Monocular and Binocular Temporal Visual Perception of Infantile Nystagmus.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
18 03 2020
Historique:
received: 12 07 2019
accepted: 26 02 2020
entrez: 20 3 2020
pubmed: 20 3 2020
medline: 24 11 2020
Statut: epublish

Résumé

Contrast sensitivity is mostly used as a tool for testing aspects of visual functions. Infantile nystagmus is a pathological phenomenon that affects the spatial-temporal visual functions due to spontaneous oscillating movements of the eyes. We examined the spatial-temporal aspects of nystagmus perception, aiming to investigate the mechanisms underlying the deterioration of their visual performance. We tested the monocular and binocular contrast sensitivity of nystagmus and normally sighted subjects by measuring contrast detection of a Gabor target with spatial frequencies slightly above the cutoff threshold of each subject (nystagmus ~3; controls = 9cpd; presentation times 60-480 ms). The dominant eye of nystagmus revealed large differences over the non-dominant eye, highlighting the superiority of the dominant over the non-dominant eye in nystagmus. In addition, binocular summation mechanism was impaired in majority of the nystagmus subjects. Furthermore, these differences are not attributed to differences in visual acuity. Moreover, the visual performance in nystagmus continue to improve for longer presentation time compared with controls and was longer in the poor eye. Since the results are not due to differences in eye movements and strabismus, we suggest that the differences are due to developmental impairment in the visual system during the critical period.

Identifiants

pubmed: 32188906
doi: 10.1038/s41598-020-61914-2
pii: 10.1038/s41598-020-61914-2
pmc: PMC7080729
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4946

Références

Leat, S. J., Yadav, N. K. & Irving, E. L. Development of Visual Acuity and Contrast Sensitivity in Children. J. Optom. 2, 19–26 (2009).
doi: 10.3921/joptom.2009.19
Neri, P. & Levi, D. M. Spatial Resolution for Feature Binding Is Impaired in Peripheral and Amblyopic Vision. J Neuro-physiol 96, 142–153 (2006).
Owsley, C., Sekuler, R. & Siemsen, D. Contrast Sensitivity Throughout Adulthood. Vision Res. 23, 689–699 (1983).
doi: 10.1016/0042-6989(83)90210-9
Birren, J. E. & Fisher, L. M. Aging and Slowing of Behavior: Consequences for Cognition and Survival. Nebr. Symp. Motiv. 39, 1–37 (1991).
Birren, J. E. & Fisher, L. M. Aging and Speed of Behavior: Possible Consequences for Psychological Functioning. Annu. Rev. Psychol. 46, 329–353 (1995).
doi: 10.1146/annurev.ps.46.020195.001553
Legge, G. E. Sustained and transient mechanisms in human vision: Temporal and spatial properties. Vision Res. 18, 69–81 (1978).
doi: 10.1016/0042-6989(78)90079-2
Mullen, K. T. The Contrast Sensitivity of Human Colour Vision to Red-Green and Blue-Yellow Chromatic Gratings. J. Physiol. 359, 381–400 (1985).
doi: 10.1113/jphysiol.1985.sp015591 pubmed: 1193381 pmcid: 1193381
Campbell, F. W. & Kulikowski, J. J. Orientational Selectivity of The Human Visual System. J. Physiol. 187, 437–45 (1966).
doi: 10.1113/jphysiol.1966.sp008101 pubmed: 1395934 pmcid: 1395934
Movshon, J. A. & Blakemore, C. Orientation Specificity and Spatial Selectivity in Human Vision. Perception 2, 53–60 (1973).
doi: 10.1068/p020053 pubmed: 4777570 pmcid: 4777570
Umino, Y., Solessio, E. & Barlow, R. B. Speed, Spatial, and Temporal Tuning of Rod and Cone Vision in Mouse. J. Neurosci. 28, 189–98 (2008).
doi: 10.1523/JNEUROSCI.3551-07.2008 pubmed: 18171936 pmcid: 18171936
Kelly, D. H. Visual Contrast Sensitivity. Opt. Acta Int. J. Opt. 24, 107–129 (1977).
doi: 10.1080/713819495
Nachmias, J. Effect of Exposure Duration on Visual Contrast Sensitivity with Square-Wave Gratings. J. Opt. Soc. Am. 57, 421 (1967).
doi: 10.1364/JOSA.57.000421
Kulikowski, J. J. Effect of Eye Movements on the Contrast Sensitivity of Spatio-Temporal Patterns. Vision Res. 11, 261–273 (1971).
doi: 10.1016/0042-6989(71)90190-8 pubmed: 5579841 pmcid: 5579841
Milling, A. F., Hons, M., Connor, A. R. O. & Hons, B. The Importance of Contrast Sensitivity Testing in Children. Br. Ir. Orthopt. J. 9–14 (2014).
Katz, G. et al. Mesopic Foveal Contrast Sensitivity is Impaired in Diabetic Patients Without Retinopathy. Graefe’s Arch. Clin. Exp. Ophthalmol. 248, 1699–1703 (2010).
doi: 10.1007/s00417-010-1413-y
Baker, D. H., Lygo, F. A., Meese, T. S. & Georgeson, M. A. Binocular Summation Revisited: Beyond √2. Psychol. Bull. 144, 1186–1199 (2018).
doi: 10.1037/bul0000163 pubmed: 30102058 pmcid: 30102058
Meese, T. S., Georgeson, M. A. & Baker, D. H. Binocular Contrast Vision at and Above Threshold. J. Vis. 6, 7–7 (2006).
doi: 10.1167/6.11.7
Pardhan, S. & Gilchrist, J. Binocular contrast summation and inhibition in amblyopia. Doc. Ophthalmol. 82, 239–248 (1992).
doi: 10.1007/BF00160771 pubmed: 1303860 pmcid: 1303860
Loshin, D. S. & Jones, R. Contrast Sensitivity as a Function of Exposure Duration in The Amblyopic Visual System. Am. J. Optom. Physiol. Opt. 59, 561–7 (1982).
doi: 10.1097/00006324-198207000-00003 pubmed: 7124895 pmcid: 7124895
Lema, S. A. & Blake, R. Binocular Summation in Normal and stereoblind humans. Vision Res. 17, 691–695 (1977).
doi: 10.1016/S0042-6989(77)80004-7
Levi, D. M., Harwerth, R. S. & Smith, E. L. Binocular interactions in normal and anomalous binocular vision. Doc. Ophthalmol. 49, 303–324 (1980).
doi: 10.1007/BF01886623
Levi, D. M., Harwerth, R. S. & Smith, E. L. Humans deprived of normal binocular vision have binocular interactions tuned to size and orientation. Science 206, 852–4 (1979).
doi: 10.1126/science.493988
Baker, D. H., Meese, T. S., Mansouri, B. & Hess, R. F. Binocular Summation of Contrast Remains Intact in Strabismic Amblyopia. Investig. Opthalmology Vis. Sci. 48, 5332 (2007).
doi: 10.1167/iovs.07-0194
Li, R., Polat, U., Makous, W. & Bavelier, D. Enhancing the contrast sensitivity function through action video game training. Nat. Neurosci. 12, 549–551 (2009).
doi: 10.1038/nn.2296 pubmed: 2921999 pmcid: 2921999
Fiser, J., Bex, P. J. & Makous, W. Contrast conservation in human vision. Vision Res. 43, 2637–2648 (2003).
doi: 10.1016/S0042-6989(03)00441-3
Polat, U., Sterkin, A. & Yehezkel, O. Spatio-temporal low-level neural networks account for visual masking. 3, 153–165 (2007).
Mansouri, B., Allen, H. A., Hess, R. F., Dakin, S. C. & Ehrt, O. Integration of orientation information in amblyopia. Vision Res. 44, 2955–2969 (2004).
doi: 10.1016/j.visres.2004.06.017
Levi, D. M. & Harwerth, R. S. Contrast sensitivity in amblyopia due to stimulus deprivation. Br. J. Ophthalmol. 64, 15–20 (1980).
doi: 10.1136/bjo.64.1.15 pubmed: 1039340 pmcid: 1039340
Kayazawa, F., Yamamoto, T. & Itoi, M. Temporal contrast sensitivity in optic neuritis and amblyopia. Ann. Ophthalmol. 15, 331–4 (1983).
Demanins, R. & Hess, R. F. Effect of Exposure Duration on Spatial Uncertainty in Normal and Amblyopic Eyes. Vision Res 36, (1996).
Spang, K. & Fahle, M. Impaired Temporal, Not Just Spatial, Resolution in Amblyopia. Investig. Opthalmology Vis. Sci. 50, 5207 (2009).
doi: 10.1167/iovs.07-1604
Straube, A., Bronstein, A. & Straumann, D., European Federation of Neurologic Societies. Nystagmus and oscillopsia. Eur. J. Neurol. 19, 6–14 (2012).
doi: 10.1111/j.1468-1331.2011.03503.x
Leigh, R. J., Dell’Osso, L. F., Yaniglos, S. S. & Thurston, S. E. Oscillopsia, retinal image stabilization and congenital nystagmus. Invest. Ophthalmol. Vis. Sci. 29, 279–282 (1988).
Harcourt, B. Hereditary nystagmus in early childhood. J. Med. Genet. 7, 253–256 (1970).
doi: 10.1136/jmg.7.3.253 pubmed: 1468883 pmcid: 1468883
Abadi, R. V. Motor and sensory characteristics of infantile nystagmus. Br. J. Ophthalmol. 86, 1152–1160 (2002).
doi: 10.1136/bjo.86.10.1152 pubmed: 1771304 pmcid: 1771304
Kalloniatis, M. & Luu, C. Temporal Resolution. Webvision: The Organization of the Retina and Visual System (University of Utah Health Sciences Center, 1995).
Maurer, D., Mondloch, C. J. & Lewis, T. L. Effects of early visual deprivation on perceptual and cognitive development. Progress in brain research 164, 87–104 (2007).
doi: 10.1016/S0079-6123(07)64005-9 pubmed: 17920427 pmcid: 17920427
Bedell, H. E. & Loshin, D. S. Interrelations Between Measures of Visual-Acuity and Parameters of Eye-Movement in Congenital Nystagmus. Invest. Ophthalmol. Vis. Sci. 32, 416–421 (1991).
Kelly, J. P., Phillips, J. O. & Weiss, A. H. Does eye velocity due to infantile nystagmus deprive visual acuity development? J. Am. Assoc. Pediatr. Ophthalmol. Strabismus 22, 50–55.e1 (2018).
doi: 10.1016/j.jaapos.2017.10.008
Abadi, R. V. & Dickinson, C. M. Waveform characteristics in congenital nystagmus. Doc. Ophthalmol. 64, 153–167 (1987).
doi: 10.1007/BF00159990
Summers, C. G. Vision in albinism. Trans. Am. Ophthalmol. Soc. 94, 1095–155 (1996).
pubmed: 8981720 pmcid: 8981720
Huurneman, B., Boonstra, F. N. & Goossens, J. Predictors of sensitivity to perceptual learning in children with infantile nystagmus. Investig. Ophthalmol. Vis. Sci. 58, 4162–4172 (2017).
doi: 10.1167/iovs.17-21913
Huurneman, B., Boonstra, F. N., Cox, R. F., Cillessen, A. H. & van Rens, G. A systematic review on ‘Foveal Crowding’ in visually impaired children and perceptual learning as a method to reduce Crowding. BMC Ophthalmol. 12, 27 (2012).
doi: 10.1186/1471-2415-12-27 pubmed: 22824242 pmcid: 22824242
Pascal, E. & Abadi, R. V. Contour interaction in the presence of congenital nystagmus. Vision Res. 35, 1785–9 (1995).
doi: 10.1016/0042-6989(94)00277-S pubmed: 7660585 pmcid: 7660585
Papageorgiou, E., McLean, R. J. & Gottlob, I. Nystagmus in Childhood. Pediatr. Neonatol. 55, 341–351 (2014).
doi: 10.1016/j.pedneo.2014.02.007 pubmed: 25086850 pmcid: 25086850
Katie Flickinger and Jeremiah P. Tao, MDEdited Ingrid U. Scott, MD, MPH, and Sharon Fekrat, M. How to Assess and Treat Infantile Nystagmus - American Academy of Ophthalmology. EyeNet Mag./November/December 2005 (2005).
Hertle, R. W. & Reese, M. Clinical Contrast Sensitivity Testing in Patients With Infantile Nystagmus Syndrome Compared With Age-Matched Controls. Am. J. Ophthalmol. 143, 1063–1065 (2007).
doi: 10.1016/j.ajo.2007.02.028 pubmed: 17524784 pmcid: 17524784
Dickinson, C. M. The elucidation and use of the effect of near fixation in congenital nystagmus. Ophthalmic Physiol. Opt. 6, 303–311 (1986).
doi: 10.1111/j.1475-1313.1986.tb00720.x pubmed: 3822471 pmcid: 3822471
Dell’Osso, L. F. & Jacobs, J. B. An expanded nystagmus acuity function: intra- and intersubject prediction of best-corrected visual acuity. Doc. Ophthalmol. 104, 249–76 (2002).
doi: 10.1023/A:1015299930849 pubmed: 12076015 pmcid: 12076015
Huurneman, B. & Boonstra, F. N. Monocular and Binocular Development in Children with Albinism, Infantile Nystagmus Syndrome, and Normal Vision. Strabismus 21, 216–224 (2013).
doi: 10.3109/09273972.2013.833954 pubmed: 24195763 pmcid: 24195763
McLean, R., Proudlock, F., Thomas, S., Degg, C. & Gottlob, I. Congenital nystagmus: Randomized, controlled, double-masked trial of memantine/gabapentin. Ann. Neurol. 61, 130–138 (2007).
doi: 10.1002/ana.21065
Kanski, B. B. Kanski’s Clinical Ophthalmology - Eighth Edition [2016][UnitedVRG].
Abadi, R. V., Carden, D. & Simpson, J. A new treatment for congenital nystagmus. Br. J. Ophthalmol. 64, 2–6 (1980).
doi: 10.1136/bjo.64.1.2 pubmed: 7356927 pmcid: 7356927
Loshin, D. S. & Browning, R. A. Contrast sensitivity in albinotic patients. Am. J. Optom. Physiol. Opt. 60, 158–66 (1983).
doi: 10.1097/00006324-198303000-00003 pubmed: 6846493 pmcid: 6846493
Porac, C. & Coren, S. Suppressive processes in binocular vision: ocular dominance and amblyopia. Am. J. Optom. Physiol. Opt. 52, 651–7 (1975).
doi: 10.1097/00006324-197510000-00001 pubmed: 1200108 pmcid: 1200108
Vedamurthy, I., Suttle, C. M., Alexander, J. & Asper, L. J. Interocular interactions during acuity measurement in children and adults, and in adults with amblyopia. Vision Res. 47, 179–188 (2007).
doi: 10.1016/j.visres.2006.08.017 pubmed: 17126872 pmcid: 17126872
Matsumoto, C. S. et al. Binocular interaction of visually evoked cortical potentials elicited by dichoptic binocular stimulation. J. Vis. 14, 4–4 (2014).
doi: 10.1167/14.11.4 pubmed: 25194016 pmcid: 25194016
Handa, T., Mukuno, K., Uozato, H. & Niida, T. Effects of Dominant and Nondominant Eyes in Binocular Rivalry. Optom. Vis. Sci. 81, 377–383 (2004).
doi: 10.1097/01.opx.0000135085.54136.65 pubmed: 15181364 pmcid: 15181364
Dell’Osso, L. F. Congenital, latent and manifest latent nystagmus–similarities, differences and relation to strabismus. Jpn. J. Ophthalmol. 29, 351–68 (1985).
pubmed: 3831487 pmcid: 3831487
Cho, K.-J., Kim, S.-Y. & Yang, S.-W. The Refractive Errors of Dominant and Non-dominant Eyes. J. Korean Ophthalmol. Soc. 50, 275 (2009).
doi: 10.3341/jkos.2009.50.2.275
Abadi, R. V. & Pascal, E. Visual resolution limits in human albinism. Vision Res. 31, 1445–1447 (1991).
doi: 10.1016/0042-6989(91)90063-B
Cesarelli, M., Bifulco, P., Loffredo, L. & Bracale, M. Relationship between visual acuity and eye position variability during foveations in congenital nystagmus. Doc. Ophthalmol. 101, 59–72 (2000).
doi: 10.1023/A:1002702609387
Blechschmidt, T., Krumsiek, M. & Todorova, M. G. The Effect of Acupuncture on Visual Function in Patients with Congenital and Acquired Nystagmus. Medicines 4, 33 (2017).
doi: 10.3390/medicines4020033 pubmed: 5590069 pmcid: 5590069
McLean, R. J., Windridge, K. C. & Gottlob, I. Living with nystagmus: a qualitative study. Br. J. Ophthalmol. 96, 981–6 (2012).
doi: 10.1136/bjophthalmol-2011-301183
Bedell, H. E. Visual and Perceptual Consequences of Congenital Nystagmus. Semin. Ophthalmol. 21, 91–95 (2006).
doi: 10.1080/08820530600614181
Harris, C., Berry, D. & Evora, L. V. A Developmental Model of Infantile Nystagmus. Semin. Ophthalmol. 21, 63–69 (2006).
doi: 10.1080/08820530600613746
Campbell, F. W. & Green, D. G. Monocular Versus Binocular Visual Acuity. Nature 208, 191–192 (1965).
doi: 10.1038/208191a0
Frisén, L. & Lindblom, B. Binocular Summation in Humans: Evidence for a Hierarchic Model. J. Physiol. 402, 773–82 (1988).
doi: 10.1113/jphysiol.1988.sp017233 pubmed: 1191920 pmcid: 1191920
Pardhan, S. A comparison of binocular summation in young and older patients. Curr. Eye Res. 15, 315–319 (1996).
doi: 10.3109/02713689609007626
Harwerth, R. S., Smith, E. L. & Levi, D. M. Suprathreshold Binocular Interactions for Grating Patterns. Percept. Psychophys. 27, 43–50 (1980).
doi: 10.3758/BF03199905
Ding, J. & Sperling, G. A Gain-Control Theory of Binocular Combination. (2005).
Cogan, A. I. Human Binocular Interaction: Towards a Neural Model. Vision Res. 27, 2125–2139 (1987).
doi: 10.1016/0042-6989(87)90127-1
Blake, R. & Wilson, H. Binocular vision. Vision Res. 51, 754–770 (2011).
doi: 10.1016/j.visres.2010.10.009
Wilson, H. R. Computational evidence for a rivalry hierarchy in vision. Proc. Natl. Acad. Sci. USA 100, 14499–503 (2003).
doi: 10.1073/pnas.2333622100
Levi, D. M., Harwerth, R. S. & Manny, R. E. Suprathreshold spatial frequency detection and binocular interaction in strabismic and anisometropic amblyopia. Investigative Ophthalmology & Visual Science 18, ([Association for Research in Vision and Ophthalmology, etc.], 1979).
Hood, A. S. & Morrison, J. D. The dependence of binocular contrast sensitivities on binocular single vision in normal and amblyopic human subjects. J. Physiol. 540, 607–622 (2002).
doi: 10.1113/jphysiol.2001.013420 pubmed: 2290246 pmcid: 2290246
Legge, G. E. Binocular contrast summation II. Quadratic summation. Vision Res. 24, 385–394 (1984).
doi: 10.1016/0042-6989(84)90064-6
Gorea, A. & Tyler, C. W. New Look at Bloch’s Law For Contrast. J. Opt. Soc. Am. A 3, 52 (2008).
doi: 10.1364/JOSAA.3.000052
Gorea, A. A Refresher of the Original Bloch’s Law Paper (Bloch, July 1885). Iperception. 6, (2015).
Scharnowski, F., Hermens, F. & Herzog, M. H. Bloch’s Law and The Dynamics of Feature Fusion. Vision Res. 47, 2444–2452 (2007).
doi: 10.1016/j.visres.2007.05.004 pubmed: 17675130 pmcid: 17675130
Abadi, R. V., Dickinson, C. M., Pascal, E. & Papas, E. Retinal image quality in albinos: A review. Ophthalmic Paediatr. Genet. 11, 171–176 (1990).
doi: 10.3109/13816819009020976 pubmed: 2280974 pmcid: 2280974
Polat, U. Effect of spatial frequency on collinear facilitation. Spat. Vis. 22, 179–193 (2009).
doi: 10.1163/156856809787465609 pubmed: 19228457 pmcid: 19228457
Watson, A. B., Barlow, H. B. & Robson, J. G. What does the eye see best? Nature 302, 419–22.
Lev, M. & Polat, U. Space and time in masking and crowding. J. Vis. 15, 10 (2015).
doi: 10.1167/15.13.10 pubmed: 26381841 pmcid: 26381841
Peli, E., Arend, L. E., Goldstein, R. B. & Young, G. M. Contrast sensitivity to patch stimuli: Effects of spatial bandwidth and temporal presentation. Spat. Vis. 7, 1–14 (1993).
doi: 10.1163/156856893X00018 pubmed: 8494806 pmcid: 8494806
Levi, D. M. & Harwerth, R. S. Spatio-temporal interactions in anisometropic and strabismic amblyopia. Investigative Ophthalmology & Visual Science 16, (C.V. Mosby Co, 1977).
Polat, U., Bonneh, Y., Ma-Naim, T., Belkin, M. & Sagi, D. Spatial interactions in amblyopia: Effects of stimulus parameters and amblyopia type. https://doi.org/10.1016/j.visres.2004.12.014 .
Bonneh, Y. S., Adini, Y. & Polat, U. Contrast sensitivity revealed by microsaccades. J. Vis. 15, 11 (2015).
doi: 10.1167/15.9.11 pubmed: 26223023 pmcid: 26223023
Ghodrati, M., Morris, A. P. & Price, N. S. C. The (un)suitability of modern liquid crystal displays (LCDs) for vision research. Front. Psychol. 6, 303 (2015).
doi: 10.3389/fpsyg.2015.00303 pubmed: 25852617 pmcid: 25852617
Scheiman, M. & Wick, B. Clinical management of binocular vision. (Wolters Kluwer, 2014).
Carlson, N. B. & Kurtz, D. Clinical procedures for ocular examination. (McGraw-Hill, Medical Pub. Div, 2004).
Valle-Inclán, F., Blanco, M. J., Soto, D. & Leirós, L. A new method to assess eye dominance. 29, (2008).
Noushad, B., Thomas, J. & Amin, S. Reliability of a modified logMAR distant visual acuity chart for routine clinical use. Oman J. Ophthalmol. 5, 87 (2012).
doi: 10.4103/0974-620X.99370 pubmed: 3441035 pmcid: 3441035
Pelli, D. G. & Bex, P. Measuring contrast sensitivity. Vision Res. 90, 10–4 (2013).
doi: 10.1016/j.visres.2013.04.015 pubmed: 3744596 pmcid: 3744596
Abadi, R. & Sandikcioglu, M. Visual resolution in congenital pendular nystagmus. Am. J. Optom. Physiol. Opt. 52, 573–581 (1975).
doi: 10.1097/00006324-197509000-00001
Levitt, H. Transformed Up-Down Methods in Psychoacoustics. J. Acoust. Soc. Am. 49, 467–477 (1971).
doi: 10.1121/1.1912375

Auteurs

Avital Moshkovitz (A)

School of Optometry and Vision Sciences, Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel.

Maria Lev (M)

School of Optometry and Vision Sciences, Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel.

Uri Polat (U)

School of Optometry and Vision Sciences, Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel. uri.polat@biu.ac.il.

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