June 2011
Volume 52, Issue 7
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Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   June 2011
The Role of Suppression in Amblyopia
Author Affiliations & Notes
  • Jingrong Li
    From the State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, People's Republic of China;
  • Benjamin Thompson
    the Department of Optometry and Vision Science, Faculty of Science, The University of Auckland, Auckland, New Zealand;
  • Carly S. Y. Lam
    the School of Optometry, and
    the The Hong Kong Jockey Club Sports Medicine and Health Sciences Centre, Faculty of Health and Social Sciences, The Hong Kong Polytechnic University, Hong Kong SAR, China; and
  • Daming Deng
    From the State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, People's Republic of China;
  • Lily Y. L. Chan
    the School of Optometry, and
    the The Hong Kong Jockey Club Sports Medicine and Health Sciences Centre, Faculty of Health and Social Sciences, The Hong Kong Polytechnic University, Hong Kong SAR, China; and
  • Goro Maehara
    the Department of Ophthalmology, McGill University, Montreal, Quebec, Canada.
  • George C. Woo
    the School of Optometry, and
  • Minbin Yu
    From the State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, People's Republic of China;
  • Robert F. Hess
    the Department of Ophthalmology, McGill University, Montreal, Quebec, Canada.
  • Corresponding author: Minbin Yu, Department of Glaucoma, Department of Optometry and Vision Science, Zhongshan Ophthalmic Center, Guangzhou 510060, People's Republic of China; max-yu@tom.com
Investigative Ophthalmology & Visual Science June 2011, Vol.52, 4169-4176. doi:10.1167/iovs.11-7233
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      Jingrong Li, Benjamin Thompson, Carly S. Y. Lam, Daming Deng, Lily Y. L. Chan, Goro Maehara, George C. Woo, Minbin Yu, Robert F. Hess; The Role of Suppression in Amblyopia. Invest. Ophthalmol. Vis. Sci. 2011;52(7):4169-4176. doi: 10.1167/iovs.11-7233.

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      © 2017 Association for Research in Vision and Ophthalmology.

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Abstract

Purpose.: This study had three main goals: to assess the degree of suppression in patients with strabismic, anisometropic, and mixed amblyopia; to establish the relationship between suppression and the degree of amblyopia; and to compare the degree of suppression across the clinical subgroups within the sample.

Methods.: Using both standard measures of suppression (Bagolini lenses and neutral density [ND] filters, Worth 4-Dot test) and a new approach involving the measurement of dichoptic motion thresholds under conditions of variable interocular contrast, the degree of suppression in 43 amblyopic patients with strabismus, anisometropia, or a combination of both was quantified.

Results.: There was good agreement between the quantitative measures of suppression made with the new dichoptic motion threshold technique and measurements made with standard clinical techniques (Bagolini lenses and ND filters, Worth 4-Dot test). The degree of suppression was found to correlate directly with the degree of amblyopia within our clinical sample, whereby stronger suppression was associated with a greater difference in interocular acuity and poorer stereoacuity. Suppression was not related to the type or angle of strabismus when this was present or the previous treatment history.

Conclusions.: These results suggest that suppression may have a primary role in the amblyopia syndrome and therefore have implications for the treatment of amblyopia.

Suppression plays a key role in the amblyopic syndrome. Its clinical importance was recognized more than 60 years ago by the pioneering work of Travers, 1 Jampolsky, 2 and later, Pratt-Johnson and Wee, 3,4 who showed that its regional distribution (visual field topography) depends on the type of strabismus present. More recently, this approach has been carried on by Joosse et al. 5 7 whose innovative work has highlighted the different types of suppression that occur in strabismic amblyopia and how it varies within any one strabismic subpopulation. 
Although we now have a better idea of the position and shape of suppressed scotomata, we are still ignorant of their role and importance in the amblyopia syndrome, a condition in which there is loss of vision of a nonorganic nature, secondary to strabismus, anisometropia or form deprivation. There are some fundamental questions that remain unanswered, the most important of which relates to whether suppression is of primary or secondary importance to amblyopia. For example, suppression could simply follow as a consequence of amblyopia as a way of ensuring that the input from a weaker eye does not disrupt binocular perception. This view is compatible with current treatment approaches that focus on patching or penalization as a first step without any regard for suppression, which is often not quantified clinically and is rarely treated as a separate entity. The idea that amblyopia and suppression are separate entities gains some support from the suggestion that there is a reciprocal relationship between the strength of suppression and the degree of amblyopia; the greater the amblyopia, the less suppression is needed to eliminate that eye's input from the binocular mix. 8 The opposite view, however, is that suppression causes the visual dysfunction in amblyopia. In this scenario, the suppression develops due to a disruption of binocular function (strabismus or anisometropia), and it is the chronic suppression itself that results in amblyopia. This alternative view gains some support from the recent finding that, even in adults using repetitive transcranial magnetic stimulation (rTMS), a noninvasive means of transiently altering neural excitability in the human cortex, a 10-minute application of TMS can temporarily improve contrast sensitivity in amblyopia, 9 suggesting that visual function is not lost but suppressed. Further support comes from the finding that antisuppression therapy not only results in improved binocular function but also in improved monocular functioning of the adult amblyopic eye. 10 However, before one can accept that suppression is of primary importance in the amblyopic syndrome, the issue of the relationship between the degree of amblyopia and the strength of suppression should be reopened, for it is only if there is a direct relationship between these two clinical features that it would be reasonable to assume that suppression is of primary importance. The present support for a reciprocal relationship rests on only a small sample of patients with clinical suppression (n = 10), only two of whom had visual acuity worse than 20/30 in the amblyopic eye. 8  
Recently a novel method of quantifying binocular combination in the normal visual system has been developed, 11 and we have applied it to quantifying the strength of suppression in both strabismic and anisometropic amblyopes, 12,13 using a global motion stimulus in which signal elements moving in a coherent direction are seen by one eye and noise elements moving in random directions are seen by the other eye. This method is an accurate way, within the context of signal/noise analysis, of measuring 12,13 and treating 10 suppression within the central field. In this study we used this approach to assess the strength of suppression in a group of anisometropic, mixed, and strabismic amblyopes. The method provides a more quantitative means (better resolution) of measuring the degree of suppression compared with the Worth 4-Dot test or the use of a red filter and neutral density wedge. We first assessed the relationship between this new signal/noise method that can precisely quantify suppression and more traditional, relatively coarse, measures of suppression (Worth 4-Dot test and modified Bagolini test). We then addressed the following two questions: What is the relationship between visual losses in amblyopia (acuity and stereo) and the degree of suppression? How does suppression vary within the amblyopic clinical population? The answers to these questions bear on the issue of whether suppression plays a causal role in the visual loss that characterizes amblyopia. 
Methods
Participants
A total of 43 amblyopic observers (23 females, 20 males), between the ages of 9 and 56 years (mean age, 20.7 ± 11.9), and 10 normal observers (4 females, 6 males), between the ages of 20 to 35 years (mean age, 29.20 ± 5.39), who met the inclusion criteria were enrolled. Clinical details for the amblyopic observers are provided in Table 1
Table 1.
 
Clinical Details for the Observers with Amblyopia
Table 1.
 
Clinical Details for the Observers with Amblyopia
Observer Sex Age (y) Type Cycloplegic Refractive Error (OD/OS) LogMAR Visual Acuity (OD) LogMAR Visual Acuity (OS) Ocular Dev. (Prism D) History Stereopsis (sec arc)
01 F 17 A +3.35−0.50x145 0.09 −0.08 4XP Diagnosed: 7 years old 100
+1.25−0.50x110 (+) Patched: 4 years
02 F 11 A +2.00−0.25x161 0.04 −0.18 4XP Diagnosed: 8 years old 50
−1.25−0.75x178 (+) Patched: 2 years
03 F 43 A −0.75 DS 0 0.15 0 Diagnosed: 43 years old 40
+3.25+0.50x076 No treatment
04 F 56 A +4.75 DS 0 0.15 0 No detection 70
+7.50−3.00x040 No treatment
05 F 34 A +2.75−0.50x170 0 0.18 0 No detection 400
+6.00−1.50x013 No treatment
06 F 17 A −2.50 DS 0 0.52 0 Diagnosed: 17 years old Suppression
+4.50+2.50x095 No treatment
07 F 11 A Plano DS 0 0.40 0 Diagnosed: 11 years old 200
+4.25+2.00x155 No treatment
08 F 13 A +0.50DS −0.18 0.70 0 Diagnosed: 13 years old Suppression
+4.50DS No treatment
09 F 13 A Plano DS −0.08 0.15 0 Diagnosed: 13 years old 70
+2.50−3.50x175 No treatment
10 F 32 A +5.50+1.00x165 0.30 0 0 Diagnosed: 6 years old Suppression
−1.00−0.75x175 (+) Patched: 6 years
11 F 24 A +5.00−1.50x021 0 0.10 0 Diagnosed: 6 years old 70
+6.75−1.75x170 (+) Patched: 4 years
12 M 43 A −1.00DS 0 0.40 0 No detection 100
+2.25DS No treatment
13 M 19 A Plano DS −0.08 0.70 0 No detection Suppression
+7.00+0.75x180 No treatment
14 M 15 A −1.00−0.50x180 0.14 0 0 Diagnosed: 15 years old 80
+2.50+1.00x180 No treatment
15 M 21 A +1.00+3.50x165 0.15 0.08 0 Diagnosed: 21 years old 100
Plano DS No treatment
16 M 15 A +0.50+0.50x175 −0.18 0.70 0 Diagnosed: 15 years old Suppression
+7.50+1.25x75 No treatment
17 M 19 A −1.25−0.50x065 0 0.30 0 Diagnosed: 7 years old 120
+3.50+1.25x175 (+) Patched: 4 years
18 M 21 A +3.50 DS 0.15 −0.08 0 No detection 100
Plano DS No treatment
19 M 40 A −0.50 DS 0 0.10 0 No detection 100
+2.50 DS No treatment
20 M 37 A +3.50+1.00x100 0.30 0 0 No detection 200
Plano DS No treatment
21 M 10 A +1.25 DS 0 0.70 0 Diagnosed: 8 years old 200
+4.50 DS (+) Patched: 2 years
22 M 18 A +5.00−0.50x130 0 0.10 0 No detection 200
+4.25+0.50x010 No treatment
23 F 10 AS +6.50−1.50x177 0.10 0 0* Diagnosed: 3 years old 30
+4.50−2.00x175 (+) Patched: 2 years
(+) Surgery at 7 years old
24 F 48 AS +5.00−0.50x130 0.70 0 20ET, 35ET′ Diagnosed: 6 years old Suppression
+3.25−0.75x090 (+) Patched
(+) Surgery
25 M 10 AS +1.00−0.75x005 −0.08 0.05 0* Diagnosed: 6 years old 20
+2.75−1.75x170 (+) Surgery at 5 years old
26 M 17 AS −1.25 DS 0 0.22 0* Diagnosed: 6 years old Suppression
+4.25+1.00x165 (+) Patched
(+) Surgery at 7 years old
27 M 15 AS +1.25+1.00x175 0 0.70 0, 20XT′ No detection Suppression
+6.50+2.25x165 No treatment
28 M 26 AS +5.25+2.00x165 0.52 −0.08 10XT, 15XT′ No detection Suppression
Plano DS No treatment
29 M 29 AS −1.25 DS −0.18 0.05 15ET Diagnosed: 5 years old 70
+2.00+1.00x165 (+) Patched
(+) Surgery
30 F 10 S −7.00−2.25x010 0 0.4 0* Diagnosed: 6 years old 100
−8.00−2.50x170 (+) Patched
(+) Surgery
31 F 10 S −0.50−1.50x178 0.14 0 15XT, 10XT′ (+) Surgery at 6 years old 40
−0.50−0.50x178 (+) Patched
(+) Surgery
32 F 26 S −1.75−1.00x032 −.04 0.10 10XT, 15XT′ Detection N/A 40
−4.25−0.75x161 (+) Vision training treatment
33 F 9 S −2.00−1.50x010 0.16 0 10ET, 15ET′ No detection 25
−4.00−0.50x166 No treatment
34 F 12 S +1.25 DS 0 0.10 0, 10XT′ Detection N/A 200
Plano DS (+) Patched
(+) Surgery at 7 years
35 F 16 S Plano DS 0.10 0 15XT, 10XT′ No detection 120
Plano+0.50x175 No treatment
36 F 15 S −0.50 DS 0.16 0 20ET Diagnosed: 8 years old 200
+1.25+0.50x175 (+) Surgery at 10 years old
37 F 15 S +1.00+0.50x030 0 0.22 35ET, 35ET′ No detection 400
+2.00+0.50x145 No treatment
38 F 12 S Plano DS 0 0.15 25ET, 15ET′ No detection 80
Plano DS No treatment
39 M 14 S +0.75 DS 0 0.15 30XT, 25XT′ Diagnosed: 6 years old 100
+0.75 DS No treatment
40 M 12 S +1.00 DS −0.08 0.10 30XT, 25XT′ No detection 140
−0.25 DS No treatment
41 M 12 S −0.25 DS −0.08 0.10 20ET, 15ET′ Diagnosed: 4 years old 80
+0.50 DS (+) Surgery at 6 years old
42 M 32 S +0.50 DS 0 0.15 30ET, 35ET′ No detection 70
−0.75 DS No treatment
43 F 10 S −4.00−2.75x002 0.05 0.15 15XT, 10XT′ No detection 30
−4.25−2.75x002 No treatment
The normal observers acted as the control group and had equal visual acuity in each eye of at least 20/20; absence of any ocular, oculomotor, or binocular abnormalities; normal stereoacuity (≤20 seconds of arc); and a spherical equivalent refractive error of between +1.00 and −3.00 D, with an unequal spherical equivalent of not more than a 1-D difference between the eyes detected during a standard ocular examination; and a cylindrical correction of less than 1 D. The amblyopic group was defined according to the Preferred Practice Protocol (PPP) of The American Academy of Ophthalmology 14 and classified under one of the following clinical conditions: strabismic amblyopia (with an angle of strabismus of less than 35Δ), anisometropic amblyopia with a visual acuity loss in the worse eye of no worse than 20/100, and mixed (those that met the criteria for both types of amblyopia). Subjects with strabismus due to ocular albinism, diplopia, anomalous correspondence, or a medical history of seizures were excluded. All tests were conducted at a constant room luminance, measured with a digital lux meter (TES Electronic Corp., Taipei, Taiwan). This study complied with the Declaration of Helsinki and was approved by the Ethics Committee of Zhongshan Ophthalmic Center and The Hong Kong Polytechnic University. Informed consent was obtained from all participants before data collection. On the basis of previous data from both amblyopic observers 13 and observers with normal binocular vision (Thompson, unpublished data, 2010), we estimated a difference in fellow fixing eye contrast at a balance point of 70% contrast between controls and observers with amblyopia with a maximum SD of 17%. To detect this difference at a significance level of P < 0.01 with a power of 0.99 would require three participants per group. Our smallest subgroup contained 10 participants. 
Stereo Acuity Test
Stereoacuity was assessed using the Randot stereo graded circle test (Random Dot 2 Acuity Test, Vision Assessment Corp., Elk Grove Village, IL). These values are reported in Table 1
Suppression Measurement
The Worth-4-Dot Test.
The Worth-4-Dot test was performed at near (33 cm) and far (6 m) test distances. The filters were placed, according to convention: red over the right eye and green over the left eye. To ensure the visibility of each filter, the participants' eyes were covered alternately to ensure that each eye was visibly aware of the red and green filters. When this testing was performed monocularly, all participants reported seeing two red dots when the left eye was occluded (right eye wearing the red filter) and three green dots when the right eye was occluded (left eye wearing the green filter). Participants were asked to report the number and color of the dots they saw under photopic (118 lux) followed by scotopic (<0.1 lux) conditions. A scoring system was assigned to grade the depth and the size of the suppression scotoma. For example, a four-dot response with the white dot at the bottom was given a score of 0 (no suppression), while a two- or three-dot response received a score of 2 (complete suppression). A score of 1 (partial suppression) was assigned to observers who reported that they saw four dots, with the color of the bottom white dot being perceived as either green or red. The sum of near and far scores, which could range from 0 to 4, was used to represent the overall level of suppression as measured by this test, as we found no reliable difference between the near and far measurements (sign test, P = 1.0). 
The Neutral-Density Filter with the Bagolini Striated Lens Test.
The relative depth of suppression in the amblyopic eye was assessed by combining the Bagolini striated lenses test with neutral-density (ND) filters. 15 Each observer viewed a light source (30 cd/m2) held at 33 cm while wearing Bagolini striated lenses under low ambient room illumination (5 lux). Under normal viewing conditions, participants with normal binocular function perceive an X, representing the combination of the / seen by one eye and the \ seen by the other. However, for participants with suppression, only one line (/ or \) is perceived within the region affected by the suppression scotoma. To measure the strength of this suppression, progressively stronger ND filters can be placed over the fellow eye until the imbalance in luminance between the two eyes is sufficiently strong to overcome the suppression and allow for the percept of the X. To achieve this, ND filters (Wratten; Eastman Kodak Company, Rochester, NY), increasing in 0.3-log-unit increments were mounted on a bar. The filters ranged from 0.3 to 3 log units and had a transmittance ranging from 50% to 0.1%. The ND filter bar was held vertically in front of the fellow fixing (fixating) eye and moved upward to increase the strength of the ND filter. Participants were asked to report when they could perceive an X. The end point of this test was defined as the ND filter strength at which the intensity of the line seen by the amblyopic eye was perceived as the same or slightly stronger than the line seen by the fellow fixing (fixating) eye. To ensure the accuracy of this end point, the ND filter strength was increased by an additional 0.6 log units below this balance point, and the end point was measured again from seeing to nonseeing until a balanced reversal point was achieved. 
Dichoptic Motion Coherence Threshold Measurements
The method we used for measuring interocular suppression using random-dot kinematograms has been described in detail elsewhere. 13 Briefly, stimuli were displayed using a video goggle apparatus (Z800 3D Visor; eMagin Corp., Washington, DC) driven by a laptop computer (MacBook Pro; Apple Computer, Cupertino, CA, running MatLab; The MathWorks, Natick, MA) and the Psychophysics Toolbox, version 3. 12,13,16 This apparatus allowed for separate images to be presented to each eye and for the images in each eye to be aligned by the participants, using routines within the stimulus presentation software. Stimuli were random-dot kinematograms, which consisted of a population of signal dots, all moving in a common direction, and a population of noise dots, that moved randomly. Dots were bright against a mean luminance background (35 cd/m2). The luminance modulation (Michelson contrast) and hence the visibility of the dots could be varied by increasing the luminance of the dots, with respect to the background, according to the following equation:   where L dots and L background are the dot and background luminance, respectively. Signal dots were presented to one eye, and noise dots were presented to the other eye. The task was to indicate the motion direction of the signal dots. A staircase procedure controlled the relative proportion of signal-to-noise dots in the stimulus to allow for the measurement of a motion coherence threshold (the number of signal dots required for 71% correct performance; see Black et al. 13 for further details [their method 1] and illustrative figures of this technique). To measure suppression, the contrast of the dots presented to the amblyopic eye was fixed at 100% whereas the contrast of the dots presented to the fellow fixing eye was varied across five contrast levels (100%, 80%, 50%, 25%, and 12.5% contrast, equivalent to dot luminances of 70, 63, 52.5, 43.8, and 39.4 cd/m2, respectively), using the method of constant stimuli. Within a single measurement session, 10 randomly interleaved staircases were presented, five for each contrast level with the signal dots shown to the amblyopic eye and five for the signal dot presentation to the fellow fixing eye. Two measurement sessions were conducted per patient separated by a 30-minute break. The fellow fixing eye contrast at which the motion coherence thresholds were the same irrespective of which eye saw the signal and which saw the noise was calculated by fitting linear functions to the average threshold data for each eye as a function of fellow fixing eye contrast and calculating the intersection of these fits. 13 We refer to this dichoptic contrast offset as the “balance point,” as it represents the point at which suppression has been overcome and information is being combined between the two eyes in a normal fashion. 12,13 Therefore, the balance point contrast can be considered as a parametric measurement of suppression. 12 For the control group the nondominant eye, as defined by the hole-in-the-card test, was designated as the amblyopic eye for these measurements. The alignment of central nonius lines (one to each eye) was used to ensure accurate alignment of the stimulus fields seen by the right and left eyes. Subjects were asked to attend to the central part of the stimulus field. The fact that for this stimulus corresponding points are not stimulated (i.e., the signal and noise dots do not overlap in space) allows fusion to occur on a more global level, and we believe it is this that makes its use as a treatment so effective. We view the point-wise suppression as more of V1 function and the global suppression more of extrastriate function. 
Results
A one-way ANOVA conducted on the balance point data revealed a significant main effect of group (control versus strabismic versus anisometropic versus mixed; F (3,49) = 12.18, P < 0.0001. Post hoc Bonferroni tests (corrected for multiple comparison) revealed that the control group balance points were significantly higher than those of each of the three amblyopic groups (strabismic P < 0.03; anisometropic P < 0.001; mixed P < 0.001). The amblyopic groups did not differ significantly from one another (P > 0.05). The mean contrast presented to the fellow fixing (or dominant) eye at the balance point and the corresponding 95% confidence interval (CI) can be seen in Figure 1. It is evident that amblyopic participants had a significantly larger imbalance between the eyes than the control participants (i.e., lower fellow eye contrasts at balance point) consistent with the presence of interocular suppression. The fact that control participants did have a small contrast offset reflects the sensitivity of this test to eye dominance. 11,17 The mean coherence thresholds (i.e., the number of signal dots) at the balance point (95% CI) were as follows: controls, 16 (14–19); anisometropic, 10 (9–12); mixed, 11 (8–13); and strabismic, 13 (11–15). These results demonstrate that once balanced, the amblyopic participants performed no worse, in fact a little better, than the control observers; however, thresholds across the groups were generally comparable. The thresholds of amblyopic participants were very similar to those in previous reports using related techniques in a group of observers with amblyopia 13 and a group of observers with normal binocular vision who were shown stimuli of equal contrast to both eyes. 17 The relatively elevated thresholds we found for the control participants may reflect the fact that this technique is designed to measure suppression, and the use of a large range of contrasts may slightly bias motion coherence estimates when suppression is not present. 
Figure 1.
 
The contrast presented to the fellow (or dominant) eye to achieve balanced performance on the motion coherence task between the two eyes (i.e., the same motion coherence threshold was achieved regardless of which eye was presented with noise and which with signal). Error bars, 95% CI of the mean. Controls, n = 10, anisometropes, n = 22; mixed, n = 7; and strabismics, n = 14.
Figure 1.
 
The contrast presented to the fellow (or dominant) eye to achieve balanced performance on the motion coherence task between the two eyes (i.e., the same motion coherence threshold was achieved regardless of which eye was presented with noise and which with signal). Error bars, 95% CI of the mean. Controls, n = 10, anisometropes, n = 22; mixed, n = 7; and strabismics, n = 14.
As our group of observers with amblyopia included both adult and juvenile (≤17 years of age) patients, we conducted a separate analysis to investigate the effect of age on the balance point data and on motion coherence thresholds. We found no difference between adults and juveniles for either the balance point data (t (41) = 0.7, P = 0.52; juvenile mean, 56.4 [SD 21.5]; adult mean, 52.7 [SD 15.3]) or the motion coherence threshold data (t (41) = 0.53, P = 0.60; juvenile mean, 11.5 [SD 3.8]; adult mean, 11.0 [SD 3.1]). We also found no correlation between age and either the balance point data (Spearman's ρ = −0.2, P = 0.22) or the motion coherence data (Spearman's ρ = 0.07, P = 0.65). These analyses indicate that the patient's age did not systematically influence these variables. As such, the observers with amblyopia were treated as a single group in subsequent analyses. 
To compare the balance point test with clinical tests of suppression, we correlated the results of the Worth 4-Dot test and the modified Bagolini striated lenses test with the balance point contrast. The near and far results for the Worth 4-Dot test were combined to give a score from 0 (no suppression for either test) to 4 (full suppression on both tests). For both suppression measures, there was a significant negative correlation with the fellow fixing eye's contrast at the balance point (rank; Worth 4-Dot, ρ = −0.57, P < 0.0001; modified Bagolini, ρ = −0.74, P < 0.0001; Fig. 2). This finding demonstrates that the larger the difference in contrast between the two eyes that is necessary for normal binocular combination of motion signals (i.e., the lower the contrast in the fellow eye; recall that the contrast to the amblyopic eye remains fixed at 100%), the larger the amount of suppression measured using standard and modified clinical tests. 
Figure 2.
 
The relationship between the contrast presented to the fellow fixing eye at the balance point and suppression on the Worth 4-Dot test (A) and the modified Bagolini striated lenses test (B). Higher numbers on both the Worth and Bagolini tests (x-axis) are indicative of greater suppression. Smaller contrast values for the balance point (y-axis) are indicative of greater suppression, as a larger imbalance between the eyes is required for binocular combination to occur. (A) Interval data on the abscissa and ordinal data on the ordinate axis. The statistical analysis for this comparison was nonparametric and conducted on the ranked data using Spearman's rho.
Figure 2.
 
The relationship between the contrast presented to the fellow fixing eye at the balance point and suppression on the Worth 4-Dot test (A) and the modified Bagolini striated lenses test (B). Higher numbers on both the Worth and Bagolini tests (x-axis) are indicative of greater suppression. Smaller contrast values for the balance point (y-axis) are indicative of greater suppression, as a larger imbalance between the eyes is required for binocular combination to occur. (A) Interval data on the abscissa and ordinal data on the ordinate axis. The statistical analysis for this comparison was nonparametric and conducted on the ranked data using Spearman's rho.
The contrast at the balance point also correlated significantly with both stereo sensitivity (ρ = 0.47, P = 0.002; the greater the stereo sensitivity, the less the difference in contrast between the eyes) and the acuity difference in log units between the eyes (ρ = −0.60, P < 0.001; the greater the acuity difference, the greater the contrast difference). These correlations are shown in Figure 3. To assess whether the relationship between these two variables and the contrast at balance point differed among anisometropic, mixed, and strabismic amblyopes, we performed a univariate general linear model analysis on the contrast at balance point data with amblyopia type (anisometropic versus mixed versus strabismic), acuity difference between the eyes, and stereo sensitivity as covariates. The model revealed a significant interaction between amblyopia type and acuity difference, F = 10.02, P = 0.003, demonstrating that the effect of visual acuity difference on balance point contrast varied across the different amblyopia subtypes. There was no significant interaction between amblyopia subtype and stereo sensitivity, suggesting that the effect of stereo sensitivity did not vary across the different amblyopia subtypes. To explore the interocular visual acuity difference and amblyopia subtype interaction further, we correlated interocular visual acuity difference with balance point contrast separately for each amblyopia subtype. Both the strabismic and mixed amblyopes showed significant negative correlations (strabismic: ρ = −0.62, P = 0.018, mixed: ρ = −0.82, P = 0.023). The anisometropic amblyopes also showed a negative correlation, but it did not quite reach significance (ρ = −0.42, P = 0.053), suggesting that the presence of strabismus influenced the strength of the relationship between acuity difference and balance point contrast. 
Figure 3.
 
The relationship between contrast in the fellow fixing eye at the balance point and stereo sensitivity (A) or acuity difference between the eyes (B). Dashed lines: the best linear fit to the data. For stereo sensitivity (A) the negative correlation shows that the lower the balance point contrast in the fellow fixing eye (i.e., the greater the difference between the eyes), the lower the stereo sensitivity. The positive correlation for acuity difference (B) demonstrates that the greater the difference between the eyes at balance point contrast, the larger the acuity difference.
Figure 3.
 
The relationship between contrast in the fellow fixing eye at the balance point and stereo sensitivity (A) or acuity difference between the eyes (B). Dashed lines: the best linear fit to the data. For stereo sensitivity (A) the negative correlation shows that the lower the balance point contrast in the fellow fixing eye (i.e., the greater the difference between the eyes), the lower the stereo sensitivity. The positive correlation for acuity difference (B) demonstrates that the greater the difference between the eyes at balance point contrast, the larger the acuity difference.
We have shown that dichoptic motion coherence thresholds can be used to assess sensory ocular dominance in observers with normal binocular vision. 18 Since the participants in this previous study did not have any interocular suppression, we did not vary contrast between the eyes but rather presented stimuli at 100% contrast to both eyes and calculated the motion coherence threshold ratio for signal dots presented to the left eye versus signal dots presented to the right eye. To assess the relationship between this measure and the balance point measure for amblyopic observers, for each participant, we calculated the threshold ratio when stimuli were presented at 100% contrast for both eyes and correlated the result with the balance point measure. The threshold ratio was calculated as amblyopic eye threshold/fellow eye threshold, and therefore larger ratios indicate a greater degree of suppression of the amblyopic eye. As shown in Figure 4 these two measures correlated significantly (ρ = −0.77, P < 0.001). This relationship did not covary with amblyopia subtype (F (1,40) = 0.17, P = 0.69). 
Figure 4.
 
The relationship between fellow eye contrast at balance point and the motion coherence threshold ratio between the eyes when 100% contrast was shown to both eyes. Larger threshold ratios and lower fellow eye contrasts indicate a greater deficit for the amblyopic eye under dichoptic viewing conditions.
Figure 4.
 
The relationship between fellow eye contrast at balance point and the motion coherence threshold ratio between the eyes when 100% contrast was shown to both eyes. Larger threshold ratios and lower fellow eye contrasts indicate a greater deficit for the amblyopic eye under dichoptic viewing conditions.
Next, we assessed whether the amount of suppression was greater in participants who had never received treatment for their amblyopia. Within our sample, 16 anisometropic and 7 strabismic amblyopes had never received treatment, 6 anisometropic and 1 mixed amblyope had received patching only, 6 strabismic and 2 mixed amblyopes had received surgery only, and 4 strabismic and 1 mixed amblyope had received both patching and surgery. We found that the patients who had received treatment showed no difference in any of our measurements relative to the nontreated group (between-subjects t-tests, P > 0.05) and none of our outcome measures covaried with treatment and amblyopia subtype (univariate ANOVA with covariates of treatment type and amblyopia subtype). Figure 5 shows the mean contrast for the fellow fixing eye at balance point (Fig. 5A) and the mean interocular acuity difference (Fig. 5B) for each of the treatment groups (no treatment, patching only, surgery only, and both surgery and patching. 
Figure 5.
 
Mean fellow eye contrast at balance point (A) and interocular acuity difference (B) for participants who had never received treatment (n = 23), received patching only (n = 7), received surgery only (n = 8), or received both patching and surgery (n = 5). Errors bars, 95% CI.
Figure 5.
 
Mean fellow eye contrast at balance point (A) and interocular acuity difference (B) for participants who had never received treatment (n = 23), received patching only (n = 7), received surgery only (n = 8), or received both patching and surgery (n = 5). Errors bars, 95% CI.
Finally, we considered only the participants with strabismic or mixed amblyopia who still had strabismus to assess whether the extent of strabismus was related to the strength of suppression. The relationship between angle of deviation and suppression is shown in Fig. 6 for both the balance point measure (Fig. 6A) and the Bagolini measure (Fig. 6B) of suppression. Exotropes and esotropes are identified in these plots by the use of filled and hollow markers, respectively. There were no reliable relationships between deviation angle and strength of suppression; however, in the esotropes there was a trend toward increasing suppression with increasing angle of deviation for the balance point measure, which did not reach significance, probably due to the small sample size of this group (n = 5; ρ = −0.7, P = 0.2). In addition, we found no relationship between angle of deviation and stereo acuity or interocular acuity difference (P > 0.05 for both). 
Figure 6.
 
The relationship between the angle of strabismus and strength of suppression using the balance point measurement (A) and the Bagolini method (B). The two larger circles indicate overlapping esotrope and exotrope data points. Dashed lines: indicate linear fits to the data.
Figure 6.
 
The relationship between the angle of strabismus and strength of suppression using the balance point measurement (A) and the Bagolini method (B). The two larger circles indicate overlapping esotrope and exotrope data points. Dashed lines: indicate linear fits to the data.
Discussion
In this study, we set out to answer the three questions detailed below. 
How does the new balance point method compare with the current clinical standards (Worth 4-Dot test and modified Bagolini test) across a clinical population? Using a novel approach involving the measurement of dichoptic motion thresholds for stimuli of different interocular contrast, we show that the degree of suppression is significant in strabismus, anisometropia, and mixed amblyopia, but that there was no significant difference across our clinical sample in the different subgroups (i.e., strabismics, anisometropes, and mixed). We also demonstrate that this new quantitative approach to the measurement of suppression correlates strongly with traditional, albeit qualitative, clinical measures. Finally, we show a significant correlation between the balance point measure and a more abbreviated measurement based on the same principle previously used to quantify sensory dominance in the normal population. 17 This conclusion is supported by data on eye dominance within the normal population. 18 In all, these results suggest that this new approach has promise for quantifying suppression in binocular dysfunction and eye dominance in both clinical and normal populations. 12,13,17  
What is the relationship between visual losses in amblyopia (acuity and stereo) and the degree of suppression? We determined the extent to which the contrast of the stimuli (signal or noise) presented to the fellow fixing eye had to be reduced in order for normal sensory binocular combination to take place (the contrast of stimuli seen by the amblyopic eye was fixed at 100%). As discussed above, this measure of suppression is in close agreement with standard clinical measures. We found that the degree of suppression measured using this technique significantly correlated with the degree of amblyopia and stereo loss. In other words, the greater the suppression, the greater the amblyopia. This result is contrary to accepted wisdom 8 that stronger suppression is associated with weaker amblyopia, but is consistent with previous reports demonstrating stronger suppression with deeper amblyopia. 18 20 It should be noted that our study differed from that of Holopigian et al. 8 in several ways. Our sample was larger and had a greater range of amblyopia severity than did the sample reported by Holopigian et al., which mainly contained patients with very mild amblyopia (visual acuity of 20/30−2 or better in the amblyopic eye). Also their sample contained a disproportionate number of patients with alternating strabismus (8 patients in a sample of 10), which may represent a special category. A comparison of our findings with those of Holopigian et al. therefore raises the possibility that the suppression found in patients with amblyopia may differ from that in patients with alternating strabismus without amblyopia or in patients with very mild amblyopia. In addition, our primary measure of suppression differed from that used by Holopigian et al., who used monocular and dichoptic increment threshold measurements for 3.3-cyc/deg sinusoidal gratings presented foveally. Of note, their data show the same, albeit a weaker, relationship between suppression and stereopsis that we report wherein stronger suppression results in reduced stereopsis, as one would expect. 
Our results, while being consistent with the idea that amblyopia results from suppression rather than the other way around, do not in themselves prove a causal connection. It is possible that they are positively correlated because both are the result of another factor, as yet unknown. What we can say is that if suppression were simply a mechanism to stop the diplopic vision from an amblyopic eye from reaching perception, then a greater degree of suppression would be necessary for mild compared with severe amblyopia. That is not what we found. 
How does suppression vary among the amblyopic clinical population? Although it is commonly thought that the greatest degree of suppression occurs in cases of strabismic amblyopia and the least in cases of anisometropia, we did not find any significant differences between the degree of suppression in adults with strabismus, anisometropia, or mixed strabismus and anisometropia using our balance point measurement. Furthermore, we did not find that the degree of suppression depended on the angle of the strabismus or the type of deviation, in agreement with previous studies. 8,21 26 However our sample size was necessarily small, and therefore these results are not definitive. A caveat is needed here, because our method averages sensitivity over the central 20° and can only provide a global measure of suppression. Since there is evidence that the size and extent of suppression scotomata depend on the type and angle of squint, 1 4,7 a more localized measure is needed to address this issue. We are currently investigating this question. 
Conclusions
If it is indeed the case that suppression plays a causal role in amblyopia, as our current data suggest, then there is an argument to be made for incorporating therapeutic approaches that directly target amblyopic eye suppression into amblyopia treatment regimens. We have recently shown that repeated exposure to dichoptic motion coherence threshold stimuli can effectively reduce suppression in adults with amblyopia, which in turn can improve visual acuity and stereopsis. 10,27 These findings add further weight to the hypothesis that suppression plays a primary role in the amblyopia syndrome and the importance of considering suppression when treating amblyopia. These visual improvements are sustained and have so far been demonstrated in adults well beyond the critical period of visual development. We are presently developing a handheld, take home device on which the balance point principles are implemented in the form of a video game, suitable for the younger age group. 
Footnotes
 Supported by equipment/resources donated by The Hong Kong Jockey Club Charities Trust, Hong Kong Polytechnic University Internal Competitive Research Grant CRG G-YH71 (CSYL), University of Auckland Faculty Development Research Fund Award (BT), CIHR Grants MOP 53346 and PPP93073 (RFH), the Fundamental Research Funds of the State Key Lab of Ophthalmology, Sun Yat-sen University (JL), a Thrasher Research Fund Early Career Award (JL), and the Guangdong Province International Collaboration Project Grant 2010B050100014 (DD).
Footnotes
 Disclosure: J. Li, None; B. Thompson, None; C.S.Y. Lam, None; D. Deng, None; L.Y.L. Chan, None; G. Maehara, None; G.C. Woo, None; M. Yu, None; R.F. Hess, None
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Figure 1.
 
The contrast presented to the fellow (or dominant) eye to achieve balanced performance on the motion coherence task between the two eyes (i.e., the same motion coherence threshold was achieved regardless of which eye was presented with noise and which with signal). Error bars, 95% CI of the mean. Controls, n = 10, anisometropes, n = 22; mixed, n = 7; and strabismics, n = 14.
Figure 1.
 
The contrast presented to the fellow (or dominant) eye to achieve balanced performance on the motion coherence task between the two eyes (i.e., the same motion coherence threshold was achieved regardless of which eye was presented with noise and which with signal). Error bars, 95% CI of the mean. Controls, n = 10, anisometropes, n = 22; mixed, n = 7; and strabismics, n = 14.
Figure 2.
 
The relationship between the contrast presented to the fellow fixing eye at the balance point and suppression on the Worth 4-Dot test (A) and the modified Bagolini striated lenses test (B). Higher numbers on both the Worth and Bagolini tests (x-axis) are indicative of greater suppression. Smaller contrast values for the balance point (y-axis) are indicative of greater suppression, as a larger imbalance between the eyes is required for binocular combination to occur. (A) Interval data on the abscissa and ordinal data on the ordinate axis. The statistical analysis for this comparison was nonparametric and conducted on the ranked data using Spearman's rho.
Figure 2.
 
The relationship between the contrast presented to the fellow fixing eye at the balance point and suppression on the Worth 4-Dot test (A) and the modified Bagolini striated lenses test (B). Higher numbers on both the Worth and Bagolini tests (x-axis) are indicative of greater suppression. Smaller contrast values for the balance point (y-axis) are indicative of greater suppression, as a larger imbalance between the eyes is required for binocular combination to occur. (A) Interval data on the abscissa and ordinal data on the ordinate axis. The statistical analysis for this comparison was nonparametric and conducted on the ranked data using Spearman's rho.
Figure 3.
 
The relationship between contrast in the fellow fixing eye at the balance point and stereo sensitivity (A) or acuity difference between the eyes (B). Dashed lines: the best linear fit to the data. For stereo sensitivity (A) the negative correlation shows that the lower the balance point contrast in the fellow fixing eye (i.e., the greater the difference between the eyes), the lower the stereo sensitivity. The positive correlation for acuity difference (B) demonstrates that the greater the difference between the eyes at balance point contrast, the larger the acuity difference.
Figure 3.
 
The relationship between contrast in the fellow fixing eye at the balance point and stereo sensitivity (A) or acuity difference between the eyes (B). Dashed lines: the best linear fit to the data. For stereo sensitivity (A) the negative correlation shows that the lower the balance point contrast in the fellow fixing eye (i.e., the greater the difference between the eyes), the lower the stereo sensitivity. The positive correlation for acuity difference (B) demonstrates that the greater the difference between the eyes at balance point contrast, the larger the acuity difference.
Figure 4.
 
The relationship between fellow eye contrast at balance point and the motion coherence threshold ratio between the eyes when 100% contrast was shown to both eyes. Larger threshold ratios and lower fellow eye contrasts indicate a greater deficit for the amblyopic eye under dichoptic viewing conditions.
Figure 4.
 
The relationship between fellow eye contrast at balance point and the motion coherence threshold ratio between the eyes when 100% contrast was shown to both eyes. Larger threshold ratios and lower fellow eye contrasts indicate a greater deficit for the amblyopic eye under dichoptic viewing conditions.
Figure 5.
 
Mean fellow eye contrast at balance point (A) and interocular acuity difference (B) for participants who had never received treatment (n = 23), received patching only (n = 7), received surgery only (n = 8), or received both patching and surgery (n = 5). Errors bars, 95% CI.
Figure 5.
 
Mean fellow eye contrast at balance point (A) and interocular acuity difference (B) for participants who had never received treatment (n = 23), received patching only (n = 7), received surgery only (n = 8), or received both patching and surgery (n = 5). Errors bars, 95% CI.
Figure 6.
 
The relationship between the angle of strabismus and strength of suppression using the balance point measurement (A) and the Bagolini method (B). The two larger circles indicate overlapping esotrope and exotrope data points. Dashed lines: indicate linear fits to the data.
Figure 6.
 
The relationship between the angle of strabismus and strength of suppression using the balance point measurement (A) and the Bagolini method (B). The two larger circles indicate overlapping esotrope and exotrope data points. Dashed lines: indicate linear fits to the data.
Table 1.
 
Clinical Details for the Observers with Amblyopia
Table 1.
 
Clinical Details for the Observers with Amblyopia
Observer Sex Age (y) Type Cycloplegic Refractive Error (OD/OS) LogMAR Visual Acuity (OD) LogMAR Visual Acuity (OS) Ocular Dev. (Prism D) History Stereopsis (sec arc)
01 F 17 A +3.35−0.50x145 0.09 −0.08 4XP Diagnosed: 7 years old 100
+1.25−0.50x110 (+) Patched: 4 years
02 F 11 A +2.00−0.25x161 0.04 −0.18 4XP Diagnosed: 8 years old 50
−1.25−0.75x178 (+) Patched: 2 years
03 F 43 A −0.75 DS 0 0.15 0 Diagnosed: 43 years old 40
+3.25+0.50x076 No treatment
04 F 56 A +4.75 DS 0 0.15 0 No detection 70
+7.50−3.00x040 No treatment
05 F 34 A +2.75−0.50x170 0 0.18 0 No detection 400
+6.00−1.50x013 No treatment
06 F 17 A −2.50 DS 0 0.52 0 Diagnosed: 17 years old Suppression
+4.50+2.50x095 No treatment
07 F 11 A Plano DS 0 0.40 0 Diagnosed: 11 years old 200
+4.25+2.00x155 No treatment
08 F 13 A +0.50DS −0.18 0.70 0 Diagnosed: 13 years old Suppression
+4.50DS No treatment
09 F 13 A Plano DS −0.08 0.15 0 Diagnosed: 13 years old 70
+2.50−3.50x175 No treatment
10 F 32 A +5.50+1.00x165 0.30 0 0 Diagnosed: 6 years old Suppression
−1.00−0.75x175 (+) Patched: 6 years
11 F 24 A +5.00−1.50x021 0 0.10 0 Diagnosed: 6 years old 70
+6.75−1.75x170 (+) Patched: 4 years
12 M 43 A −1.00DS 0 0.40 0 No detection 100
+2.25DS No treatment
13 M 19 A Plano DS −0.08 0.70 0 No detection Suppression
+7.00+0.75x180 No treatment
14 M 15 A −1.00−0.50x180 0.14 0 0 Diagnosed: 15 years old 80
+2.50+1.00x180 No treatment
15 M 21 A +1.00+3.50x165 0.15 0.08 0 Diagnosed: 21 years old 100
Plano DS No treatment
16 M 15 A +0.50+0.50x175 −0.18 0.70 0 Diagnosed: 15 years old Suppression
+7.50+1.25x75 No treatment
17 M 19 A −1.25−0.50x065 0 0.30 0 Diagnosed: 7 years old 120
+3.50+1.25x175 (+) Patched: 4 years
18 M 21 A +3.50 DS 0.15 −0.08 0 No detection 100
Plano DS No treatment
19 M 40 A −0.50 DS 0 0.10 0 No detection 100
+2.50 DS No treatment
20 M 37 A +3.50+1.00x100 0.30 0 0 No detection 200
Plano DS No treatment
21 M 10 A +1.25 DS 0 0.70 0 Diagnosed: 8 years old 200
+4.50 DS (+) Patched: 2 years
22 M 18 A +5.00−0.50x130 0 0.10 0 No detection 200
+4.25+0.50x010 No treatment
23 F 10 AS +6.50−1.50x177 0.10 0 0* Diagnosed: 3 years old 30
+4.50−2.00x175 (+) Patched: 2 years
(+) Surgery at 7 years old
24 F 48 AS +5.00−0.50x130 0.70 0 20ET, 35ET′ Diagnosed: 6 years old Suppression
+3.25−0.75x090 (+) Patched
(+) Surgery
25 M 10 AS +1.00−0.75x005 −0.08 0.05 0* Diagnosed: 6 years old 20
+2.75−1.75x170 (+) Surgery at 5 years old
26 M 17 AS −1.25 DS 0 0.22 0* Diagnosed: 6 years old Suppression
+4.25+1.00x165 (+) Patched
(+) Surgery at 7 years old
27 M 15 AS +1.25+1.00x175 0 0.70 0, 20XT′ No detection Suppression
+6.50+2.25x165 No treatment
28 M 26 AS +5.25+2.00x165 0.52 −0.08 10XT, 15XT′ No detection Suppression
Plano DS No treatment
29 M 29 AS −1.25 DS −0.18 0.05 15ET Diagnosed: 5 years old 70
+2.00+1.00x165 (+) Patched
(+) Surgery
30 F 10 S −7.00−2.25x010 0 0.4 0* Diagnosed: 6 years old 100
−8.00−2.50x170 (+) Patched
(+) Surgery
31 F 10 S −0.50−1.50x178 0.14 0 15XT, 10XT′ (+) Surgery at 6 years old 40
−0.50−0.50x178 (+) Patched
(+) Surgery
32 F 26 S −1.75−1.00x032 −.04 0.10 10XT, 15XT′ Detection N/A 40
−4.25−0.75x161 (+) Vision training treatment
33 F 9 S −2.00−1.50x010 0.16 0 10ET, 15ET′ No detection 25
−4.00−0.50x166 No treatment
34 F 12 S +1.25 DS 0 0.10 0, 10XT′ Detection N/A 200
Plano DS (+) Patched
(+) Surgery at 7 years
35 F 16 S Plano DS 0.10 0 15XT, 10XT′ No detection 120
Plano+0.50x175 No treatment
36 F 15 S −0.50 DS 0.16 0 20ET Diagnosed: 8 years old 200
+1.25+0.50x175 (+) Surgery at 10 years old
37 F 15 S +1.00+0.50x030 0 0.22 35ET, 35ET′ No detection 400
+2.00+0.50x145 No treatment
38 F 12 S Plano DS 0 0.15 25ET, 15ET′ No detection 80
Plano DS No treatment
39 M 14 S +0.75 DS 0 0.15 30XT, 25XT′ Diagnosed: 6 years old 100
+0.75 DS No treatment
40 M 12 S +1.00 DS −0.08 0.10 30XT, 25XT′ No detection 140
−0.25 DS No treatment
41 M 12 S −0.25 DS −0.08 0.10 20ET, 15ET′ Diagnosed: 4 years old 80
+0.50 DS (+) Surgery at 6 years old
42 M 32 S +0.50 DS 0 0.15 30ET, 35ET′ No detection 70
−0.75 DS No treatment
43 F 10 S −4.00−2.75x002 0.05 0.15 15XT, 10XT′ No detection 30
−4.25−2.75x002 No treatment
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