Abnormal Fixational Eye Movements in Amblyopia
Aasef G Shaikh, Jorge Otero-Millan, Priyanka Kumar, Fatema F Ghasia, Aasef G Shaikh, Jorge Otero-Millan, Priyanka Kumar, Fatema F Ghasia
Abstract
Purpose: Fixational saccades shift the foveal image to counteract visual fading related to neural adaptation. Drifts are slow eye movements between two adjacent fixational saccades. We quantified fixational saccades and asked whether their changes could be attributed to pathologic drifts seen in amblyopia, one of the most common causes of blindness in childhood.
Methods: Thirty-six pediatric subjects with varying severity of amblyopia and eleven healthy age-matched controls held their gaze on a visual target. Eye movements were measured with high-resolution video-oculography during fellow eye-viewing and amblyopic eye-viewing conditions. Fixational saccades and drifts were analyzed in the amblyopic and fellow eye and compared with controls.
Results: We found an increase in the amplitude with decreased frequency of fixational saccades in children with amblyopia. These alterations in fixational eye movements correlated with the severity of their amblyopia. There was also an increase in eye position variance during drifts in amblyopes. There was no correlation between the eye position variance or the eye velocity during ocular drifts and the amplitude of subsequent fixational saccade. Our findings suggest that abnormalities in fixational saccades in amblyopia are independent of the ocular drift.
Discussion: This investigation of amblyopia in pediatric age group quantitatively characterizes the fixation instability. Impaired properties of fixational saccades could be the consequence of abnormal processing and reorganization of the visual system in amblyopia. Paucity in the visual feedback during amblyopic eye-viewing condition can attribute to the increased eye position variance and drift velocity.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
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![Fig 4. Comparison of amplitude to velocity…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4773232/bin/pone.0149953.g004.jpg)
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References
- Preslan MW, Novak A (1996) Baltimore Vision Screening Project. Ophthalmology 103: 105–109.
- Flom MC, Neumaier RW (1966) Prevalence of amblyopia. Am J Optom Arch Am Acad Optom 43: 732–751.
- Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278: 377–409.
- Wiesel TN, Hubel DH (1963) Single-Cell Responses in Striate Cortex of Kittens Deprived of Vision in One Eye. J Neurophysiol 26: 1003–1017.
- McKee SP, Levi DM, Movshon JA (2003) The pattern of visual deficits in amblyopia. J Vis 3: 380–405.
- Levi DM (2006) Visual processing in amblyopia: human studies. Strabismus 14: 11–19.
- Kiorpes L (2006) Visual processing in amblyopia: animal studies. Strabismus 14: 3–10.
- McCamy MB, Macknik SL, Martinez-Conde S (2014) Different fixational eye movements mediate the prevention and the reversal of visual fading. J Physiol 592: 4381–4394. 10.1113/jphysiol.2014.279059
- Ratliff F, Riggs LA (1950) Involuntary motions of the eye during monocular fixation. J Exp Psychol 40: 687–701.
- Martinez-Conde S (2006) Fixational eye movements in normal and pathological vision. Prog Brain Res 154: 151–176.
- Ditchburn RW (1980) The function of small saccades. Vision Res 20: 271–272.
- Ditchburn RW, Ginsborg BL (1952) Vision with a stabilized retinal image. Nature 170: 36–37.
- Ditchburn RW, Ginsborg BL (1953) Involuntary eye movements during fixation. J Physiol 119: 1–17.
- Engbert R, Mergenthaler K (2006) Microsaccades are triggered by low retinal image slip. Proc Natl Acad Sci U S A 103: 7192–7197.
- Martinez-Conde S, Macknik SL, Hubel DH (2000) Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nat Neurosci 3: 251–258.
- Gonzalez EG, Wong AM, Niechwiej-Szwedo E, Tarita-Nistor L, Steinbach MJ (2012) Eye position stability in amblyopia and in normal binocular vision. Invest Ophthalmol Vis Sci 53: 5386–5394. 10.1167/iovs.12-9941
- Subramanian V, Jost RM, Birch EE (2013) A quantitative study of fixation stability in amblyopia. Invest Ophthalmol Vis Sci 54: 1998–2003. 10.1167/iovs.12-11054
- Chung ST, Kumar G, Li RW, Levi DM (2015) Characteristics of fixational eye movements in amblyopia: Limitations on fixation stability and acuity? Vision Res 114: 87–99. 10.1016/j.visres.2015.01.016
- Schneider RM, Thurtell MJ, Eisele S, Lincoff N, Bala E, Leigh RJ (2013) Neurological basis for eye movements of the blind. PLoS One 8: e56556 10.1371/journal.pone.0056556
- McCamy MB, Otero-Millan J, Macknik SL, Yang Y, Troncoso XG, Baer SM, et al. (2012) Microsaccadic efficacy and contribution to foveal and peripheral vision. J Neurosci 32: 9194–9204. 10.1523/JNEUROSCI.0515-12.2012
- Troncoso XG, Macknik SL, Martinez-Conde S (2008) Microsaccades counteract perceptual filling-in. J Vis 8: 15 11–19.
- Otero-Millan J, Castro JL, Macknik SL, Martinez-Conde S (2014) Unsupervised clustering method to detect microsaccades. J Vis 14.
- Martinez-Conde S, Macknik SL, Troncoso XG, Hubel DH (2009) Microsaccades: a neurophysiological analysis. Trends Neurosci 32: 463–475. 10.1016/j.tins.2009.05.006
- Rolfs M (2009) Microsaccades: small steps on a long way. Vision Res 49: 2415–2441. 10.1016/j.visres.2009.08.010
- Mergenthaler K, Engbert R (2010) Microsaccades are different from saccades in scene perception. Exp Brain Res 203: 753–757. 10.1007/s00221-010-2272-9
- Collewijn H, Kowler E (2008) The significance of microsaccades for vision and oculomotor control. J Vis 8: 20 21–21.
- Ko HK, Poletti M, Rucci M (2010) Microsaccades precisely relocate gaze in a high visual acuity task. Nat Neurosci 13: 1549–1553. 10.1038/nn.2663
- Steinman RM, Cushman WB, Martins AJ (1982) The precision of gaze. A review. Hum Neurobiol 1: 97–109.
- Thaler L, Schutz AC, Goodale MA, Gegenfurtner KR (2013) What is the best fixation target? The effect of target shape on stability of fixational eye movements. Vision Res 76: 31–42. 10.1016/j.visres.2012.10.012
- Castet E, Crossland M (2012) Quantifying eye stability during a fixation task: a review of definitions and methods. Seeing Perceiving 25: 449–469.
- McCamy MB, Otero-Millan J, Leigh RJ, King SA, Schneider RM, Macknik SL, et al. (2015) Simultaneous recordings of human microsaccades and drifts with a contemporary video eye tracker and the search coil technique. PLoS One 10: e0128428 10.1371/journal.pone.0128428
- Otero-Millan J, Serra A, Leigh RJ, Troncoso XG, Macknik SL, Martinez-Conde S (2011) Distinctive features of saccadic intrusions and microsaccades in progressive supranuclear palsy. J Neurosci 31: 4379–4387. 10.1523/JNEUROSCI.2600-10.2011
- Otero-Millan J, Macknik SL, Langston RE, Martinez-Conde S (2013) An oculomotor continuum from exploration to fixation. Proc Natl Acad Sci U S A 110: 6175–6180. 10.1073/pnas.1222715110
- Shi XF, Xu LM, Li Y, Wang T, Zhao KX, Sabel BA (2012) Fixational saccadic eye movements are altered in anisometropic amblyopia. Restor Neurol Neurosci 30: 445–462. 10.3233/RNN-2012-129000
- Otero-Millan J, Troncoso XG, Macknik SL, Serrano-Pedraza I, Martinez-Conde S (2008) Saccades and microsaccades during visual fixation, exploration, and search: foundations for a common saccadic generator. J Vis 8: 21 21–18.
- Leigh RJZDS (2006) The Neurology of Eye Movements.
Source: PubMed