Eye Movements, Strabismus, Amblyopia, and Neuro-Ophthalmology The Role of Suppression in Amblyopia Jingrong Li,1 Benjamin Thompson,2 Carly S. Y. Lam,3,4 Daming Deng,1 Lily Y. L. Chan,3,4 Goro Maehara,5 George C. Woo,3 Minbin Yu,1 and Robert F. Hess5 PURPOSE. This study had three main goals: to assess the degree uppression plays a key role in the amblyopic syndrome. Its of suppression in patients with strabismic, anisometropic, and Sclinical importance was recognized more than 60 years ago mixed amblyopia; to establish the relationship between sup- by the pioneering work of Travers,1 Jampolsky,2 and later, pression and the degree of amblyopia; and to compare the Pratt-Johnson and Wee,3,4 who showed that its regional distri- degree of suppression across the clinical subgroups within the bution (visual field topography) depends on the type of stra- sample. bismus present. More recently, this approach has been carried on by Joosse et al.5–7 whose innovative work has highlighted METHODS. Using both standard measures of suppression (Bago- the different types of suppression that occur in strabismic lini lenses and neutral density [ND] filters, Worth 4-Dot test) amblyopia and how it varies within any one strabismic subpop- and a new approach involving the measurement of dichoptic ulation. motion thresholds under conditions of variable interocular Although we now have a better idea of the position and contrast, the degree of suppression in 43 amblyopic patients shape of suppressed scotomata, we are still ignorant of their with strabismus, anisometropia, or a combination of both was role and importance in the amblyopia syndrome, a condition in quantified. which there is loss of vision of a nonorganic nature, secondary RESULTS. There was good agreement between the quantitative to strabismus, anisometropia or form deprivation. There are measures of suppression made with the new dichoptic motion some fundamental questions that remain unanswered, the threshold technique and measurements made with standard most important of which relates to whether suppression is of clinical techniques (Bagolini lenses and ND filters, Worth 4-Dot primary or secondary importance to amblyopia. For example, test). The degree of suppression was found to correlate directly suppression could simply follow as a consequence of amblyo- with the degree of amblyopia within our clinical sample, pia as a way of ensuring that the input from a weaker eye does whereby stronger suppression was associated with a greater not disrupt binocular perception. This view is compatible with current treatment approaches that focus on patching or penal- difference in interocular acuity and poorer stereoacuity. Sup- ization as a first step without any regard for suppression, which pression was not related to the type or angle of strabismus is often not quantified clinically and is rarely treated as a when this was present or the previous treatment history. separate entity. The idea that amblyopia and suppression are CONCLUSIONS. These results suggest that suppression may have separate entities gains some support from the suggestion that a primary role in the amblyopia syndrome and therefore have there is a reciprocal relationship between the strength of implications for the treatment of amblyopia. (Invest Ophthal- suppression and the degree of amblyopia; the greater the mol Vis Sci. 2011;52:4169–4176) DOI:10.1167/iovs.11-7233 amblyopia, the less suppression is needed to eliminate that eye’s input from the binocular mix.8 The opposite view, how- ever, is that suppression causes the visual dysfunction in am- blyopia. In this scenario, the suppression develops due to a 1 From the State Key Laboratory of Ophthalmology, Zhongshan disruption of binocular function (strabismus or anisometropia), Ophthalmic Center, Sun Yat-sen University, Guangzhou, People’s Re- and it is the chronic suppression itself that results in amblyo- public of China; the 2Department of Optometry and Vision Science, Faculty of Science, The University of Auckland, Auckland, New Zea- pia. This alternative view gains some support from the recent land; the 3School of Optometry, and the 4The Hong Kong Jockey Club finding that, even in adults using repetitive transcranial mag- Sports Medicine and Health Sciences Centre, Faculty of Health and netic stimulation (rTMS), a noninvasive means of transiently Social Sciences, The Hong Kong Polytechnic University, Hong Kong altering neural excitability in the human cortex, a 10-minute SAR, China; and the 5Department of Ophthalmology, McGill Univer- application of TMS can temporarily improve contrast sensitiv- sity, Montreal, Quebec, Canada. ity in amblyopia,9 suggesting that visual function is not lost but Supported by equipment/resources donated by The Hong Kong suppressed. Further support comes from the finding that anti- Jockey Club Charities Trust, Hong Kong Polytechnic University Inter- suppression therapy not only results in improved binocular nal Competitive Research Grant CRG G-YH71 (CSYL), University of function but also in improved monocular functioning of the Auckland Faculty Development Research Fund Award (BT), CIHR 10 Grants MOP 53346 and PPP93073 (RFH), the Fundamental Research adult amblyopic eye. However, before one can accept that Funds of the State Key Lab of Ophthalmology, Sun Yat-sen University suppression is of primary importance in the amblyopic syn- (JL), a Thrasher Research Fund Early Career Award (JL), and the drome, the issue of the relationship between the degree of Guangdong Province International Collaboration Project Grant amblyopia and the strength of suppression should be re- 2010B050100014 (DD). opened, for it is only if there is a direct relationship between Submitted for publication January 15, 2011; revised February 27, these two clinical features that it would be reasonable to 2011; accepted March 16, 2011. assume that suppression is of primary importance. The present Disclosure: J. Li, None; B. Thompson, None; C.S.Y. Lam, None; support for a reciprocal relationship rests on only a small , None; , None; , None; , D. Deng L.Y.L. Chan G. Maehara G.C. Woo sample of patients with clinical suppression (n ϭ 10), only two None; M. Yu, None; R.F. Hess, None of whom had visual acuity worse than 20/30 in the amblyopic Corresponding author: Minbin Yu, Department of Glaucoma, De- 8 partment of Optometry and Vision Science, Zhongshan Ophthalmic eye. Center, Guangzhou 510060, People’s Republic of China; Recently a novel method of quantifying binocular combina- [email protected]. tion in the normal visual system has been developed,11 and we Investigative Ophthalmology & Visual Science, June 2011, Vol. 52, No. 7 Copyright 2011 The Association for Research in Vision and Ophthalmology, Inc. 4169 Downloaded from jov.arvojournals.org on 09/25/2021 4170 Li et al. IOVS, June 2011, Vol. 52, No. 7 have applied it to quantifying the strength of suppression in Suppression Measurement both strabismic and anisometropic amblyopes,12,13 using a global motion stimulus in which signal elements moving in a The Worth-4-Dot Test. The Worth-4-Dot test was performed at coherent direction are seen by one eye and noise elements near (33 cm) and far (6 m) test distances. The filters were placed, moving in random directions are seen by the other eye. This according to convention: red over the right eye and green over the left method is an accurate way, within the context of signal/noise eye. To ensure the visibility of each filter, the participants’ eyes were analysis, of measuring12,13 and treating10 suppression within covered alternately to ensure that each eye was visibly aware of the red the central field. In this study we used this approach to assess and green filters. When this testing was performed monocularly, all the strength of suppression in a group of anisometropic, participants reported seeing two red dots when the left eye was mixed, and strabismic amblyopes. The method provides a occluded (right eye wearing the red filter) and three green dots when more quantitative means (better resolution) of measuring the the right eye was occluded (left eye wearing the green filter). Partici- degree of suppression compared with the Worth 4-Dot test or pants were asked to report the number and color of the dots they saw Ͻ the use of a red filter and neutral density wedge. We first under photopic (118 lux) followed by scotopic ( 0.1 lux) conditions. assessed the relationship between this new signal/noise A scoring system was assigned to grade the depth and the size of the method that can precisely quantify suppression and more tra- suppression scotoma. For example, a four-dot response with the white ditional, relatively coarse, measures of suppression (Worth dot at the bottom was given a score of 0 (no suppression), while a two- 4-Dot test and modified Bagolini test). We then addressed the or three-dot response received a score of 2 (complete suppression). A following two questions: What is the relationship between score of 1 (partial suppression) was assigned to observers who re- visual losses in amblyopia (acuity and stereo) and the degree of ported that they saw four dots, with the color of the bottom white dot suppression? How does suppression vary within the amblyopic being perceived as either green or red. The sum of near and far scores, clinical population? The answers to these questions bear on the which could range from 0 to 4, was used to represent the overall level issue of whether suppression plays a causal role in the visual of suppression as measured by this test, as we found no reliable ϭ loss that characterizes amblyopia. 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 METHODS was assessed by combining the Bagolini striated lenses test with neu- tral-density (ND) filters.15 Each observer viewed a light source (30 Participants cd/m2) held at 33 cm while wearing Bagolini striated lenses under low ambient room illumination (5 lux).