Dichoptic Perceptual Training in Children With Amblyopia With or Without Patching History

Xiang-Yun Liu, Yu-Wei Zhang, Feng Gao, Fei Chen, Jun-Yun Zhang, Xiang-Yun Liu, Yu-Wei Zhang, Feng Gao, Fei Chen, Jun-Yun Zhang

Abstract

Purpose: Dichoptic training is becoming a popular tool in amblyopia treatment. Here we investigated the effects of dichoptic demasking training in children with amblyopia who never received patching treatment (NPT group) or were no longer responsive to patching (PT group).

Methods: Fourteen NPT and thirteen PT amblyopes (6-16.5 years; 24 anisometropic, two strabismus, and one mixed) received dichoptic demasking training for 17 to 22 sessions. They used the amblyopic eye (AE) to practice contrast discrimination between a pair of Gabors that were dichoptically masked by a band-filtered noise pattern simultaneously presented in the fellow eye (FE). Dichoptic learning was quantified by the increase of maximal tolerable noise contrast (TNC) for AE contrast discrimination. Computerized visual acuities and contrast sensitivity functions for both eyes and the Randot stereoacuity were measured before and after training.

Results: Training improved maximal TNC by six to eight times in both groups, along with a boost of AE acuities by 0.15 logMAR (P < 0.001) in the NPT group and 0.06 logMAR (P < 0.001) in the PT group. This visual acuity improvement was significantly dependent on the pretraining acuity. Stereoacuity was significantly improved by 41.6% (P = 0.002) in the NPT group and 64.2% (P < 0.001) in the PT group. The stereoacuity gain was correlated to the pretraining interocular acuity difference (r = -0.49, P = 0.010), but not to the interocular acuity difference change (r = -0.28, P = 0.15). Training improved AE contrast sensitivity in the NPT group (P = 0.009) but not the PT group (P = 0.76). Moreover, the learning effects in 12 retested observers were retained for 10 to 24 months.

Conclusions: Dichoptic training can improve, and sometimes even restore, the stereoacuity of amblyopic children, especially those with mild amblyopia (amblyopic VA ≦0.28 logMAR). The dissociation of stereoacuity gain and the interocular acuity difference change suggests that the stereoacuity gain may not result from a reduced interocular suppression in most amblyopes. Rather, the amblyopes may have learned to attend to, or readout, the stimulus information to improve stereopsis.

Conflict of interest statement

Disclosure: X.-Y. Liu, None; Y.-W. Zhang, None; F. Gao, None; F. Chen, None; J.-Y. Zhang, None

Figures

Figure 1.
Figure 1.
(A) A flowchart of the study design. Two groups of observers (NPT and PT) were recruited according to their treatment history. The experiment consisted of pretraining assessment, dichoptic demasking training, and posttraining assessment. (B) Visual function assessment. Top: Single-E and crowded-E acuities test; Middle: A Gabor patch used for contrast sensitivity measurement. Bottom: The Randot Stereo Test. (C) The dichoptic training paradigm of a contrast discrimination task. From top-left to bottom-right: binocular fusion was first achieved with the assistance of two half-crosses. Then a cue was presented for 200 ms to prime AE. A pair of collinear Gabors were then presented to AE for 200 ms, whereas a bandpass noise masker was presented to FE simultaneously. Observers judged which Gabor had higher contrast. AE, amblyopic eye; FE, fellow eye; NPT, never patch-treated; PT, patch-treated.
Figure 2.
Figure 2.
The effects of dichoptic de-masking training on maximal TNC for AE contrast discrimination task. (A) Session by session changes of the mean maximal TNC for AE contrast discrimination in NPT and PT groups. The lines are the best-fitting exponential functions. (B) Comparisons of individual and mean posttraining and pretraining maximal TNCs. The large symbols represent the group means. (C) Mean percent improvement of performance in NPT and PT groups. (D) Dichoptic demasking learning as a function of pretraining maximal TNC. Data are plotted on a logarithmic scale, and a Deming regression line is plotted. (E) Maximal TNC as a function of training sessions for all observers. In each panel, the line is the exponential fit of the data. Error bars = 1 SEM. AE, amblyopic eye; NPT, never patch-treated; PT, patch-treated; TNC, tolerable noise contrast.
Figure 3.
Figure 3.
The impact of dichoptic training on visual acuities. (A) Pretraining and posttraining single-E and crowded E-acuities for NPT AEs and PT AEs. The filled symbols indicate group means. The digits indicate individual observers (see Tables 1 and 2). Because one PT observer (SA13) did not complete the pretraining computerized-E acuity assessment, his/her data were not included here. The mean of the PT group was based on the other 12 observers. (B) Mean acuity improvement of NPT and PT AEs and FEs. We also replotted data from our previous study for comparison. Error bars = 1 SEM. (C) The correlation between AE acuity improvement and pretraining AE acuity. The solid line shows Deming regression for all observers. Three strabismic observers were indicated by the letter “s.” (D) The correlation between the interocular acuity difference reduction and the pretraining interocular acuity difference. The solid line shows Deming regression for all observers. (E) The visual acuity improvement versus dichoptic demasking learning. (F) The visual acuity improvement versus age. AE, amblyopic eye; FE, fellow eye; NPT, never patch-treated; PT, patch-treated.
Figure 4.
Figure 4.
The impact of dichoptic training on stereoacuity. (A) Pretraining and posttraining stereoacuity for NPT and PT groups. The large symbols indicate group means. The digits indicate individual observers (see Tables 1 and 2). The arrows on the y-axis indicate amblyopic observers who failed the Randot Stereo Test (stereoblind). Their stereoacuity was set at 500 arcsec, the lowest score, for data analysis. (B) Mean improvement of stereoacuity. Left: NPT and PT groups in the current study. Right: Replotted NPT and PT data after monocular training in a previous study.Error bars = 1 SEM. (C) The improvement of stereoacuity as a function of the pre-training interocular acuity difference. The line shows a Deming regression fitting. Strabismic observers are indicated by the letter “s.” (DH) The improvement of stereoacuity against the reduction of interocular acuity difference (D), the improvement of dichoptic demasking training (E), the improvement of visual acuity (F), the pretraining stereoacuity (G), and children age (H). NPT, never patch-treated; PT, patch-treated.
Figure 5.
Figure 5.
The impact of dichoptic training on contrast sensitivity functions. (A, B) The mean contrast sensitivity functions of the AEs and FEs before and after training in NPT (A) and PT (B) groups, along with individual data points. Each curve is the best fitting of a difference-of-Gaussian function. (C) The mean contrast sensitivity functions for AEs and FEs before and after training, with stimulus spatial frequencies normalized by the corresponding cutoff spatial frequencies. (D) The ratios of the pretraining and posttraining normalized contrast sensitivity functions in AEs and FEs. Error bars = 1 SEM. AE, amblyopic eye; FE, fellow eye; NPT, never patch-treated; PT, patch-treated.

References

    1. Birch EE. Amblyopia and binocular vision. Progr Retinal Eye Res. 2013; 33: 67–84.
    1. Kiorpes L, Kiper DC, O'Keefe LP, Cavanaugh JR, Movshon JA. Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. J Neurosci. 1998; 18: 6411–6424.
    1. Harrad R, Sengpiel F, Blakemore C. Physiology of suppression in strabismic amblyopia. Br J Ophthalmol. 1996; 80: 373–377.
    1. Shooner C, Hallum LE, Kumbhani RD, et al. .. Asymmetric dichoptic masking in visual cortex of amblyopic macaque monkeys. J Neurosci. 2017; 37: 8734–8741.
    1. Sengpiel F, Blakemore C. The neural basis of suppression and amblyopia in strabismus. Eye (Lond). 1996; 10(Pt 2): 250–258.
    1. Wiesel TN, Hubel DH. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol. 1963; 26: 1003–1017.
    1. Hess RF, Thompson B, Baker DH. Binocular vision in amblyopia: structure, suppression and plasticity. Ophthalmic Physiol Opt. 2014; 34: 146–162.
    1. McKee SP, Levi DM, Movshon JA. The pattern of visual deficits in amblyopia. J Vis. 2003; 3: 380–405.
    1. Giaschi D, Lo R, Narasimhan S, Lyons C, Wilcox LM. Sparing of coarse stereopsis in stereodeficient children with a history of amblyopia. J Vis. 2013; 13(10): 17.
    1. Scheiman MM, Hertle RW, Beck RW, et al. .. Randomized trial of treatment of amblyopia in children aged 7 to 17 years. Arch Ophthalmol. 2005; 123: 437–447.
    1. Wallace DK, Lazar EL, Melia M, et al. .. Stereoacuity in children with anisometropic amblyopia. J AAPOS. 2011; 15: 455–461.
    1. Birch EE, Wang J. Stereoacuity outcomes after treatment of infantile and accommodative esotropia. Optom Vis Sci. 2009; 86: 647–652.
    1. Wong AM New concepts concerning the neural mechanisms of amblyopia and their clinical implications. Can J Ophthalmol. 2012; 47: 399–409.
    1. Pediatric Eye Disease Investigator Group Writing, C, Rutstein RP, Quinn GE, Lazar EL, et al. .. A randomized trial comparing Bangerter filters and patching for the treatment of moderate amblyopia in children. Ophthalmology. 2010; 117: 998–1004 e1006.
    1. Levi DM, Knill DC, Bavelier D. Stereopsis and amblyopia: a mini-review. Vision Res. 2015; 114: 17–30.
    1. Liu XY, Zhang T, Jia YL, Wang NL, Yu C. The therapeutic impact of perceptual learning on juvenile amblyopia with or without previous patching treatment. Invest Ophthalmol Vis Sci. 2011; 52: 1531–1538.
    1. Li RW, Provost A, Levi DM. Extended perceptual learning results in substantial recovery of positional acuity and visual acuity in juvenile amblyopia. Invest Ophthalmol Vis Sci. 2007; 48: 5046–5051.
    1. Polat U, Ma-Naim T, Spierer A. Treatment of children with amblyopia by perceptual learning. Vision Res. 2009; 49: 2599–2603.
    1. Polat U, Ma-Naim T, Belkin M, Sagi D. Improving vision in adult amblyopia by perceptual learning. Proc Natl Acad Sci USA. 2004; 101: 6692–6697.
    1. Levi DM, Polat U. Neural plasticity in adults with amblyopia. Proc Natl Acad Sci USA. 1996; 93: 6830–6834.
    1. Ding J, Levi DM. Recovery of stereopsis through perceptual learning in human adults with abnormal binocular vision. Proc Natl Acad Sci USA. 2011; 108: E733–741.
    1. Astle AT, McGraw PV, Webb BS. Recovery of stereo acuity in adults with amblyopia. BMJ Case Rep. 2011; 2011: bcr0720103143.
    1. Xi J, Jia WL, Feng LX, Lu ZL, Huang CB. Perceptual learning improves stereoacuity in amblyopia. Invest Ophthalmol Vis Sci 2014, 55, 2384–2391.
    1. Hess RF, Mansouri B, Thompson B. A new binocular approach to the treatment of amblyopia in adults well beyond the critical period of visual development. Restor Neurol Neurosci. 2010; 28: 793–802.
    1. Hess RF, Mansouri B, Thompson B. A binocular approach to treating amblyopia: antisuppression therapy. Optom Vis Sci. 2010; 87: 697–704.
    1. Li J, Thompson B, Deng D, Chan LY, Yu M, Hess RF. Dichoptic training enables the adult amblyopic brain to learn. Curr Biol. 2013; 23: R308–309.
    1. Vedamurthy I, Nahum M, Huang SJ, et al. .. A dichoptic custom-made action video game as a treatment for adult amblyopia. Vis Res. 2015; 114: 173–187.
    1. Liu XY, Zhang JY. Dichoptic training in adults with amblyopia: Additional stereoacuity gains over monocular training. Vis Res. 2018; 152: 84–90.
    1. Liu XY, Zhang JY. Dichoptic de-masking learning in adults with amblyopia and its mechanisms. Invest Ophthalmol Vis Sci 2019; 60: 2968–2977.
    1. Kelly KR, Jost RM, Dao L, Beauchamp CL, Leffler JN, Birch EE. Binocular iPad game vs patching for treatment of amblyopia in children: a randomized clinical trial. JAMA Ophthalmol. 2016; 134: 1402–1408.
    1. Li SL, Reynaud A, Hess RF, et al. .. Dichoptic movie viewing treats childhood amblyopia. J AAPOS. 2015; 19: 401–405.
    1. Li SL, Jost RM, Morale SE, et al. .. A binocular iPad treatment for amblyopic children. Eye (Lond). 2014; 28: 1246–1253.
    1. Birch EE, Li SL, Jost RM, et al. .. Binocular iPad treatment for amblyopia in preschool children. J AAPOS. 2015; 19: 6–11.
    1. Holmes JM, Manh VM,, Lazar EL, et al. .. Effect of a binocular iPad game vs part-time patching in children aged 5 to 12 years with amblyopia: a randomized clinical trial. JAMA Ophthalmol. 2016; 134: 1391–1400.
    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.
    1. Gambacorta C, Nahum M, Vedamurthy I, et al. .. An action video game for the treatment of amblyopia in children: a feasibility study. Vis Res. 2018; 148: 1–14.
    1. Gao TY, Guo CX, Babu RJ, et al. .. Effectiveness of a binocular video game vs placebo video game for improving visual functions in older children, teenagers, and adults with amblyopia: a randomized clinical trial. JAMA Ophthalmol. 2018; 136: 172–181.
    1. Manh VM, Holmes JM, Lazar EL, et al. .. A randomized trial of a binocular iPad game versus part-time patching in children aged 13 to 16 years with amblyopia. Am J Ophthalmol. 2018; 186: 104–115.
    1. Bossi M, Tailor VK, Anderson EJ, et al. .. Binocular therapy for childhood amblyopia improves vision without breaking interocular suppression. Invest Ophthalmol Vis Sci. 2017; 58: 3031–3043.
    1. Kelly KR, Jost RM, Wang YZ, et al. .. Improved binocular outcomes following binocular treatment for childhood amblyopia. Invest Ophthalmol Vis Sci 2018; 59: 1221–1228.
    1. Knox PJ, Simmers AJ, Gray LS, Cleary M. An exploratory study: prolonged periods of binocular stimulation can provide an effective treatment for childhood amblyopia. Invest Ophthalmol Vis Sci 2012; 53: 817–824.
    1. Pelli DG. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis. 1997; 10: 437–442.
    1. Levi DM. Crowding—an essential bottleneck for object recognition: a mini-review. Vis Res 2008; 48: 635–654.
    1. Sjöstrand J. Contrast sensitivity in children with strabismic and anisometropic amblyopia. A study of the effect of treatment. Acta Ophthalmol (Copenh). 1981; 59: 25–34.
    1. Fahle M, Henke-Fahle S. Interobserver variance in perceptual performance and learning. Invest Ophthalmol Vis Sci. 1996; 37: 869–877.
    1. Astle AT, Li RW, Webb BS, Levi DM, McGraw PV. A Weber-like law for perceptual learning. Sci Rep. 2013; 3: 1158.
    1. Levi DM, Li RW, Silver MA, Chung ST. Sequential perceptual learning of letter identification and “uncrowding” in normal peripheral vision: Effects of task, training order, and cholinergic enhancement. J Vis. 2020; 4: 1–13.
    1. Li RW, Ngo C, Nguyen J, Levi DM. Video-game play induces plasticity in the visual system of adults with amblyopia. PLoS Biol. 2011, 9, e1001135.
    1. Adams WE, Leske DA, Hatt SR, Holmes JM. Defining real change in measures of stereoacuity. Ophthalmology. 2009; 116: 281–285.
    1. Fawcett SL, Birch EE. Validity of the Titmus and Randot circles tasks in children with known binocular vision disorders. J AAPOS. 2003; 7: 333–338.
    1. Li J, Thompson B, Lam CS, et al. .. The role of suppression in amblyopia. Invest Ophthalmol Vis Sci. 2011; 52: 4169–4176.
    1. Stewart CE, Moseley MJ, Stephens DA, Fielder AR. Treatment dose-response in amblyopia therapy: the Monitored Occlusion Treatment of Amblyopia Study (MOTAS). Invest Ophthalmol Vis Sci. 2004; 45: 3048–3054.
    1. Fronius M, Cirina L, Ackermann H, Kohnen T, Diehl CM. Efficiency of electronically monitored amblyopia treatment between 5 and 16 years of age: new insight into declining susceptibility of the visual system. Vision Res. 2014; 103: 11–19.
    1. Stewart CE, Stephens DA, Fielder AR, Moseley MJ, Cooperative R. Objectively monitored patching regimens for treatment of amblyopia: randomised trial. BMJ 2007; 335: 707.
    1. Cotter SA, Pediatric Eye Disease Investigator Group, Edwards AR, et al. .. Treatment of anisometropic amblyopia in children with refractive correction. Ophthalmology. 2006; 113: 895–903.
    1. Stewart CE, Moseley MJ, Fielder AR, Stephens DA, Cooperative M. Refractive adaptation in amblyopia: quantification of effect and implications for practice. Br J Ophthalmol. 2004; 88: 1552–1556.
    1. Simmers AJ, Ledgeway T, Hess RF, McGraw PV. Deficits to global motion processing in human amblyopia. Vis Res. 2003; 43;729–738.
    1. Knox PJ, Ledgeway T, Simmers AJ. The effects of spatial offset, temporal offset and image speed on sensitivity to global motion in human amblyopia. Vis Res. 2013; 86: 59–65.
    1. Stifter E, Burggasser G, Hirmann E, Thaler A, Radner W. Monocular and binocular reading performance in children with microstrabismic amblyopia. Br J Ophthalmol. 2005; 89: 1324–1329.
    1. Birch EE, Kelly KR, Giaschi DE. Fellow eye deficits in amblyopia. J Binocul Vis Ocul Motil. 2019; 69: 116–125.
    1. Stewart CE, Wallace MP, Stephens DA, Fielder AR, Moseley MJ, Cooperative M. The effect of amblyopia treatment on stereoacuity. J AAPOS. 2013; 17: 166–173.
    1. Saxena R, Puranik S, Singh D, Menon V, Sharma P, Phuljhele S. Factors predicting recurrence in successfully treated cases of anisometropic amblyopia. Ind J Ophthalmol. 2013; 61: 630–633.
    1. Tsirlin I; Colpa L; Goltz HC; Wong AM. Behavioral training as new treatment for adult amblyopia: a meta-analysis and systematic review. Invest Ophthalmol Vis Sci. 2015; 56: 4061–4075.
    1. Xiao LQ, Zhang JY, Wang R, Klein SA, Levi DM, Yu C. Complete transfer of perceptual learning across retinal locations enabled by double training. Curr Biol. 2008; 18;1922–1926.
    1. Zhang JY, Zhang GL, Xiao LQ, Klein SA, Levi DM, Yu C. Rule-based learning explains visual perceptual learning and its specificity and transfer. J Neurosci. 2010; 30: 12323–12328.
    1. Hess RF, Pointer JS. Differences in the neural basis of human amblyopia: the distribution of the anomaly across the visual field. Vis Res. 1985; 25: 1577–1594.
    1. Levi DM, Klein S. Differences in Vernier discrimination for grating between strabismic and anisometropic amblyopes. Invest Ophthalmol Vis Sci. 1982; 23: 398–407.
    1. Moseley MJ, Fielder AR, Stewart CE. The optical treatment of amblyopia. Optom Vis Sci. 2009; 86: 629–633.

Source: PubMed

3
購読する