Suppression Rather Than Visual Acuity Loss Limits Stereoacuity in Amblyopia
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Eye Movements, Strabismus, Amblyopia and Neuro-Ophthalmology Suppression Rather Than Visual Acuity Loss Limits Stereoacuity in Amblyopia Ann L. Webber,1 Katrina L. Schmid,1 Alex S. Baldwin,2 and Robert F. Hess2 1School of Optometry & Vision Sciences and Institute of Health & Biomedical Innovation, Queensland University of Technology (QUT), Kelvin Grove, Queensland, Australia 2Department of Ophthalmology & Visual Sciences, McGill University, Montreal, Quebec, Canada Correspondence: Ann L. Webber, PURPOSE. To investigate the influence of interocular suppression and visual acuity loss on School of Optometry & Vision stereoacuity in observers with and without abnormal vision development from strabismus Science and Institute of Health & or amblyopia. To determine whether stereoacuity improves in amblyopic observers when Biomedical Innovation, Queensland suppression is neutralized. University of Technology (QUT), 60 Musk Avenue, Kelvin Grove, METHODS. Experiment 1: Visual acuity (VA), depth of suppression (contrast ratio Queensland, 4059 Australia; [CR]), and stereoacuity (digital random-dot) were tested in adult amblyopic observers [email protected]. (n = 21; age 27 ± 11 years). Experiment 2: VA, stereoacuity, and CR were measured Received: October 3, 2019 at baseline and through a series of monocular contrast attenuation and Bangerter filter Accepted: April 16, 2020 conditions that degrade visual input in participants with normal binocular vision (n = 19; Published: June 24, 2020 age 31 ± 13 years). Multiple regression models were used to determine relative contribu- tion of VA and CR to stereoacuity in both groups. Experiment 3: stereoacuity was retested Citation: Webber AL, Schmid KL, = Baldwin AS, Hess RF. Suppression in a subsample of amblyopic observers (n 7) after contrast reduction of the stimulus rather than visual acuity loss limits presented to dominant eye to neutralize suppression. stereoacuity in amblyopia. Invest RESULTS. In amblyopic observers, stereoacuity significantly correlated with CR Ophthalmol Vis Sci. 2020;61(6):50. (P < 0.001), but not with interocular VA difference (P = 0.863). In participants with https://doi.org/10.1167/iovs.61.6.50 normal vision development, stereoacuity, VA, and CR declined with introduction of monocular Bangerter filterP ( < 0.001), and stereoacuity reduced with monocular attenu- ation of stimulus contrast (P < 0.001). Reduction in stereoacuity correlated with both VA decrement and degraded CR. Stereoacuity significantly improved in amblyopic observers when the contrast to the dominant eye was adjusted based on the contrast ratio. CONCLUSIONS. Suppression rather than visual acuity loss limits stereoacuity in observers with abnormal vision development. Stereopsis can be improved when interocular sensory dominance is neutralized. Keywords: stereopsis, suppression, stereoacuity, amblyopia, visual acuity mblyopia is a developmental disorder of the visual or lens anomalies, with both blur and contrast differences A system in the brain. In most cases, patients suffering known to degrade stereoacuity.10 Stereoacuity also requires from amblyopia will have reduced visual acuity in one eye. accurate ocular alignment so that the dichoptic images stim- There is a degree to which the brain suppresses (or ignores) ulate corresponding retinal areas for the perception of fused the visual signal from that eye. This typically results in single vision.2 reduced or absent stereopsis (binocular depth perception). Nonconcordance of retinal images from ocular media Stereopsis, the ability to perceive the depth of an object obstruction, high anisometropic refractive error or strabis- relative to an observer, arises from the binocular sensory mus early in life will interrupt the neurodevelopment of the fusion of slightly dissimilar retinal images that have hori- visual system and cause amblyopia.11 Patients with ambly- zontal disparity by virtue of the lateral separation of the opia may have nonrecoverable reduced visual acuity, may two eyes.1,2 Stereoacuity, reported in minutes or seconds of suppress or ignore the visual signal from one eye and are arc, describes the smallest horizontal disparity in binocular likely to have reduced or absent stereopsis (binocular depth images that leads to the perception of depth in the observed vision).12–15 In addition to visual acuity and stereoacuity loss, stimulus. In observers with equal normal visual acuity and amblyopia results in impaired position discrimination and normal vision development, stereoacuity thresholds are typi- contrast sensitivity11 and, furthermore, may be associated cally of 20 to 40 seconds of arc.2–4 Stereoacuity will be with higher order functional and processing impairments worse when there are significant differences in the retinal that suggest visual neurodevelopmental retardation beyond images between eyes, that is, if the dichoptic images differ the primary visual cortex.16–18 in contrast, size, or clarity.5–9 Differences in retinal image Interocular suppression of visual information from the clarity and size can occur if there is unequal refractive error amblyopic eye is frequently reported in amblyopia,13,19 (anisometropia) or ocular media obstruction from corneal presumably to compensate for conflicting visual input.20 As Copyright 2020 The Authors iovs.arvojournals.org | ISSN: 1552-5783 1 This work is licensed under a Creative Commons Attribution 4.0 International License. Downloaded from iovs.arvojournals.org on 09/29/2021 Suppression Limits Stereoacuity in Amblyopia IOVS | June 2020 | Vol. 61 | No. 6 | Article 50 | 2 well as limiting stereopsis by preventing sensory fusion,21 simulation of the monocular acuity loss) should be more the role that suppression plays in causing or limiting ambly- correlated with stereoacuity than with monocular contrast opia recovery is yet to be fully determined. Novel treat- attenuation (our simulation of the interocular suppressive ments for amblyopia are aimed at reducing suppression of imbalance). In the case that stereopsis is more affected the amblyopic visual pathway to improve binocularity22–25; by the binocular suppressive imbalance, then the reverse however, the relative contribution of interocular differences would be the case; stereoacuity would be more impacted in visual acuity and depth of suppression in determin- by the interocular contrast difference. Finally, stereoacuity ing the limit of stereoacuity is unclear. For example, it was retested in a subset of amblyopic participants with has been believed for some time that amblyopia (reduced the contrast of the stimulus presented to the dominant acuity in one eye) is the primary problem and loss of eye reduced, proportional to the determined interocular binocularity, the consequence. However, more recently it dominance, to counter suppression. For amblyopic partic- has been suggested that it is the other way around13,26,27; ipants the prediction was that if stereopsis were limited loss of binocularity is the primary problem and amblyopia mainly by suppression, then by neutralizing suppression the consequence. According to the former explanation one by altering the contrast, stereoacuity would be expected to would expect an inverse relationship between suppression improve. and acuity loss; the more amblyopic the eye, the less it This study had three aims: (1) to determine the rela- needs to be suppressed to ensure it does not interfere in tive strength of association between reduced visual acuity, binocular vision. On the other hand, the latter explanation the depth of suppression (contrast balance) and the would assume a direct relationship, whereby the greater the stereoacuity in observers with abnormal binocular vision suppression the greater the resultant amblyopia. A number development (this directly bears on the etiology), (2) of studies have shown that there is a direct relationship to determine the relative contribution of induced visual between suppression and acuity loss in amblyopia.4,15 Quite acuity or interocular dominance deficits to stereoacuity apart from these interrelationships in amblyopia, it would be loss when vision is monocularly impaired in observers of value to know the extent to which sensory eye dominance with normal vision development, and (3) to determine and stereopsis are correlated in the normal binocular popu- whether stereoacuity improves in amblyopic observers when lation and the extent to which degraded monocular input interocular dominance balance is altered to neutralize affects ocular sensory dominance and stereopsis. suppression. In this study we seek to make a distinction between simulations of acuity-like losses and suppressive-like losses. From what we know about the contrast sensitivity deficit in METHODS amblyopia,28–30 the higher the spatial frequency, the greater Participants the loss. It is like a lowpass filtering, and the resultant loss in acuity would be simulated by an increased slope of the Adult participants were prospectively recruited for a study of amplitude spectrum. We use the Bangerter filters in normal binocular vision perception. All had a comprehensive vision participants to simulate the amblyopic loss.31,32 Suppression and intraocular health exam (previous treatment history, affects low as well as high spatial frequencies33 and is best visual acuity (electronic Early Treatment of Diabetic Study simulated by a vertical translation of the 1/f amplitude spec- e-ETDRS and near logMAR), clinical stereoacuity (Randot trum line. It is the standard metric used to quantify suppres-