 40 monitor was fixed at 170 cd/m2 and this the main experiments. Any differences
seconds of arc (arcsec). level was reduced to about 21 cd/m2 at for the training sessions are indicated in
each eye by the goggles. The goggles were Procedures.
ANISOMETROPES AND AMBLYOPES worn using an elasticated strap and were On each trial, a central target was pre-
1. Visual acuity for anisometropes: held in place by an assistant to reduce sented to the tested eye only for a period of
0.1 logMAR or better in each eye, with their weight and to minimise discomfort. 140 ms (400 ms in training sessions), to
an interocular difference of less than In the full occlusion (monocular) condi- minimise the impact of eye movements.33
0.1 logMAR tion, an opaque eye-patch was used to With full occlusion, the non-tested eye was

© 2012 The Authors Clinical and Experimental Optometry 95.4 July 2012
Clinical and Experimental Optometry © 2012 Optometrists Association Australia 413
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

per degree [cpd]) subtending 3.5° at a


viewing distance of 2 m, with the standard
deviation of the Gaussian envelope 0.65°.
Alignment sensitivity was assessed with
three Gabor patches at 65 per cent Mich-
elson contrast (vertical, at six cycles per
degree, presented at a viewing distance of
1 m) with the upper and lower patches in
vertical alignment and the central patch
displaced to the left or right relative to this
alignment on each trial.

SQUARE PARTIAL OCCLUSION


The square partial occlusion was at -0.78
Weber contrast, subtending 2.3°, 3.5° and
9.5° of the visual field for acuity, contrast
sensitivity and alignment sensitivity tests,
respectively. This form of partial occlusion
applied only to the shutter goggles.

FUSION LOCK
The fusion lock, intended to maintain in
the dichoptic, partial occlusion condi-
tions, was a ring target at -0.78 Weber con-
trast with a width of 0.1°, subtending 4° for
acuity, 8° for contrast sensitivity and 15°
for alignment sensitivity.

SUPPRESSION MARKERS
Suppression markers were four lines, two
presented to each eye (subtending 0.3°,
2.5° and 1° at locations 6°, 10° and 19.5° in
the periphery for acuity, contrast sensitiv-
Figure 2. Examples of stimuli presented to the tested eye [i] and the non-tested eye [ii] ity and alignment sensitivity measure-
with partial occlusion for the acuity [A], contrast sensitivity (central target at 4 cpd is ments, respectively). These markers were
presented here, virtual target was at 6 cpd) [B] and alignment sensitivity (central target presented in the goggle square partial
at 2 cpd is presented here, virtual target was at 6 cpd) [C] measurements when shutter occlusion condition only.
goggles were used as a viewing system The experimental tasks were identical
in the training and the main experiments.
These tasks were:
1. in the acuity test, to indicate by point-
fully occluded, while with partial occlu- (not with the TFA) in partial occlusion ing the orientation of the E target
sion, the non-tested eye was masked with only to check for suppression of either eye. 2. contrast sensitivity was measured using
either a square low-luminance patch a temporal two-alternative forced
(viewed via shutter goggles and referred to CENTRAL TARGET choice method, in which subjects ver-
as ‘square partial occlusion’; Figure 2) or a Acuity was assessed with a single letter E bally reported whether the Gabor
star-shaped occluder (viewed via the TFA; presented at one of four possible orienta- patch was presented in interval ‘one’ or
Figure 1). A fusion lock was constantly pre- tions (right, left, up or down) at a viewing ‘two’ after each trial and
sented to both eyes. It was visible to the distance of 4 m. The letter was constructed 3. in the alignment sensitivity test, the task
tested eye only in the full occlusion condi- in a 5 ¥ 5 grid, in which each stroke and was to point to the offset direction (left
tion when the shutter goggles were used gap was one-fifth of the dimension of the or right) of the central Gabor patch.
and in both viewing conditions when the square grid. All responses were input to the program
TFA was used. Suppression markers (see The contrast sensitivity test consisted of a by the examiner (author XJL). No feed-
below) were used with the shutter goggles circular Gabor patch (vertical, at six cycles back was given.

Clinical and Experimental Optometry 95.4 July 2012 © 2012 The Authors
414 Clinical and Experimental Optometry © 2012 Optometrists Association Australia
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

Procedures In both training and main experiments, the box to tell us which game you would
In the training session, the dominant eye an ‘unforced-choice method’36 (allowing like to play and cross the one you don’t
of each subject was tested in all three visual ‘don’t know’ answers) was used in like. Check both of them if you like both
functions with partial occlusion only, using acuity and contrast sensitivity tests due of them and cross both of them if you
both viewing systems (all tests were con- to long experimental duration (up to don’t like either of them.’
ducted in a pseudo-random order). In eight minutes), to enhance subjects’ co- Response options were: ‘(A) Glasses
these sessions, a two-down one-up (2/1) operation and to increase the likelihood with spider web or (B) Diving mask’, rep-
single staircase method was used for acuity of test completion.36,37 Although subjects resenting (A) TFA and (B) shutter
and contrast sensitivity testing, while a 1/1 were not forced to give a response to each goggles, respectively.
double staircase method was used for trial, they tended to give as many answers
alignment sensitivity testing. Start levels as they could, with an average of only one
were based on previous findings to ensure ‘don’t know’ answer given by each subject Data analysis
subjects could easily detect the stimuli, and during each test. An ‘incorrect’ response
the step sizes were sufficiently small to was recorded for the ‘don’t know’ answers. THRESHOLDS AND INTERACTION INDEX
ensure the stimuli were always supra- A ‘forced-choice method’38 was used in the In the single and double staircase
threshold during training.2,34,35 The square alignment sensitivity test to reduce the methods, trials up to the first reversal on
partial occlusion used with shutter goggles variability of the subjects’ judgment of each track were excluded. In the acuity
in this training session subtended 3°, 5° alignment. and contrast sensitivity tests, the mean of
and 7° in the acuity, contrast sensitivity and A game-like atmosphere39 was mid-points of peaks and valleys of the
alignment sensitivity tests, respectively. employed. At the beginning of the experi- remaining reversals were taken to repre-
Subjects who could give 10 consecutively ments, the child was asked to add his/her sent threshold. In the alignment sensitivity
correct answers were regarded as having name to a list of ‘challengers’ pasted on a test, the standard deviation (SD) of the
passed the training for each visual function wall and was told that he/she was going to mid-points was taken to represent the vari-
and viewing system. Duration of training play three games (three visual function ability of a subject’s judgment of align-
sessions for each visual function test were tests) that day. Each game included two ment and the reciprocal of this was
recorded using a stopwatch in 10 subjects stages (two viewing conditions) and he/ recorded as alignment sensitivity.
of each group, for the TFA and the she was allowed to paste a little red flag The difference in non-dominant eye
goggles, respectively. after his/her name when he/she passed a visual function between the full and
The main experiments were conducted stage of a game. At the end of each day, partial occlusion is termed the ‘interac-
within three days of the training. The the child who had most flags would be the tion index’. As a threshold measure, the
three visual functions were measured in ‘champion of red flags’. The examiner acuity ‘interaction index’ was calculated
the non-dominant eye only in each (XJL) frequently praised and encouraged by the following normalising function:
subject. Four testing conditions were used: the subjects throughout the experiments
1. shutter goggles with full occlusion and words were carefully used in experi- Acuity(Partial ) - Acuity(Full )
Interaction Index =
2. shutter goggles with partial occlusion mental task instructions to ensure they Acuity(Partial ) + Acuity(Full )
3. trial frame with full occlusion and were easily understood by the subjects.
4. trial frame with partial occlusion. Subjects were tested in groups of two As sensitivity measures, contrast and
Different viewing systems were tested during the main experiments and thus alignment sensitivity interaction indices
on separate days and all tests using each they were tested in turns and a break was were calculated as follows:
viewing system were conducted in a given after each visual function test under
pseudo-random order. Initially, individual one viewing condition. Subjects were also Interaction Index
start level was determined using a 1/1 allowed to take breaks by request at any Sensitivity(Full ) - Sensitivity(Partial )
=
single staircase method in the acuity and time during a test. The number of breaks Sensitivity(Full ) + Sensitivity(Partial )
contrast sensitivity tests and a 1/1 double requested by subjects (excluding those
staircase method in the alignment sensi- given after each visual function test) was For each visual function measurement,
tivity test. Following this, thresholds were recorded in 10 subjects of each group, for a positive index value indicates poorer
measured using a 2/1 double staircase the TFA and shutter goggles respectively. non-dominant eye visual function (stron-
method in the acuity and contrast sensi- After all tests, 10 subjects of each group ger inhibitory impact) with partial relative
tivity tests and a 1/1 double staircase were given a slip of paper with one ques- to full occlusion of the dominant eye. The
method in the alignment sensitivity test. tion and two response options. They were interaction index of each visual function
The step sizes were 0.08 logMAR, 3.5 dB asked to mark one or both of the option evaluated using the TFA was compared
and 1.5 arcmin in the acuity, contrast boxes. The question was: between anisometropes and amblyopes
sensitivity and alignment sensitivity tests, ‘Do you want to play some more games using the repeated measures analysis of
respectively. with us in the next semester? Please check variance (ANOVA).

© 2012 The Authors Clinical and Experimental Optometry 95.4 July 2012
Clinical and Experimental Optometry © 2012 Optometrists Association Australia 415
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

Agreement between shutter goggles and FEASIBILITY OF THE SHUTTER between shutter goggles and the TFA in all
the trial frame was examined for ani- GOGGLES AND TRIAL FRAME three visual function measures and in
sometropes and amblyopes, in terms of: The duration of each subject training their interaction index evaluations. The
1. absolute measures of each visual func- session, the number of breaks requested t-test indicated that in each visual func-
tion with partial occlusion and by subjects in the main experiments and tion, interaction index was not signifi-
2. interaction index for each of these the willingness to attend further experi- cantly different when evaluated using
three visual functions. Two methods ments were recorded in 10 subjects from shutter goggles or the trial frame (p >
were used to test for agreement: the each group to assess the feasibility of the 0.05). Absolute measures of acuity and
paired-samples t-test and the Bland- two viewing systems. Based on the chil- alignment sensitivity also did not differ sig-
Altman method.40 The Bland-Altman dren’s answers to the question of willing- nificantly between the two viewing systems
method includes the following four ness to attend further experiments, a tick (p > 0.05). Contrast sensitivity was not
steps: to a viewing system was marked as ‘1’, significantly different between viewing
1. The means and the differences while a cross to a viewing system was systems in the amblyopes (p > 0.05) but it
between measures using two viewing marked as ‘0’. For each test of visual func- was significantly lower (poorer) when
systems were calculated for each tion, these scores, duration of training and measured using the trial frame than using
subject, the number of breaks requested by sub- goggles in the anisometropes (p = 0.042).
2. the differences were plotted as a func- jects were each compared among the Acuity interaction index evaluated using
tion of the means, three groups of subjects for data obtained the trial frame was significantly higher in
3. the mean and standard deviation of the using the trial frame and shutter goggles, amblyopes than in anisometropes (F1,13 =
differences were calculated and respectively, using the one-way ANOVA or 5.000, p = 0.044) but there was no signifi-
4. the lower and upper ‘limits of agree- the Kruskal-Wallis analysis of variance and cant difference between these two groups
ment’ (LOA) were calculated: were each compared between the TFA and in contrast sensitivity (F1,13 = 0.025, p >
shutter goggles using the repeated mea- 0.05) or alignment sensitivity (F1,13 = 2.483,
LOA = Mean difference ± 1.96 × SD sures ANOVA or the Wilcoxon signed- p > 0.05) interaction index. The interac-
rank test. tion index evaluated using shutter goggles
where
is discussed elsewhere.41

Mean difference =
∑ (TFA - Shutter goggles ) RESULTS
n Feasibility of use of the shutter
goggles and the trial frame
1 n ⎡(TFA - Shutter goggles )i ⎤
2 Visual functions and interocular The training duration of each visual func-
SD = ∑
n i =1 ⎢⎣ - Mean difference ⎥⎦
interactions in anisometropes tion for each group is presented in
and amblyopes Figure 5. No significant difference was
n = number of subjects For anisometropes and amblyopes, mea- found among subject groups in any mea-
The trial frame and shutter goggles sures of visual function with partial occlu- surement of visual function, using either
were considered to show very good agree- sion using the trial frame and shutter the TFA (acuity: c2[2] = 2.754; contrast
ment if: goggles are presented in Figure 3. The sensitivity: c2[2] = 5.292; alignment sensi-
1. ninety per cent of the differences (n = ‘interaction indices’ of each visual func- tivity: F2,27 = 0.263; p > 0.05) or shutter
14) between the goggles and the trial tion evaluated using the TFA and shutter goggles (acuity: c2[2] = 4.055; contrast
frame were within the two limits of goggles are presented in Figure 4. High sensitivity: F2,27 = 3.021; alignment sensitiv-
agreement and inter-individual variation was found in all ity: F2,27 = 0.477; p > 0.05). For all three
2. the standard deviation of the differ- three visual functions and in interaction groups of subjects, the durations of train-
ences was less than the SD of the results index of these visual functions in both ani- ing sessions for acuity (Z = -0.930, p > 0.05)
(visual function or interaction index) sometropes and amblyopes. The limits of and alignment sensitivity (Z = -0.154, p >
obtained using the goggles. agreement and the number of subjects 0.05) tests were not significantly different
They were considered to show lower but showing differences beyond these limits when using the trial frame and the goggles
acceptable agreement if the SD of the dif- and the results of agreement assessment as viewing systems. The training sessions
ferences was more than the SD of the between these two viewing systems (Bland- for contrast sensitivity testing were signifi-
results obtained using the goggles but Altman and t-test methods) are shown in cantly longer using goggles than using
equal to or less than 1.96 ¥ SD of the Table 2. The agreement between these the trial frame in all groups of subjects
results obtained using the goggles. They two viewing systems in control subjects is (controls: F1,9 = 21.423, p = 0.001; ani-
were considered to show poor agreement discussed elsewhere.14 sometropes: Z = -2.703, p = 0.007; ambly-
if the SD of the differences was more than For both anisometropes and amblyopes, opes: F1,9 = 30.146, p < 0.001).
1.96 ¥ SD of the results obtained using the the Bland-Altman method indicated The number of breaks requested by
goggles. acceptable or very good agreement each group is shown in Table 3. The

Clinical and Experimental Optometry 95.4 July 2012 © 2012 The Authors
416 Clinical and Experimental Optometry © 2012 Optometrists Association Australia
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

Anisometropes Amblyopes
Anisometropes Amblyopes A
A

TFA acuity Interaction Index


1.2 0.45
TFA acuity (logMAR)

1.1 0.35
1.0
0.9 0.25
0.8 0.15
0.7
0.6 0.05
0.5
-0.05
0.4
0.3 -0.15
0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 1.1 -0.15 -0.05 0.05 0.15 0.25 0.35 0.45

Shutter goggle acuity (logMAR)


Shutter goggle acuity Interaction Index

B B
Shutter goggle contrast sensitivity (dB)
TFA contrast sensitivity (dB)

0.2

TFA contrast sensitivity


-40 -35 -30 -25 -20 -15 -10 0.15

Interaction Index
-10
0.1
-15
-20 0.05

-25
0

-30 -0.05
-35 -0.1
-40 -0.1 -0.05 0 0.05 0.1 0.15 0.2

Shutter goggle contrast sensitivity Interaction Index

C C
TFA alignment sensitivity
TFA alignment sensitivity

0.8
1.0
Interaction Index

0.6
0.8
0.4
(arcmin-1)

0.6 0.2
0.0
0.4
-0.2
0.2 -0.4
-0.6
0
0 0.2 0.4 0.6 0.8 1.0 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8

-1
Shutter goggle alignment sensitivity (arcmin ) Shutter goggle alignment sensitivity Interaction Index

Figure 3. Non-dominant eye acuity (logMAR) [A], contrast Figure 4. Acuity [A], contrast sensitivity [B] and alignment
sensitivity (dB) [B] and alignment sensitivity (arcmin-1) [C] sensitivity [C] interaction indices evaluated using the trial
measured using the trial frame and shutter goggles with frame and shutter goggles in the non-dominant eye of 14
partial occlusion on the dominant eye of 14 anisometropic anisometropic children without amblyopia (anisometropes;
children without amblyopia (anisometropes; solid circles) solid circles) and 14 anisometropic amblyopic children
and 14 anisometropic amblyopic children (amblyopes; open (amblyopes; open squares). Index towards the positive y-axis
squares) indicates poorer non-dominant eye visual function with partial
relative to full occlusion of the dominant eye.

number was not significantly different sitivity testing did not differ significantly Z = -2.165, p = 0.030; amblyopes: Z =
among subject groups, using either the between the trial frame and goggle -2.041, p = 0.041) when goggles were used,
trial frame (acuity: c2[2] = 1.036; contrast viewing systems (Z = -1.265, p > 0.05). Sig- compared to when the TFA was used.
sensitivity: c2[2] = 0.558; alignment sensi- nificantly more breaks were requested by The total scores indicated by each
tivity: c2[2] = 0.558; p > 0.05) or shutter controls (Z = -2.070, p = 0.038) and ambly- group of subjects for willingness to attend
goggles (acuity: c2[2] = 0.180; contrast opes (Z = -2.111, p = 0.035) during the further sessions using the trial frame and
sensitivity: c2[2] = 0.201; alignment sensi- acuity test and by all groups of subjects shutter goggles are shown in Table 4. The
tivity: c2[2] = 0.330; p > 0.05). The number during the contrast sensitivity test (con- scores did not differ significantly among
of breaks requested during alignment sen- trols: Z = -2.070, p = 0.038; anisometropes: subject groups (TFA: c2[2] = 2.000;

© 2012 The Authors Clinical and Experimental Optometry 95.4 July 2012
Clinical and Experimental Optometry © 2012 Optometrists Association Australia 417
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

Agreement test
LOA Outlier Agreement
Bland–Altman t-test

Anisometropic Acuity Function -0.07 ⫾ 0.50 1 Acceptable p = 0.338


amblyopic children Index -0.02 ⫾ 0.24 1 Acceptable p = 0.644
Contrast Function -0.54 ⫾ 11.81 0 Acceptable p = 0.745
sensitivity Index 0 ⫾ 0.11 0 Good p = 0.874
Alignment Function -0.09 ⫾ 0.55 0 Good p = 0.241
sensitivity Index 0.10 ⫾ 0.64 0 Good p = 0.254
Anisometropic Acuity Function 0.04 ⫾ 0.46 0 Acceptable p = 0.540
children without Index 0.05 ⫾ 0.23 1 Good p = 0.120
amblyopia
Contrast Function 4.59 ⫾ 14.90 0 Acceptable p = 0.042
sensitivity Index -0.02 ⫾ 0.09 0 Good p = 0.133
Alignment Function 0 ⫾ 0.58 0 Acceptable p = 0.954
sensitivity Index 0.05 ⫾ 0.50 1 Acceptable p = 0.495

Table 2 Agreement between the two viewing systems. 1. The limits of agreement (LOA) for absolute measures and ‘interaction
indices’ measured using the two viewing systems (the trial frame and shutter goggles) in anisometropic children with and without
amblyopia. 2. The number of subjects in whom differences between the two viewing systems (the trial frame versus shutter goggles)
exceeded the two LOA (outliers) and 3. The agreement between the two viewing systems (Bland-Altman and t-test methods). For the
t-test, p > 0.05 indicates no significant difference between measurements using shutter goggles and the trial frame apparatus.
Differences between these two viewing systems were found only in contrast sensitivity measurements for anisometropic children
without amblyopia.

4.0 goggles: c2[2] = 1.050; p > 0.05). They


Duration of training session (minutes)

3.5
were significantly higher for the trial
3.0
2.5 frame than for goggles in anisometropes
2.0 (Z = -2.236, p = 0.025), indicating that
1.5
1.0 these subjects had significantly greater
0.5 TFA willingness to attend more experiments
0.0 Shutter goggles using the TFA than using goggles. The
Amblyopes

Amblyopes

Amblyopes
Anisometropes

Anisometropes

Anisometropes
Controls

Controls

Controls

scores from controls (Z = -1.633, p > 0.05)


and amblyopes (Z = -1.732, p > 0.05) did
not differ significantly between the two
viewing systems.
Acuity test Contrast sensitivity test Alignment sensitivity test

Figure 5. Duration of training sessions (minutes) using shutter goggles and the trial DISCUSSION
frame as viewing systems in acuity, contrast sensitivity and alignment sensitivity testing Shutter goggles and the trial frame gener-
in normally sighted children (controls) and anisometropic children with (amblyopes) ally show acceptable to good agreement in
and without (anisometropes) amblyopia. Error bars represent 95 per cent confidence visual function measures and in interac-
intervals. tion index evaluations in anisometropes
and amblyopes, with one exception. Con-
trast sensitivity in anisometropes showed
poor agreement between the two viewing
systems based on the paired t-test (but

Clinical and Experimental Optometry 95.4 July 2012 © 2012 The Authors
418 Clinical and Experimental Optometry © 2012 Optometrists Association Australia
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

system.41 This may be due to the use of the


Controls Anisometropes Amblyopes pinhole in front of the tested eye that
Acuity Trial frame 0 1 1 resulted in the reduction in retinal illumi-
nance.14,41 The present study found a sig-
Shutter goggles 8 7 8
nificantly higher acuity interaction index
Contrast sensitivity Trial frame 2 1 1
in amblyopes than in anisometropes
Shutter goggles 9 10 10
(evaluated using the trial frame). This sug-
Alignment Trial frame 1 1 2 gests that the extent to which acuity of the
sensitivity Shutter goggles 3 2 3 non-dominant eye is influenced by stimu-
lation of the dominant eye is greater in
Table 3 Total numbers of breaks requested by normally sighted children (controls) and anisometropic children with amblyopia
anisometropic children with (amblyopes) and without (anisometropes) amblyopia than in those without. This finding agrees
during acuity, contrast sensitivity and alignment sensitivity testing using the trial frame with previous work using shutter goggles;41
and shutter goggles as viewing systems however, the sample size in the present
study is small and the statistical power in
this sample is only 38 per cent (PS Power
and Sample Size Program42). Further
experiments with a larger sample may
improve understanding of the relation-
ship between interactions and anisome-
tropic amblyopia.
Subject group Trial frame Shutter goggles Two amblyopic subjects had negative
Controls 9 5 acuity interaction index (Figure 4), indi-
Anisometropes 10 5 cating better acuity with partial rather
Amblyopes 10 7 than full occlusion in these subjects. This
suggests that the relationship between
interocular interaction and anisometropic
Table 4 Total scores from normally sighted children (controls) amblyopia may vary in amblyopic subjects.
and anisometropic children with (amblyopes) and without (ani- The reason for this inconsistency is
sometropes) amblyopia indicating willingness to attend further unclear due to the lack of information
experiments using the trial frame and shutter goggles about the history of the development of
amblyopia and about the deficits at sub-
cortical and cortical levels in amblyopic
subjects. Similar studies on subjects with a
clear history of development of amblyopia
and accompanied by objective measures of
acceptable agreement was shown based on to the non-tested eye was 22° to 24° using amblyopia-related deficits would provide a
the Bland-Altman method). These find- the trial frame and 3.5° using goggles, it is better understanding of this relationship.
ings agree with previous work in controls,14 possible that the size of the central occlu- The pool of subjects tested here was
and suggest that the trial frame may be sion and the amount of light transmitted recruited from a larger group of 106 chil-
applicable in the evaluation of interocular from the periphery had a strong impact dren.43 While parents of all children gave
interaction in children and in investiga- on contrast sensitivity but a less significant consent for them to be tested using the
tion of these interactions in amblyopes, in impact on acuity or alignment sensitivity. TFA, consent for testing with the shutter
populations where more complex devices Perhaps better agreement in contrast goggles was received from parents of only
cannot be used. It is important to note sensitivity measurement may be found 42 of these children. Some of the parents
that the TFA does not have the flexibility between these two systems if similar sizes expressed concern that the use of unfamil-
of shutter goggles and mirror or prism of central occlusion were used. iar equipment could be harmful to their
devices and it may be used to study limited As shown in Figure 3, it is interesting to children’s vision. In addition, not all of the
forms of dichoptic masking. note that the acuity of the non-dominant 42 children were able to complete the
The poor agreement between shutter eye measured with partial occlusion did experimental processes using the goggles.
goggles and the trial frame in contrast sen- not differ significantly between amblyopes Three children in the anisometropes
sitivity measurement in anisometropes is and anisometropes (one-way ANOVA, p > group and one child in the amblyopes
consistent with findings in controls.14 As 0.05), which is consistent with previous group did not complete testing with
the size of the central occlusion presented findings using shutter goggles as a viewing goggles due to discomfort when wearing

© 2012 The Authors Clinical and Experimental Optometry 95.4 July 2012
Clinical and Experimental Optometry © 2012 Optometrists Association Australia 419
Interocular interaction evaluation in children Lai, Alexander, He, Yang and Suttle

the goggles and their parents were not vision in strabismic and anisometropic amblyopia. strabismic amblyopia. Invest Ophthalmol Vis Sci
Arch Ophthalmol 2006; 124: 844–850. 2007; 48: 5332–5338.
able to persuade them to continue with
6. McKee SP, Bravo MJ, Taylor DG, Legge GE. Stereo 26. Sengpiel F, Blakemore C. The neural basis of sup-
the tests. Thus, only 38 of the 106 children matching precedes dichoptic masking. Vision Res pression and amblyopia in strabismus. Eye (Lond)
underwent all tests with both viewing 1994; 34: 1047–1060. 1996; 10: 250–258.
7. Brown RJ, Candy TR, Norcia AM. Development of 27. Smith EL, Chino YM, Ni J, Cheng H, Crawford
systems, due to difficulties encountered in
rivalry and dichoptic masking in human infants. MLJ, Harwerth RS. Residual binocular interac-
using the shutter goggles. Invest Ophthalmol Vis Sci 1999; 40: 3324–3333. tions in the striate cortex of monkeys reared with
In addition to discomfort and parental 8. Baker DH, Meese TS. Binocular contrast interac- abnormal binocular vision. J Neurophysiol 1997; 78:
tions: dichoptic masking is not a single process. 1353–1362.
concerns about the shutter goggles,
Vision Res 2007; 47: 3096–3107. 28. Scheiman MM, Hertle RW, Beck RW, Edwards AR,
another complication with this viewing 9. Baker DH, Meese TS, Hess RF. Contrast masking Birch E, Cotter SA, Donahue S et al. Randomized
system was that the lenses were occasion- in strabismic amblyopia: attenuation, noise, trial of treatment of amblyopia in children aged 7
interocular suppression and binocular summa- to 17 years. Arch Ophthalmol 2005; 123: 437–447.
ally affected by condensation. This compli-
tion. Vision Res 2008; 48: 1625–1640. 29. Grosvenor TP. Primary Care Optometry. Boston:
cation is related to the fact that the 10. Vedamurthy I, Suttle CM, Alexander J, Asper LJ. Butterworth-Heinemann, 2002.
present study was conducted in a warm Interocular interactions during acuity measure- 30. Coren S, Kaplan CP. Patterns of ocular domi-
ment in children and adults, and in adults with nance. Am J Optom Arch Am Acad Optom 1973; 50:
environment, in high humidity and might
amblyopia. Vision Res 2007; 47: 179–188. 283–292.
not arise in cooler, less humid conditions. 11. Borra T, Hooge IT, Verstraten FA. A dichoptic 31. Roth HL, Lora AN, Heilman KM. Effects of
This factor may in part explain the differ- study of the oblique effect. Perception 2010; 39: monocular viewing and eye dominance on spatial
909–917. attention. Brain 2002; 125: 2023–2035.
ences between the two viewing systems in
12. Meese TS, Hess RF. Low spatial frequencies are 32. Weakley DRJ. The association between nonstrabis-
terms of duration of training, number of suppressively masked across spatial scale, orienta- mic anisometropia, amblyopia, and subnormal
breaks and willingness to participate in tion, field position, and eye of origin. J Vis 2004; 4: binocularity. Ophthalmology 2001; 108: 163–171.
843–859. 33. Bartz AE. Eye-movement latency, duration, and
further test sessions.
13. Meese TS, Georgeson MA, Baker DH. Binocular response time as a function of angular displace-
contrast vision at and above threshold. J Vis 2006; ment. J Exp Psychol 1962; 64: 318–324.
6: 1224–1243. 34. France TD, France LW. Low-contrast visual acuity
SUMMARY 14. Lai XJ, Alexander J, Ho A, Yang ZK, He MG, Suttle cards in pediatric ophthalmology. Graefes Arch Clin
C. Design and validation of a method for evalua- Experiment Ophthalmol 1988; 226: 158–160.
Our findings indicate acceptable agree- tion of interocular interaction. Optom Vis Sci 2011. 35. Skoczenski AM, Norcia AM. Late maturation of
[Epub ahea of print] visual hyperacuity. Psychol Sci 2002; 13: 537–541.
ment between shutter goggles and the
15. Moseley M, Fielder A. Amblyopia: A Multidisci- 36. Kaernbach C. Adaptive threshold estimation with
trial frame in acuity, contrast sensitivity plinary Approach. Woburn: Butterworth- unforced-choice tasks. Percept Psychophys 2001; 63:
and alignment sensitivity testing and in Heinemann, 2002. 1377–1388.
16. Hirsch MJ. Anisometropia: a preliminary report of 37. Green DM. A maximum-likelihood method for
evaluation of a form of interocular inter-
the Ojai Longitudinal Study. Am J Optom Arch Am estimating thresholds in a yes-no task. J Acoust Soc
action for these visual functions, in ani- Acad Optom. 1967;44:581–585. Am 1993; 93: 2096–2105.
sometropic children with and without 17. Blum HL. Vision Screening for Elementary 38. Leek MR. Adaptive procedures in psychophysical
Schools: The Orinda Study. Berkeley: University of research. Percept Psychophys 2001; 63: 1279–1292.
amblyopia. The trial frame is better
California Press, 1959. 39. Carkeet A, Levi DM, Manny RE. Development of
accepted by anisometropic children 18. Pediatric Eye Disease Investigator Group. The vernier acuity in childhood. Optom Vis Sci 1997; 74:
without amblyopia than the shutter clinical profile of moderate amblyopia in children 741–750.
younger than 7 years. Arch Ophthalmol 2002; 120: 40. Bland JM, Altman DG. Statistical methods for
goggles. The TFA may be a useful system
281–287. assessing agreement between two methods of clini-
in studies of interocular interaction in 19. Pediatric Eye Disease Investigator Group. A ran- cal measurement. Lancet 1986; 1: 307–310.
amblyopes, particularly in children. domized trial of atropine vs. patching for treat- 41. Lai XJ, Alexander J, He M, Yang Z, Suttle C. Visual
ment of moderate amblyopia in children. Arch functions and interocular interactions in anisome-
Ophthalmol 2002; 120: 268–278. tropic children with and without amblyopia. Invest
ACKNOWLEDGEMENT 20. Ruth AL, Lambert SR. Amblyopia in the phakic Ophthalmol Vis Sci 2011; 52: 6849–6859.
The authors thank Jinping Zheng for assis- eye after unilateral congenital cataract extraction. 42. Dupont WD, Plummer WD. Power and sample size
J AAPOS 2006; 10: 587–588. calculations. A review and computer program.
tance with data collection.
21. Levi DM, Harwerth RS, Manny RE. Suprathresh- Control Clin Trials 1990; 11: 116–128.
old spatial frequency detection and binocular 43. Lai XJ. Visual Functions and Interocular Interac-
interaction in strabismic and anisometropic tions in Normally Sighted Children and Anisome-
REFERENCES
amblyopia. Invest Ophthalmol Vis Sci 1979; 18: 714– tropic Children with and Without Amblyopia.
1. Norton TT, Corliss DA, Bailey JE. The Psycho- 725. School of Optometry and Vision Science. 2010,
physical Measurement of Visual Function. 22. Sireteanu R, Fronius M, Singer W. Binocular inter- The University of New South Wales: Sydney, 2010.
Woburn: Butterworth-Heinemann, 2002. p 201– action in the peripheral visual field of humans
204. with strabismic and anisometropic amblyopia.
2. Vedamurthy I, Suttle CM, Alexander J, Asper LJ. A Vision Res 1981; 21: 1065–1074. Corresponding author:
psychophysical study of human binocular interac- 23. Holopigian K, Blake R, Greenwald MJ. Selective Dr Xin Jie (Angela) Lai
tions in normal and amblyopic visual systems. losses in binocular vision in anisometropic ambly- School of Optometry and Vision Science
Vision Res. 2008; 48: 1522–1531. opes. Vision Res 1986; 26: 621–630.
3. Meese TS, Hess RF. Interocular suppression is 24. Hood AS, Morrison JD. The dependence of bin- The University of New South Wales
gated by interocular feature matching. Vision Res ocular contrast sensitivities on binocular single Kensington
2005; 45: 9–15. vision in normal and amblyopic human subjects. J NSW 2051
4. Paradiso MA, Nakayama K. Brightness perception Physiol 2002; 540: 607–622.
and filling-in. Vision Res 1991; 31: 1221–1236. 25. Baker DH, Meese TS, Mansouri B, Hess RF. Bin- AUSTRALIA
5. Agrawal R, Conner IP, Odom JV, Schwartz TL, ocular summation of contrast remains intact in E-mail: xinjie.lai@gmail.com
Mendola JD. Relating binocular and monocular

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