Normal saccades but decreased fixation stability in a population of children with dyslexia
Keywords:eye movements, dyslexia, saccades, fixations
Developmental dyslexia affects around 5-15% of the population and has a heterogeneous aetiology. Optometric disorders are more prevalent in dyslexic populations but the relationship be- tween eye movement control and dyslexia is not well established. In this study, we investigated whether children with dyslexia show saccadic or fixation deficits and whether these deficits are related to deficits in visual acuity and/or accommodation. Thirty-four children with and without dyslexia were recruited for the project. All participants had an optometric examination and performed a saccade and fixation experiment. We used two eye movement paradigms: the step and the gap task. Eye movements were recorded by an infrared eye-tracker and saccade and fixation parameters were analysed separately. Saccadic latencies, premature saccades, and directional errors were similar between children with dyslexia and typically developing children. In contrast, fixations were significantly less stable in the dyslexic group. Neither saccades nor fixations were associated with deficits in accommodation or visual acuity. Children with dyslexia showed no difficulties in saccadic performance, but their fixation stability was reduced compared to the control group. The reduced fixation stability can be explained by general deficits in the cognitive processes that underpin eye movement control, that have also been found in other neuro-developmental disorders.
Amore, F. M., Fasciani, R., Silvestri, V., Crossland, M. D., de Waure, C., Cruciani, F., & Reibaldi, A. (2013). Relationship between fixation stability measured with MP-1 and reading performance. Ophthalmic and Physiological Optics, 33(5), 611–7. https://doi.org/10.1111/opo.12048
Bednarek, D. B., Tarnowski, A., & Grabowska, A. (2006). Latencies of stimulus-driven eye movements are shorter in dyslexic subjects. Brain and Cognition, 60 (1), 64–9. https://doi.org/10.1016/j.bandc.2005.09.007
Bellocchi, S., Muneaux, M., Bastien-Toniazzo, M., & Ducrot, S. (2013). I can read it in your eyes: What eye movements tell us about visuo-attentional processes in developmental dyslexia. Research in Developmental Disabilities, 34(1), 452–60. https://doi.org/10.1016/j.ridd.2012.09.002
Biscaldi, M., Fischer, B., & Aiple, F. (1994). Saccadic eye movements of dyslexic and normal reading children. Perception, 23(1), 45–64.
Biscaldi, M., Gezeck, S., & Stuhr, V. (1998). Poor saccadic control correlates with dyslexia. Neuropsychologia, 36 (11), 1189–202.
Bishop, D. V., & Snowling, M. J. (2004). Developmental dyslexia and specific language impairment: Same or different? Psychological Bulletin, 130(6), 858–86. https://doi.org/10.1037/0033-2909.130.6.858
Bucci, M. P., Bremond-Gignac, D., & Kapoula, Z. (2008a). Latency of saccades and vergence eye movements in dyslexic children. Experimental Brain Research, 188 (1), 1–12. https://doi.org/10.1007/s00221-008-1345-5
Bucci, M. P., Bremond-Gignac, D., & Kapoula, Z. (2008b). Poor binocular coordination of saccades in dyslexic children. Graefe’s Archive for Clinical and Experimental Ophthalmology, 246(3), 417–28. https://doi.org/10.1007/s00417-007-0723-1
Bucci, M. P., Melithe, D., Ajrezo, L., Bui-Quoc, E., & Gerard, C. L. (2014). The influence of oculomotor tasks on postural control in dyslexic children. Frontiers in Human Neuroscience, 8:981.(doi). https://doi.org/10.3389/fnhum.2014.00981
Bucci, M. P., Nassibi, N., Gerard, C.-L., Bui-Quoc, E., & Seassau, M. (2012). Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: Evidence from a reading and visual search study. PLoS ONE, 7(3), 33458.
Castro, S. M., Salgado, C. A., Andrade, F. P., Ciasca, S. M., & Carvalho, K. M. (2008). Visual control in children with developmental dyslexia. Arquivos Brasileiros de Oftalmologia, 71(6), 837–40.
Cesareo, M., Manca, D., Ciuffoletti, E., De Giovanni, V., Ricci, F., Nucci, C., & Cerulli, L. (2014). Evaluation of fixation stability using different targets with the MP1 microperimeter. International Ophthalmology. https://doi.org/10.1007/s10792-014-9924-x
Evans, B. J., Drasdo, N., & Richards, I. L. (1994). An investigation of some sensory and refractive visual factors in dyslexia. Vision Research, 34(14), 1913–26.
Falkenberg, H. K., Rubin, G. S., & Bex, P. J. (2007). Acuity, crowding, reading and fixation stability. Vision Research, 47(1), 126–35. https://doi.org/10.1016/j.visres.2006.09.014
Fischer, B. (2012). Subitizing, dynamic vision, saccade and fixation control in dyslexia. In J. Stein & Z. Kapoula (Eds.), Visual aspects of dyslexia (pp. 15–43). Oxford University Press.
Gonzalez, C. C., Mon-Williams, M., Burke, S., & Burke, M. R. (2016). Cognitive control of saccadic eye movements in children with developmental coordination disorder. PLoS One, 11(11), e0165380. https://doi.org/10.1371/journal.pone.0165380
Heim, S., Tschierse, J., Amunts, K., Wilms, M., Vossel, S., Willmes, K., Grabowska, A., & Huber, W. (2008). Cognitive subtypes of dyslexia. Acta Neurobiologiae Experimentalis (Wars), 68(1), 73–82.
Helland, T., Plante, E., & Hugdahl, K. (2011). Predicting dyslexia at age 11 from a risk index questionnaire at age 5. Dyslexia, 17(3), 207–26. https://doi.org/10.1002/dys.432
Holmqvist, K., Nyström, M., Andersson, R., Dewhurst, R., Jarodzka, H., &
van de Weijer, J. (2011). Eye tracking - a comprehensive guide to methods and measures (1st ed.). Oxford University Press.
Hutzler, F., Kronbichler, M., Jacobs, A. M., & Wimmer, H. (2006). Perhaps correlational but not causal: No effect of dyslexic readers’ magnocellular system on their eye movements during reading. Neuropsychologia, 44(4), 637–48. https://doi.org/10.1016/j.neuropsychologia.2005.06.006
Jainta, S., & Kapoula, Z. (2011). Dyslexic children are confronted with unstable binocular fixation while reading. PLoS One, 6(4), e18694. https://doi.org/10.1371/journal.pone.0018694
Kapoula, Z., Bucci, M. P., Jurion, F., Ayoun, J., Afkhami, F., & Bremond-Gignac, D. (2007). Evidence for frequent divergence impairment in French dyslexic children: Deficit of convergence relaxation or of divergence per se? Graefe’s Archive for Clinical and Experimental Ophthalmology, 245(7), 931–6. https://doi.org/10.1007/s00417-006-0490-4
Kowler, E., Anderson, E., Dosher, B., & Blaser, E. (1995). The role of attention in the programming of saccades. Vision Research, 35(13), 1897–916.
Kristjànsson2011, À. (2011). The intriguing interactive relationship between visual attention and saccadic eye movements. In S. P. Liversedge, I. D. Gilchrist, & S. Everling (Eds.), The oxford handbook of eye movements (pp. 456–466). Oxford University Press.
Kulp, M. T., & Schmidt, P. P. (1996). Effect of oculomotor and other visual skills on reading performance: A literature review. Optometry and Vision Science, 73(4), 283–92.
Leonard, C. M., Lombardino, L. J., Walsh, K., Eckert, M. A., Mockler, J. L., Rowe, L. A., Williams, S., & DeBose, C. B. (2002). Anatomical risk factors that distinguish dyslexia from SLI predict reading skill in normal children. Journal of Communication Disorders, 35(6), 501–31.
Lukov, L., Friedmann, N., Shalev, L., Khentov-Kraus, L., Shalev, N., Lorber, R., & Guggenheim, R. (2014). Dissociations between developmental dyslexias and attention deficits. Frontiers in Psychology, 5, 1501. https://doi.org/10.3389/fpsyg.2014.01501
Mapp, A. P., Ono, H., & Barbeito, R. (2003). What does the dominant eye dominate? A brief and somewhat contentious review. Perception & Psychophysics, 65(2), 310–7.
Melby-Lervåg, M., Lyster, S. A., & Hulme, C. (2012). Phonological skills and their role in learning to read: A meta-analytic review. Psychological Bulletin, 138(2), 322–52. https://doi.org/10.1037/a0026744
Morken, F., & Helland, T. (2013). Writing in dyslexia: Product and process. Dyslexia, 19(3), 131–48. https://doi.org/10.1002/dys.1455
Munoz, D. P., Armstrong, I. T., Hampton, K. A., & Moore, K. D. (2003). Altered control of visual fixation and saccadic eye movements in attention-deficit hyperactivity disorder. Journal of Neurophysiology, 90(1), 503–14. https://doi.org/10.1152/jn.00192.2003
Nergård-Nilssen, T., & Eklund, K. (2018). Evaluation of the psychometric properties of ”The Norwegian screening test for dyslexia”. Dyslexia, 24(3), 250–262. https://doi.org/10.1002/dys.1577
Nicolson, R. I., Fawcett, A. J., Berry, E. L., Jenkins, I. H., Dean, P., &
Brooks, D. J. (1999). Association of abnormal cerebellar activation with motor learning difficulties in dyslexic adults. Lancet, 353(9165), 1662–7. https://doi.org/10.1016/s0140-6736(98)09165-x
Norton, E. S., Beach, S. D., & Gabrieli, J. D. (2015). Neurobiology of dyslexia. Current Opinion in Neruobiology, 30, 73–8. https://doi.org/10.1016/j.conb.2014.09.007
Olulade, O. A., Napoliello, E. M., & Eden, G. F. (2013). Abnormal visual motion processing is not a cause of dyslexia. Neuron, 79(1), 180–190. https://doi.org/110.1016/j.neuron.2013.1005.1002
Otero-Millan, J., Macknik, S. L., & Martinez-Conde, S. (2014). Fixational eye movements and binocular vision. Frontiers in Integrative Neuroscience, 8, 52. https://doi.org/10.3389/fnint.2014.00052
Ottem, E., & Frost, J. (2011). Språk 6-16 - manual III.
Peterson, R. L., & Pennington, B. F. (2012). Developmental dyslexia. Lancet,
Clinical Ophthalmology, 7, 869–81. https://doi.org/10.2147/opth.s41607
Raymond, J. E., Ogden, N. A., Fagan, J. E., & Kaplan, B. J. (1988). Fixational instability and saccadic eye movements of dyslexic children with subtle cerebellar dysfunction. American Journal of Optometry and Physiological Optics, 65(3), 174–81.
Rayner, K. (1998). Eye movements in reading and information processing: 20 years of research. Psychological Bulletin, 124(3), 372–422.
Rice, M. L., Leske, D. A., Smestad, C. E., & Holmes, J. M. (2008). Results of ocular dominance testing depend on assessment method. Journal of American Association for Pediatric Ophthalmology and Strabismus, 12(4), 365–9. https://doi.org/10.1016/j.jaapos.2008.01.017
Richlan, F. (2012). Developmental dyslexia: Dysfunction of a left hemisphere reading network. Frontiers in Human Neuroscience, 6, 120. https://doi.org/10.3389/fnhum.2012.00120
Rolfs, M. (2009). Microsaccades: Small steps on a long way. Vision Research, 49(20), 2415–41. https://doi.org/10.1016/j.visres.2009.08.010
Rommelse, N. N., Van der Stigchel, S., & Sergeant, J. A. (2008). A review on eye movement studies in childhood and adolescent psychiatry. Brain and Cognition, 68(3), 391–414. https://doi.org/10.1016/j.bandc.2008.08.025
Scheiman, M., & Wick, B. (2002). Clinical management of binocular vision: Heterophoric, accommodative, and eye movement disorders (2nd ed. Philadelphia). Lippincott Williams & Wilkins.
Schulte-Korne, G. (2010). The prevention, diagnosis, and treatment of dyslexia. Deutsches Arzteblatt international, 107(41), 718–26, quiz 27. https://doi.org/10.3238/arztebl.2010.0718
Shaywitz, B. A., Lyon, G. R., & Shaywitz, S. E. (2006). The role of functional magnetic resonance imaging in understanding reading and dyslexia. Developmental Neuropsychology, 30(1), 613–32. http://www.tandfonline.com/doi/abs/10.1207/s15326942dn3001_5
Stein, J. (2014). Dyslexia: The role of vision and visual attention. Current Development Disorders Reports, 1(4), 267–280. http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC4203994/pdf/40474_2014_Article_30.pdf
Stoodley, C. J., & Stein, J. F. (2013). Cerebellar function in developmental dyslexia. Cerebellum, 12(2), 267–76. https://doi.org/10.1007/s12311-012-0407-1
Sumner, E., Hutton, S. B., Kuhn, G., & Hill, E. L. (2016). Oculomotor atypicalities in developmental coordination disorder. Developmental Science. https://doi.org/10.1111/desc.12501
Vagge, A., Cavanna, M., Traverso, C. E., & Iester, M. (2015). Evaluation of ocular movements in patients with dyslexia. Annals of Dyslexia, 65(1), 24–32. https://doi.org/10.1007/s11881-015-0098-7
Vidyasagar, T. R. (2019). Visual attention and neural oscillations in reading and dyslexia: Are they possible targets for remediation? Neuropsychologia, 130, 59–65. https://doi.org/10.1016/j.neuropsychologia.2019.02.009
Vidyasagar, T. R., & Pammer, K. (2010). Dyslexia: A deficit in visuo-spatial attention, not in phonological processing. Trends in Cognitive Sciences, 14(2), 57–63. https://doi.org/10.1016/j.tics.2009.12.003
Vikesdal, G., & Langaas, T. (2016a). Optically induced refractive errors reduces fixation stability but saccade latency remains stable. Journal of Eye Movement Research, 9(7), 1–8.
Vikesdal, G., & Langaas, T. (2016b). Saccade latency and fixation stability: Repeatability and reliability. Journal of Eye Movement Research, 9(2), 1–13.
Vikesdal, G., Mon-Williams, M., & Langaas, T. (2020). Optometric disorders in children and adults with dyslexia. Scandinavian Journal of Educational Research, 64(4), 601–611. https://doi.org/10.1080/00313831.2019.1595715
Wahlberg-Ramsay, M., Nordstrom, M., Salkic, J., & Brautaset, R. (2012). Evaluation of aspects of binocular vision in children with dyslexia. Strabismus., 20(4), 139–44. https://doi.org/10.3109/09273972.2012.735335
Williams, M. C., & Lecluyse, K. (1990). Perceptual consequences of a temporal processing deficit in reading disabled children. Journal of the American Optometry Association, 61(2), 111–21.
WMA Declaration of Helsinki - Ethical principles for medical research involving human subjects. (2013). http://www.wma.net/en/30publications/10policies/b3/index.html
Ygge, J., Lennerstrand, G., Rydberg, A., Wijecoon, S., & Pettersson, B. M. (1993). Oculomotor functions in a swedish population of dyslexic and normally reading children. Acta Ophthalmologica, 71(1), 10–21.