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Reading difficulties in amblyopia: Consequence of visual sensory and oculomotor dysfunction

Published:September 27, 2022DOI:https://doi.org/10.1016/j.jns.2022.120438

      Highlights

      • Reading performance was altered in subjects with amblyopia.
      • Subjects with amblyopia showed increased vergence and fixation instability.
      • The instability was seen in amblyopic subjects with and without nystagmus.
      • Ocular motor dysfunction and severity of visual and stereoacuity deficits contribute to reading difficulties in amblyopia.

      Abstract

      Introduction

      Reading is a vision-reliant task, requiring sequential eye movements. Binocularly discordant input results in visual sensory and oculomotor dysfunction in amblyopia, which may contribute to reading difficulties. This study aims to determine the contributions of fixation eye movement (FEM) abnormalities, clinical type and severity of amblyopia to reading performance under binocular and monocular viewing conditions.

      Methods

      Twenty-three amblyopic patients and nine healthy controls were recruited. Eye movements elicited during fixation and reading of preselected passages were collected for each subject using infrared video-oculography. Subjects were classified as having no nystagmus (n = 9), fusion maldevelopment nystagmus (FMN, n = 5), or nystagmus without structural anomalies that does not meet criteria for FMN or infantile nystagmus (n = 9). Reading rate (words/min), the number of forward and regressive saccades (per 100 words) and fixation duration (s) were computed.

      Results

      Amblyopic patients with and without nystagmus exhibited greater vergence and fixation instability. In patients without nystagmus, the instability arises from increased amplitude and velocity of fast and slow FEMs respectively. Amblyopic patients with and without nystagmus exhibited lower reading speeds with increased fixation duration, regressive and progressive saccades than controls in all viewing conditions. Mixed etiology, greater amblyopic eye visual acuity and stereopsis deficits were associated with greater reading difficulties under binocular viewing.

      Conclusions

      The presence of oculomotor dysfunction and the extent of visual acuity and stereoacuity deficits contribute to reading difficulties in patients with amblyopia, with and without nystagmus. The understanding of reading difficulties is essential to devise accommodations to limit long-term academic and vocational consequences of amblyopia.

      Keywords

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      References

        • Attebo K.
        • Mitchell P.
        • Cumming R.
        • Smith W.
        • Jolly N.
        • Sparkes R.
        Prevalence and causes of amblyopia in an adult population.
        Ophthalmology. Jan 1998; 105: 154-159
        • Preslan M.W.
        • Novak A.
        Baltimore vision screening project.
        Ophthalmology. Jan 1996; 103: 105-109
        • American Academy of Pediatric Ophthalmology and Strabimsus Panel
        Preferred Practice Pattern Guidelines.
        Amblyopia, 2007 (Available online at wwwaaoorg/ppp)
        • Chatzistefanou K.I.
        • Theodossiadis G.P.
        • Damanakis A.G.
        • Ladas I.D.
        • Moschos M.N.
        • Chimonidou E.
        Contrast sensitivity in amblyopia: the fellow eye of untreated and successfully treated amblyopes.
        J AAPOS. Oct 2005; 9: 468-474https://doi.org/10.1016/j.jaapos.2005.05.002
        • Repka M.X.
        • Kraker R.T.
        • Beck R.W.
        • et al.
        Contrast sensitivity following amblyopia treatment in children.
        Arch. Ophthalmol. Sep 2009; 127: 1225-1227https://doi.org/10.1001/archophthalmol.2009.219
        • Abrahamsson M.
        • Sjostrand J.
        Contrast sensitivity and acuity relationship in strabismic and anisometropic amblyopia.
        Br. J. Ophthalmol. Jan 1988; 72: 44-49
        • Barnes G.R.
        • Hess R.F.
        • Dumoulin S.O.
        • Achtman R.L.
        • Pike G.B.
        The cortical deficit in humans with strabismic amblyopia.
        J Physiol. May 15 2001; 533: 281-297
        • Ciuffreda K.J.
        • Fisher S.K.
        Impairment of contrast discrimination in amblyopic eyes.
        Ophthalmic Physiol Opt. 1987; 7: 461-467
        • Hou C.
        • Pettet M.W.
        • Norcia A.M.
        Abnormalities of coherent motion processing in strabismic amblyopia: Visual-evoked potential measurements.
        J Vis. Apr 8 2008; 8 (2 1–12)https://doi.org/10.1167/8.4.2
        • McKee S.P.
        • Levi D.M.
        • Movshon J.A.
        The pattern of visual deficits in amblyopia.
        J. Vis. 2003; 3: 380-405https://doi.org/10.1167/3.5.5
        • Murray J.G.K.
        • Ghasia F.
        Monocular and binocular visual function deficits in amblyopic patients with and without fusion Maldevelopment nystagmus.
        Eye Brain. 2021 Apr; 28: 99-109
        • Hubel D.H.
        • Wiesel T.N.
        • LeVay S.
        Plasticity of ocular dominance columns in monkey striate cortex.
        Philos Trans R Soc Lond B Biol Sci. Apr 26 1977; 278: 377-409
        • Wiesel T.N.
        • Hubel D.H.
        Single-cell responses in striate cortex of kittens deprived of vision in one eye.
        J. Neurophysiol. Nov 1963; 26: 1003-1017
        • Wiesel T.N.
        Postnatal development of the visual cortex and the influence of environment.
        Nature. Oct 14 1982; 299: 583-591
        • Kiorpes L.
        • Kiper D.C.
        • O’Keefe L.P.
        • Cavanaugh J.R.
        • Movshon J.A.
        Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia.
        J Neurosci. Aug 15 1998; 18 (6411–24)
        • Hendrickson A.E.
        • Movshon J.A.
        • Eggers H.M.
        • Gizzi M.S.
        • Boothe R.G.
        • Kiorpes L.
        Effects of early unilateral blur on the macaque’s visual system. II. Anatomical observations.
        J Neurosci. May 1987; 7: 1327-1339
        • Kiorpes L.
        • Boothe R.G.
        Naturally occurring strabismus in monkeys (Macaca nemestrina).
        Invest. Ophthalmol. Vis. Sci. Feb 1981; 20: 257-263
        • Kiorpes L.
        • Boothe R.G.
        • Hendrickson A.E.
        • Movshon J.A.
        • Eggers H.M.
        • Gizzi M.S.
        Effects of early unilateral blur on the macaque’s visual system. I. Behavioral observations.
        J Neurosci. May 1987; 7: 1318-1326
        • Movshon J.A.
        • Eggers H.M.
        • Gizzi M.S.
        • Hendrickson A.E.
        • Kiorpes L.
        • Boothe R.G.
        Effects of early unilateral blur on the macaque’s visual system. III. Physiological observations.
        J Neurosci. May 1987; 7: 1340-1351
        • Bedell H.E.
        • Yap Y.L.
        • Flom M.C.
        Fixational drift and nasal-temporal pursuit asymmetries in strabismic amblyopes.
        Invest. Ophthalmol. Vis. Sci. May 1990; 31: 968-976
        • Martinez-Conde S.
        Fixational eye movements in normal and pathological vision.
        Prog. Brain Res. 2006; 154: 151-176https://doi.org/10.1016/S0079-6123(06)54008-7
        • Kommerell G.
        The relationship between infantile strabismus and latent nystagmus.
        Eye (Lond). 1996; 10: 274-281https://doi.org/10.1038/eye.1996.58
        • Tychsen L.
        • Leibole M.
        • Drake D.
        Comparison of latent nystagmus and nasotemporal asymmetries of optokinetic nystagmus in adult humans and macaque monkeys who have infantile strabismus.
        Strabismus. 1996; 4: 171-177https://doi.org/10.3109/09273979609057145
        • Lang J.
        The congenital strabismus syndrome.
        Strabismus. Sep 2000; 8: 195-199
        • Ciuffreda K.J.
        • Kenyon R.V.
        • Stark L.
        Fixational eye movements in amblyopia and strabismus.
        J. Am. Optom. Assoc. Nov 1979; 50: 1251-1258
        • Kang S.L.B.S.
        • Otero-Millan J.
        • Shaikh A.G.
        • Ghasia F.F.
        Fixational eye movement waveforms in amblyopia: characteristics of fast and slow eye movements.
        JEMR- in press. 2019; 12: 1-22
        • Bowers N.R.
        • Poletti M.
        Microsaccades during reading.
        PLoS One. 2017; 12e0185180https://doi.org/10.1371/journal.pone.0185180
        • Subramanian V.
        • Jost R.M.
        • Birch E.E.
        A quantitative study of fixation stability in amblyopia.
        Invest Ophthalmol Vis Sci. Mar 19 2013; 54: 1998-2003https://doi.org/10.1167/iovs.12-11054
        • Gonzalez E.G.
        • Wong A.M.
        • Niechwiej-Szwedo E.
        • Tarita-Nistor L.
        • Steinbach M.J.
        Eye position stability in amblyopia and in normal binocular vision.
        Invest Ophthalmol Vis Sci. Aug 9 2012; 53: 5386-5394https://doi.org/10.1167/iovs.12-9941
        • Shaikh A.G.
        • Otero-Millan J.
        • Kumar P.
        • Ghasia F.F.
        Abnormal Fixational eye movements in amblyopia.
        PLoS One. 2016; 11e0149953https://doi.org/10.1371/journal.pone.0149953
        • Niechwiej-Szwedo E.
        • Chandrakumar M.
        • Goltz H.C.
        • Wong A.M.
        Effects of strabismic amblyopia and strabismus without amblyopia on visuomotor behavior, I: saccadic eye movements.
        Invest Ophthalmol Vis Sci. Nov 1 2012; 53: 7458-7468https://doi.org/10.1167/iovs.12-10550
        • Hrisos S.
        • Clarke M.P.
        • Kelly T.
        • Henderson J.
        • Wright C.M.
        Unilateral visual impairment and neurodevelopmental performance in preschool children.
        Br. J. Ophthalmol. Jul 2006; 90: 836-838https://doi.org/10.1136/bjo.2006.090910
        • Webber A.L.
        • Wood J.M.
        • Gole G.A.
        • Brown B.
        The effect of amblyopia on fine motor skills in children.
        Invest. Ophthalmol. Vis. Sci. Feb 2008; 49: 594-603https://doi.org/10.1167/iovs.07-0869
        • O’Connor A.R.
        • Birch E.E.
        • Anderson S.
        • Draper H.
        Relationship between binocular vision, visual acuity, and fine motor skills.
        Optometry and Vision Science: Official Publication of the American Academy of Optometry. Dec 2010; 87: 942-947https://doi.org/10.1097/OPX.0b013e3181fd132e
        • Kanonidou E.
        • Gottlob I.
        • Proudlock F.A.
        The effect of font size on reading performance in strabismic amblyopia: an eye movement investigation.
        Invest Ophthalmol Vis Sci. Jan 23 2014; 55: 451-459https://doi.org/10.1167/iovs.13-13257
        • Kanonidou E.
        • Proudlock F.A.
        • Gottlob I.
        Reading strategies in mild to moderate strabismic amblyopia: an eye movement investigation.
        Invest. Ophthalmol. Vis. Sci. Jul 2010; 51: 3502-3508https://doi.org/10.1167/iovs.09-4236
        • Kelly K.R.
        • Jost R.M.
        • De La Cruz A.
        • et al.
        Slow reading in children with anisometropic amblyopia is associated with fixation instability and increased saccades.
        J Aapos. Dec 2017; 21 (e1): 447-451
        • Henderson J.M.H.A.
        High-level scene perception.
        Annu. Rev. Psychol. 1999; 50: 243-271
        • Falkenberg H.K.R.G.
        • Bex P.J.
        Acuity, crowding, reading and fixation stability.
        Vis. Res. 2007, Jan; 47: 126-135
        • Macedo A.F.C.M.
        • Rubin G.S.
        The effect of retinal image slip on peripheral visual acuity.
        J. Vis. 2008, Nov 12; 8 (16.1-11)
        • Manh V.M.
        • Holmes J.M.
        • Lazar E.L.
        • 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. Feb 2018; 186: 104-115https://doi.org/10.1016/j.ajo.2017.11.017
        • Engbert R.
        • Kliegl R.
        Microsaccades uncover the orientation of covert attention.
        Vis. Res. Apr 2003; 43: 1035-1045
        • Engbert R.
        • Kliegl R.
        Microsaccades keep the eyes’ balance during fixation.
        Psychol. Sci. Jun 2004; 15: 431-436https://doi.org/10.1111/j.0956-7976.2004.00697.x
        • Laubrock J.
        • Engbert R.
        • Kliegl R.
        Microsaccade dynamics during covert attention.
        Vis. Res. Mar 2005; 45: 721-730https://doi.org/10.1016/j.visres.2004.09.029
        • Dell’Osso L.F.S.D.
        • Daroff R.B.
        Latent, manifest latent, and congenital nystagmus.
        Arch Ophthalmology. 1979, Oct; 97 (1877–85)
        • Tychsen L.R.M.
        • Wong A.
        • Foeller P.
        • Bradley D.
        • Burkhalter A.
        The neural mechanism for Latent (fusion maldevelopment) nystagmus.
        J Neuroophthalmol. 2010 Sep; 30 (276–83)
        • Legge G.E.
        • Ross J.A.
        • LALJ.
        Psychophysics of reaing VIII. The Minnesota low-vision Reading test.
        Optom. Vis. Sci. 1989; 66: 843-853
        • Chen D.
        • Otero-Millan J.
        • Kumar P.
        • Shaikh A.G.
        • Ghasia F.F.
        Visual search in amblyopia: abnormal Fixational eye movements and suboptimal sampling strategies.
        Invest Ophthalmol Vis Sci. Sep 4 2018; 59: 4506-4517https://doi.org/10.1167/iovs.18-24794
        • Shi X.F.
        • Xu L.M.
        • Li Y.
        • Wang T.
        • Zhao K.X.
        • Sabel B.A.
        Fixational saccadic eye movements are altered in anisometropic amblyopia.
        Restor. Neurol. Neurosci. 2012; 30: 445-462https://doi.org/10.3233/RNN-2012-129000
        • Birch E.S.
        • Vidhya & Weakley, David.
        Fixation instability in anisometropic children with reduced stereopsis.
        Journal of AAPOS. 2013; 17: 287-290
        • Chung S.T.
        • Kumar G.
        • Li R.W.
        • Levi D.M.
        Characteristics of fixational eye movements in amblyopia: limitations on fixation stability and acuity?.
        Vis. Res. Sep 2015; 114: 87-99https://doi.org/10.1016/j.visres.2015.01.016
        • Scaramuzzi M.
        • Murray J.
        • Otero-Millan J.
        • Nucci P.
        • Shaikh A.G.
        • Ghasia F.F.
        Part time patching treatment outcomes in children with amblyopia with and without fusion maldevelopment nystagmus: an eye movement study.
        PLoS One. 2020; 15e0237346https://doi.org/10.1371/journal.pone.0237346
        • Ghasia F.F.
        • Otero-Millan J.
        • Shaikh A.G.
        Abnormal fixational eye movements in strabismus.
        Br. J. Ophthalmol. Feb 2018; 102: 253-259https://doi.org/10.1136/bjophthalmol-2017-310346
        • Kelly K.R.J.R.
        • Wang S.X.
        • Stager Jr., D.R.
        • Birch E.E.
        Binocular reading in children following extraction of a dense congenital or infantile unilateral cataract.
        J AAPOS. 2020 Aug; 24: 228e1-228e7
        • Kelly K.R.J.R.
        • De La Cruz A.
        • Birch E.E.
        Amblyopic children read more slowly than controls under natural, binocular reading conditions.
        J AAPOS. 2015 Dec; 19: 515-520
        • Kelly K.R.J.R.
        • De La Cruz A.
        • Dao L.
        • Beauchamp C.L.
        • Stager Jr., D.
        • Birch E.E.
        Slow reading in children with anisometropic amblyopia is associated with fixation instability and increased saccades.
        J AAPOS. 2017 Dec; 21: 447-451
        • Buczkowska H.
        • Miśkowiak B.
        Comparison of reading speed, phonological decoding, and comprehension in the group of children with anisometropic amblyopia and control group.
        Opt. Appl. 2017; 47: 351-362
        • Repka M.X.
        • Kraker R.T.
        • Beck R.W.
        • Cotter S.A.
        • Holmes J.M.
        • Arnold R.W.
        • Astle W.F.
        • Sala N.A.
        • Tien D.R.
        Pediatric eye disease Investigator Group. Monocular oral reading performance after amblyopia treatment in children.
        Am J. Ophthalmol. 2008; 146: 942-947
        • Kugathasan L.P.M.
        • Chu V.
        • Lyons C.
        • Giaschi D.
        Reading ability of children treated for amblyopia.
        Vis. Res. 2019 Mar; 156: 28-38
        • Rayner K.I.A.
        • Morrison R.E.
        • Slowiaczek M.L.
        • Bertera J.H.
        Masking of foveal and parafoveal vision during eye fixations in reading.
        J Exp Psychol Hum Percept Perform. 1981; 7: 167-179
        • K. R.
        Eye movements in reading and information processing: 20 years of research.
        Psychol. Bull. 1998; 124: 372-422
        • Fine E.M.R.G.
        The effects of simulated cataract on reading with normal vision and simulated central scotoma.
        Vis. Res. 1999; 39: 4274-4285
        • McMahon T.T.H.M.
        • Viana M.
        Fixation characteristics in macular disease: relationship between saccadic frequency, sequencing, and reading rate.
        Invest Ophthalmol Vis Sci. 1991; 32: 567-574
        • Cheong A.M.
        • Legge E.G.
        • Lawrence M.G.
        • Cheung S.H.
        • Ruff M.A.
        Relationship between visual span and reading performance in age-related macular degeneration.
        Vis. Res. 2008; 48: 577-588
        • Upadhyaya S.D.V.
        Response properties of cells within the rostral superior colliculus of Strabismic monkeys.
        Invest. Ophthalmol. Vis. Sci. 2019 Oct 1; 60: 4292-4302
        • Kapoula Z.L.B.H.
        • Yang Q.
        • Bucci M.P.
        Latency of saccades, vergence and combined saccade vergence movements in a subject with manifest latent nystagmus.
        Strabismus. 2004 Sep; 12: 157-167
        • Niechwiej-Szwedo E.
        • Goltz H.C.
        • Chandrakumar M.
        • Hirji Z.A.
        • Wong A.M.
        Effects of anisometropic amblyopia on visuomotor behavior, I: saccadic eye movements.
        Invest. Ophthalmol. Vis. Sci. Dec 2010; 51: 6348-6354https://doi.org/10.1167/iovs.10-5882
        • Holmes J.M.
        • Beck R.W.
        • Kraker R.T.
        • et al.
        Impact of patching and atropine treatment on the child and family in the amblyopia treatment study.
        Arch. Ophthalmol. Nov 2003; 121: 1625-1632https://doi.org/10.1001/archopht.121.11.1625
        • van de Graaf E.S.
        • van der Sterre G.W.
        • Polling J.R.
        • van Kempen H.
        • Simonsz B.
        • Simonsz H.J.
        Amblyopia & Strabismus Questionnaire: design and initial validation.
        Strabismus. Sep 2004; 12: 181-193https://doi.org/10.1080/09273970490491196