Abstract
Purpose:
Binocular discordance due to strabismus, anisometropia, or both may result in not only monocular visual acuity deficits, but also in motion perception deficits. We determined the prevalence of fellow-eye deficits in motion-defined form (MDF) perception, the ability to identify a two-dimensional (2D) shape defined by motion rather than luminance contrast. We also examined the following: the causative role of reduced visual acuity and binocularity, associations with clinical and sensory factors, and effectiveness of binocular amblyopia treatment in alleviating deficits.
Methods:
Participants included 91 children with residual amblyopia (strabismic, anisometropic, or both; age, 9.0 ± 1.7 years), 79 nonamblyopic children with treated strabismus or anisometropia (age, 8.5 ± 2.1 years), and 20 controls (age, 8.6 ± 1.5 years). MDF coherence thresholds, visual acuity, stereoacuity, and interocular suppression were measured.
Results:
MDF deficits, relative to controls, were present in the fellow eye of 23% of children with residual amblyopia and 20% of nonamblyopic children. Stereoacuity and age first patched were correlated with MDF threshold (r = 0.29, 95% CI: 0.09–0.47; r = −0.33, 95% CI: −0.13 to −0.50, respectively). MDF deficits were more common in children treated with patching alone than in those receiving contrast-rebalanced binocular treatment with games or movies (t89 = 3.46; P = 0.0008). The latter was associated with a reduction in mean fellow eye MDF threshold (t26 = 6.32, P < 0.0001).
Conclusions:
Fellow eye MDF deficits are common and likely reflect abnormalities in binocular cortical mechanisms that result from early discordant visual experience. Binocular amblyopia treatment, which is effective in improving amblyopic eye visual acuity, appears to provide a benefit for the fellow eye.
Binocularly discordant visual experience during early childhood can result not only in a monocular visual acuity deficit (amblyopia), but can also affect perception with the fellow eye, possibly due to abnormal development of binocular neurons that can be stimulated by either eye. Altered development may occur when childhood strabismus or anisometropia induce abnormal binocular interactions, interocular competition, and/or interocular suppression.
1–4 Our understanding of the effects of binocularly discordant experience on fellow eye visual function is limited, and whether fellow eye deficits can be targeted to improve treatment outcomes remains to be determined.
One widely appreciated consequence of binocularly discordant visual experience is the subnormal or nil stereoacuity that typically accompanies amblyopia and often is resistant to rehabilitation by patching treatment.
5–7 Measurement of stereoacuity does not allow the effects of discordant binocular visual experience on the amblyopic and fellow eyes to be examined separately; disparity detection inherently relies on comparison of inputs from both eyes. However, a subset of binocular cortical functions may provide insight into the effect of discordant binocular experience on the fellow eye, namely, binocular neurons that respond regardless of eye of origin.
Some neurons in V2
8 and most neurons in MT
9 respond to stimulation through either eye. In animal models of amblyopia these neurons show spiking irregularities,
10 disrupted receptive field structure
8 and abnormally high neuronal variability
9 when driven by either the amblyopic eye or the fellow eye. These neuronal abnormalities correlate with the level of interocular suppression, as well as with the level of perceptual loss of contrast sensitivity or motion sensitivity in amblyopic monkeys, and they have been attributed to abnormal binocular interactions during early development.
The human homolog of MT, hMT/V5 has been implicated in the perception of motion-defined form
11–13 (i.e., the ability to identify a two-dimensional [2D] shape defined by motion rather than luminance contrast).
14–18 These neurons may not develop normally if they receive degraded information from one eye.
9
Up to 40% of amblyopic children have been reported to have a fellow eye deficit in perceiving motion-defined form (MDF).
16,19,20 It has also been reported that fellow eye MDF deficits were resistant to rehabilitation by patching.
16 However, the sample sizes in these studies were small and included only amblyopic children and controls. As a result, it is unclear whether amblyopia or impaired binocular function was the primary causative factor for fellow eye MDF deficits. To address this limitation, three cohorts of children were evaluated: (1) amblyopic children, (2) nonamblyopic children who have been treated for strabismus, anisometropia, or both, and (3) control children. Amblyopic children have reduced visual acuity in the nonpreferred eye and impaired binocular function. Nonamblyopic children who have been treated for strabismus, anisometropia, or both have normal visual acuity but impaired binocular function. If the primary causative factor for fellow eye MDF deficits is amblyopia, amblyopic children should differ in prevalence and severity of MDF deficits compared with nonamblyopic children and controls. If the primary causative factor for fellow eye MDF deficits is impaired binocular function, both amblyopic and nonamblyopic children should differ in prevalence and severity of MDF deficits compared to controls.
This study had four aims: (1) determine the prevalence of fellow eye MDF deficits among amblyopic and nonamblyopic children treated for strabismus, anisometropia, or both, (2) determine whether reduced visual acuity (amblyopia) or reduced binocularity is the causative factor for fellow eye deficits, (3) investigate clinical and sensory factors that may be associated with risk for fellow eye MDF deficits in amblyopia, and (4) evaluate whether MDF deficits in amblyopic children can be ameliorated with binocular amblyopia treatment.
Of the three sensory indices of severity of amblyopia evaluated for the amblyopic children (amblyopic eye BCVA, stereoacuity, and suppression CBI), only stereoacuity was significantly correlated with MDF threshold (r = 0.29, 95% CI: 0.09–0.47). Only 1 of 25 (4%) of amblyopic children with measurable stereoacuity had a fellow eye MDF deficit, whereas a significantly higher proportion of amblyopic children with nil stereoacuity had fellow eye MDF deficits (19 of 66; 29%; 95% CI for difference in proportions: 7%–37%). Interestingly, there was a similar pattern of prevalence among nonamblyopic children. Only 3 of 43 (7%) of nonamblyopic children with measurable stereoacuity had a fellow eye MDF deficit, whereas a significantly higher proportion of nonamblyopic children with nil stereoacuity had fellow eye deficits (13 of 36; 36%; 95% CI for difference in proportions: 11%–46%).
The proportion of amblyopic children with a fellow eye MDF deficit was higher by a factor of 2 for combined mechanism amblyopia (10 of 30; 30%) compared with anisometropic amblyopia (6 of 41; 15%) or with strabismic amblyopia (4 of 23; 17%), but this difference was not statistically significant (95% CI for difference in proportions: 0%–38% and 0%–37%, respectively;
Fig. 3). Mean (±SD) fellow eye MDF threshold was significantly elevated for combined mechanism amblyopia compared with anisometropic amblyopia (32% vs. 23%,
P = 0.01). Of the three additional clinical factors examined (age first patched, duration of patching, lines of BCVA improvement with patching), only age first patched was linearly correlated with MDF threshold (age first patched:
r = −0.33, 95% CI: −0.13 to −0.50; duration of patching:
r = 0.16, 95% CI: −0.05 to 0.35; lines of BCVA improvement:
r = −0.04, 95% CI: −0.24 to 0.17); the earlier the child started patching treatment, the more severe the fellow eye MDF deficit.
Does Reduced Visual Acuity (Amblyopia) or Impaired Binocular Function Cause Fellow Eye MDF Deficits?
Can Fellow Eye MDF Deficits in Amblyopic Children Ameliorated With Binocular Amblyopia Treatment?
Supported in part by Thrasher Research Fund Grant TRF13441 and National Eye Institute Grant EY022313.
Disclosure: E.E. Birch, None; R.M. Jost, None; Y.-Z. Wang, None; K.R. Kelly, None; D.E. Giaschi, None