Evaluation of a Virtual Reality implementation of a binocular imbalance test

Santiago Martín, Juan A Portela, Jian Ding, Oliver Ibarrondo, Dennis M Levi, Santiago Martín, Juan A Portela, Jian Ding, Oliver Ibarrondo, Dennis M Levi

Abstract

The purpose of this study was (1) to implement a test for binocular imbalance in a Virtual Reality headset, (2) to assess its testability, reliability and outcomes in a population of clinical patients and (3) to evaluate the relationships of interocular acuity difference, stereoacuity and binocular imbalance to amblyogenic risk factors. 100 volunteers (6 to 70 years old, mean 21.2 ± 16.2), 21 with no amblyogenic risk factors and 79 with amblyopia or a history of amblyopia participated. Participants were classified by amblyogenic risk factor (24 anisometropic, 25 strabismic and 30 mixed) and, for those with strabismus, also by refractive response (16 accommodative and 39 non-accommodative). We characterized our sample using three variables, called the 'triplet' henceforth: interocular acuity difference, stereoacuity and imbalance factor. Binocular imbalance showed high test-retest reliability (no significant difference between test and retest in a subgroup, n = 20, p = 0.831); was correlated with Worth 4 dots test (r = 0.538, p<0.0001); and correlated with both interocular acuity difference (r = 0.575, p<0.0001) and stereoacuity (r = 0.675, p<0.0001). The mean values of each variable of the triplet differed depending on group classification. Mixed and non-accommodative groups showed the worst mean values compared with the other groups. Among participants with strabismus, strabismic vs mixed subgroups did not show significant differences in any variable of the triplet, whereas the accommodative vs non-accommodative subgroups showed significant differences in all of them. According to a univariate logistic model, any variable of the triplet provides a good metric for differentiating patients from controls, except for binocular imbalance for anisometropic subgroup. The proposed binocular imbalance test is feasible and reliable. We recommend monitoring amblyopia clinically not only considering visual acuity, but also stereoacuity and interocular imbalance. Stereoacuity on its own fails because of the high percentage of patients with no measurable stereoacuity. Binocular imbalance may help to fill that gap.

Conflict of interest statement

I have read the journal's policy and the authors of this manuscript have the following competing interests: SM and JP promoted, with the support of the University of Oviedo, the creation of the startup VisionaryTool. Both have assisted VisionaryTool, S.L. (www.visionarytool.com) to create a commercial version of the VR imbalance test described in this manuscript (University of Oviedo contract FUO-EM-19-099). VisionaryTool has not had any role (writing, analysis, or control over publication) in the production of the paper. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1. Binocular imbalance test.
Fig 1. Binocular imbalance test.
Prior to the test itself, a dichoptic nonius alignment screen is presented (bottom). The test consists of a series of trials, each one divided into three steps (from bottom to top): firstly, a fusion frame of a dichoptic nine square grid surrounded by a high contrast frame is presented to facilitate fixation. After the experimenter presses the spacebar, the computer displays two dichoptic letters, randomly selected and filtered to the target interocular contrast, for 200 msec. Finally, both letters are presented binocularly one next to the other with enhanced contrast and size. The observer’s task is to indicate which letter he/she has perceived (two-alternative forced choice). The computer adjusts the imbalance ratio following a 1 up/ 1 down staircase for the next trial, until a valid threshold is obtained.
Fig 2. Binocular imbalance repeatability Bland-Altman plot.
Fig 2. Binocular imbalance repeatability Bland-Altman plot.
Binocular imbalance results in first and second measurements. N = 20 volunteers.
Fig 3. Triplet variables box plots.
Fig 3. Triplet variables box plots.
Graphical display of the continuous variables (LogMAR acuity difference, log10 stereoacuity and imbalance factor) using boxplots for each classification groups: amblyogenic factor (control, anisometropic, strabismus and mixed) and deviation nature (accommodative and non-accommodative). The box plot shows the mean and distribution in quartiles of the data. Circles represents each single participant.

References

    1. Levi DM, Knill DC, Bavelier D. Stereopsis and amblyopia: A mini-review. Vision Res. 2015;114:17–30. 10.1016/j.visres.2015.01.002
    1. Birch EE. Amblyopia and binocular vision. Prog Retin Eye Res. 2013;33:67–84. 10.1016/j.preteyeres.2012.11.001
    1. Chen AM, Cotter SA. The Amblyopia Treatment Studies: Implications for Clinical Practice. Adv Ophthalmol Optom. 2016;1:287–305. 10.1016/j.yaoo.2016.03.007
    1. Hamm LM, Black J, Dai S et al. Global processing in amblyopia: a review. Front Psychol. 2014;5:583 10.3389/fpsyg.2014.00583
    1. Ciuffreda KJ, Levi DM, Selenow A. Amblyopia: Basic and Clinical Aspects. Butterworth-Heinemann; 1991:1–64.
    1. McKee SP, Levi DM, Movshon JA. The pattern of visual deficits in amblyopia. J Vis. 2003;3:380–405. 10.1167/3.5.5
    1. Joly O, Frankó E. Neuroimaging of amblyopia and binocular vision: a review. Front Integr Neurosci. 2014;8:62 10.3389/fnint.2014.00062
    1. Harrad R. Psychophysics of suppression. Eye. 1996;10:270–273. 10.1038/eye.1996.57
    1. Hess RF, Thompson B, Baker DH. Binocular vision in amblyopia: structure, suppression and plasticity. Ophthalmic Physiol Opt. 2014;34:146–162 10.1111/opo.12123
    1. Huang C-BB, Zhou J, Lu Z-LL et al. Deficient binocular combination reveals mechanisms of anisometropic amblyopia: signal attenuation and interocular inhibition. J Vis. 2011;11:10.1167/11.6.4
    1. Mansouri B, Thompson B, Hess RF. Measurement of suprathreshold binocular interactions in amblyopia. Vision Res. 2008;48:2775–2784. 10.1016/j.visres.2008.09.002
    1. Levi DM, McKee SP, Movshon JA. Visual deficits in anisometropia. Vision Res. 2011;51:48–57. 10.1016/j.visres.2010.09.029
    1. Tidbury LP, Black RH, O’connor AR. Perceiving 3D in the absence of measurable stereo-acuity. Br Ir Orthopt J. 2014;11:34–38.
    1. Kelly KR, Jost RM, Wang YZ, et al. Improved binocular outcomes following binocular treatment for childhood amblyopia. Investig Ophthalmol Vis Sci. 2018;59:1221–1228.
    1. Gantz L, Bedell HE. Variation of Stereothreshold with Random-Dot Stereogram Density. Optom Vis Sci. 2011;88:1066–1071. 10.1097/OPX.0b013e3182217487
    1. Witz N, Hess RF. Mechanisms underlying global stereopsis in fovea and periphery. Vision Res. 2013;87:10–21. 10.1016/j.visres.2013.05.003
    1. Webber AL, Schmid KL, Baldwin AS HR. Suppression Rather Than Visual Acuity Loss Limits Stereoacuity in Amblyopia. Invest Ophthalmol Vis Sci. 2020;61:50.
    1. Webber AL, Wood JM, Thompson B, Birch EE. From suppression to stereoacuity: a composite binocular function score for clinical research. Ophthalmic Physiol Opt. 2019;39:53–62. 10.1111/opo.12599
    1. Li J, Thompson B, Lam CSY, et al. The role of suppression in amblyopia. Invest Ophthalmol Vis Sci. 2011;52:4169–4176. 10.1167/iovs.11-7233
    1. Webber AL, Wood JM, Thompson B. Fine Motor Skills of Children With Amblyopia Improve Following Binocular Treatment. Invest Ophthalmol Vis Sci. 2016;57:4713–4720. 10.1167/iovs.16-19797
    1. Birch EE, Morale SE, Jost RM, et al. Assessing suppression in amblyopic children with a dichoptic eye chart. Investig Ophthalmol Vis Sci. 2016;57:5649–5654.
    1. Black JM, Hess RF, Cooperstock JR et al. The Measurement and Treatment of Suppression in Amblyopia. J Vis Exp. 2012;70:e3927.
    1. Ding J, Klein SA, Levi DM. Binocular combination in abnormal binocular vision. J Vis. 2013;13:14.
    1. Ding J, Levi DM. Rebalancing binocular vision in amblyopia. Ophthalmic Physiol Opt. 2014;34:199 10.1111/opo.12115
    1. Babu RJ, Clavagnier SR, Bobier W et al. The regional extent of suppression: Strabismics versus nonstrabismics. Investig Ophthalmol Vis Sci. 2013;54:6585–6593.
    1. Kwon MY, Lu ZL, Miller A et al. Assessing binocular interation in amblyopia and its clinical feasibility. PLoS One. 2014;9:e100156 10.1371/journal.pone.0100156
    1. Kwon M, Wiecek E, Dakin SC et al. Spatial-frequency dependent binocular imbalance in amblyopia. Sci Rep. 2015;5:1–12.
    1. R Hess RF, Mansouri B, Thompson B. Restoration of binocular vision in amblyopia. Strabismus. 2011;19:110–118. 10.3109/09273972.2011.600418
    1. Kelly KR, Jost RM, Dao L et al. Binocular iPad Game vs Patching for Treatment of Amblyopia in Children: A Randomized Clinical Trial. JAMA Ophthalmol. 2016;134: 1402–1408. 10.1001/jamaophthalmol.2016.4224
    1. Ding J, Levi DM. Recovery of stereopsis through perceptual learning in human adults with abnormal binocular vision. Proc Natl Acad Sci U S A. 2011;108:E733–41. 10.1073/pnas.1105183108
    1. Saraiva AA, Barros MP, Nogueira AT et al. Virtual Interactive Environment for Low-Cost Treatment of Mechanical Strabismus and Amblyopia. Information. 2018;9:175.
    1. Žiak P, Holm A, Halička J et al. Amblyopia treatment of adults with dichoptic training using the virtual reality oculus rift head mounted display: Preliminary results. BMC Ophthalmol. 2017;17:105 10.1186/s12886-017-0501-8
    1. Vedamurthy I, Knill DC, Huang SJ et al. Recovering stereo vision by squashing virtual bugs in a virtual reality environment. Philos Trans R Soc LondonSeries B, Biol Sci. 2016;371:10.1098/rstb.2015.0264
    1. Li X, Yang C, Zhang G et al. Intermittent Exotropia Treatment With Dichoptic Visual Training Using a Unique Virtual Reality Platform No Title. Cyberpsychol Behav Soc Netw. 2019;22:22–30. 10.1089/cyber.2018.0259
    1. Portela-Camino JA, Martín-González S, Ruiz-Alcocer J et al. A Random Dot Computer Video Game Improves Stereopsis. Optom Vis Sci. 2018;95:523–535. 10.1097/OPX.0000000000001222
    1. Pai A MP. Prevalence of amblyopia and strabismus. Ophthalmology. 2010;117:2043–2044.
    1. Govindan M, Mohney BG, Diehl NN BJ. Incidence and types of childhood exotropia: a population-based study. Ophthalmology. 2005;112:104–108. 10.1016/j.ophtha.2004.07.033
    1. Ahn SJ, Yang HK HJ. Binocular visual acuity in intermittent exotropia: role of accommodative convergence. Am J Ophthalmol. 2012;154:981–986.e3. 10.1016/j.ajo.2012.05.026
    1. Mohney BG, Holmes JM. An office-based scale for assessing control in intermittent exotropia. Strabismus. 2006;14:147–150. 10.1080/09273970600894716
    1. Lee HJ, Kim SJ, Yu YS. Stereopsis in patients with refractive accommodative esotropia. J Am Assoc Pediatr Ophthalmol Strabismus. 2017;21:190–195.
    1. Stewart CE, Wallace MP, Cooperative MOTAS. The effect of amblyopia treatment on stereoacuity. J Am Assoc Pediatr Ophthalmol Strabismus. 2013;17:166–173.
    1. Holmes JM, Leske DA, Hohberger GG. Defining real change in prism-cover test measurements. Am J Ophthalmol. 2008;145:381–385. 10.1016/j.ajo.2007.09.012
    1. Dodgson N. Variation and extrema of human interpupillary distance. Stereosc Displays Virtual Real Syst XI. 2004;5291:36–46.
    1. Organization WH. Child growth standards, Head circumference-for-age. .
    1. Chopin A, Bavelier D, Levi DM. The prevalence and diagnosis of ‘stereoblindness’ in adults less than 60 years of age: a best evidence synthesis. Ophthalmic Physiol Opt. 2019;39:66–85. 10.1111/opo.12607
    1. Chung STL, Levi DM, Legge GE et al. Spatial-frequency properties of letter identification in amblyopia. Vision Res. 2002;42:1571–1581. 10.1016/s0042-6989(02)00065-2
    1. Chung STL, Tjan BS. Spatial-frequency and contrast properties of reading in central and peripheral vision. J Vis. 2009;9:16–16.
    1. Jones J.A, Krum D.M. The effect of eye position on the view of virtual geometry. IEEE Virtual Real. 2014:87–88.
    1. Woods A. J., Merritt J. O., Benton et al. Stereoscopic Displays and Virtual Reality Systems XI. Stereosc Displays Virtual Real Syst XI. 2004;5921:36–46.
    1. Bossi M, Hamm LM, Dahlmann-Noor A DS. A comparison of tests for quantifying sensory eye dominance. Vis Res. 2018;153:60–69. 10.1016/j.visres.2018.09.006
    1. Babu RJ, Clavagnier S, Bobier WR et al. Regional extent of peripheral suppression in amblyopia. Investig Ophthalmol Vis Sci. 2017;58:2329–2340.
    1. Liu XY, Zhang JY. Dichoptic training in adults with amblyopia: Additional stereoacuity gains over monocular training. Vision Res. 2018;152:84–90. 10.1016/j.visres.2017.07.002
    1. Read JCA. Stereo Vision and Strabismus. Eye. 2015;29:214–224. 10.1038/eye.2014.279
    1. Birch EE, Wang J. Stereoacuity outcomes after treatment of infantile and accommodative esotropia. Optom Vis Sci. 2009;86:647–652. 10.1097/OPX.0b013e3181a6168d

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