Pursuit eye movements in dyslexic children: evidence for an immaturity of brain oculomotor structures?

Background: Dyslexia is a disorder found in 5–10% of school-aged children. Several studies reported visual deficits and oculomotor abnormalities in dyslexic children. The objective of our study was to examine horizontal pursuit performance in dyslexic children, despite its poor involvement in reading. Methods: Eye movements were recorded by video-oculography in 92 children (46 dyslexic children, mean age: 9.77 ± 0.26 and 46 non dyslexic, IQ- and age-matched children). Both the number of catch-up saccades occurring during pursuit task and the gain of pursuit were measured. Results: Catch-up saccades were significantly more frequent in the dyslexic group than in the non-dyslexic group of children. Pursuit performance (in terms of the number of catch-up saccades and gain) significantly improved with increasing age in the non-dyslexic children group only. Conclusions: The atypical pursuit patterns observed in dyslexic children suggest a deficiency in the visual attentional processing and an immaturity of brain structures responsible for pursuit triggering. This finding needs to be validated by neuroimaging studies on dyslexia population.

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Role of Primate Cerebellar Hemisphere in Voluntary Eye Movement Control Revealed by Lesion Effects

Journal of Neurophysiology ◽

10.1152/jn.90440.2008 ◽

2009 ◽

Vol 101 (2) ◽

pp. 934-947 ◽

Cited By ~ 35

Author(s):

Masafumi Ohki ◽

Hiromasa Kitazawa ◽

Takahito Hiramatsu ◽

Kimitake Kaga ◽

Taiko Kitamura ◽

...

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Smooth Pursuit ◽

Movement Control ◽

Cerebellar Hemisphere ◽

Target Velocity ◽

Eye Movement Control ◽

Pursuit Eye Movements ◽

Catch Up

The anatomical connection between the frontal eye field and the cerebellar hemispheric lobule VII (H-VII) suggests a potential role of the hemisphere in voluntary eye movement control. To reveal the involvement of the hemisphere in smooth pursuit and saccade control, we made a unilateral lesion around H-VII and examined its effects in three Macaca fuscata that were trained to pursue visually a small target. To the step (3°)-ramp (5–20°/s) target motion, the monkeys usually showed an initial pursuit eye movement at a latency of 80–140 ms and a small catch-up saccade at 140–220 ms that was followed by a postsaccadic pursuit eye movement that roughly matched the ramp target velocity. After unilateral cerebellar hemispheric lesioning, the initial pursuit eye movements were impaired, and the velocities of the postsaccadic pursuit eye movements decreased. The onsets of 5° visually guided saccades to the stationary target were delayed, and their amplitudes showed a tendency of increased trial-to-trial variability but never became hypo- or hypermetric. Similar tendencies were observed in the onsets and amplitudes of catch-up saccades. The adaptation of open-loop smooth pursuit velocity, tested by a step increase in target velocity for a brief period, was impaired. These lesion effects were recognized in all directions, particularly in the ipsiversive direction. A recovery was observed at 4 wk postlesion for some of these lesion effects. These results suggest that the cerebellar hemispheric region around lobule VII is involved in the control of smooth pursuit and saccadic eye movements.

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Adaptation of catch-up saccades during the initiation of smooth pursuit eye movements

Experimental Brain Research ◽

10.1007/s00221-011-2581-7 ◽

2011 ◽

Vol 209 (4) ◽

pp. 537-549 ◽

Cited By ~ 8

Author(s):

Alexander C. Schütz ◽

David Souto

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Catch Up

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Choosing a foveal goal recruits the saccadic system during smooth pursuit

Journal of Neurophysiology ◽

10.1152/jn.00418.2017 ◽

2018 ◽

Vol 120 (2) ◽

pp. 489-496 ◽

Cited By ~ 4

Author(s):

Stephen J. Heinen ◽

Jeremy B. Badler ◽

Scott N. J. Watamaniuk

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Retinal Image ◽

Central Element ◽

Central Feature ◽

Smooth Pursuit Eye Movements ◽

Large Object ◽

Pursuit Eye Movements ◽

Saccadic System ◽

Catch Up

Models of smooth pursuit eye movements stabilize an object’s retinal image, yet pursuit is peppered with small, destabilizing “catch-up” saccades. Catch-up saccades might help follow a small, spot stimulus used in most pursuit experiments, since fewer of them occur with large stimuli. However, they can return when a large stimulus has a small central feature. It may be that a central feature on a large object automatically recruits the saccadic system. Alternatively, a cognitive choice is made that the feature is the pursuit goal, and the saccadic system is then recruited to pursue it. Observers pursued a 5-dot stimulus composed of a central dot surrounded by four peripheral dots arranged as a diamond. An attention task specified the pursuit goal as either the central element, or the diamond gestalt. Fewer catch-up saccades occurred with the Gestalt goal than with the central goal, although the additional saccades with the central goal neither enhanced nor impeded pursuit. Furthermore, removing the central element from the diamond goal further reduced catch-up saccade frequency, indicating that the central element automatically triggered some saccades. Higher saccade frequency was not simply due to narrowly focused attention, since attending a small peripheral diamond during pursuit elicited fewer saccades than attending the diamond positioned foveally. The results suggest some saccades are automatically elicited by a small central element, but when it is chosen as the pursuit goal the saccadic system is further recruited to pursue it. NEW & NOTEWORTHY Smooth-pursuit eye movements stabilize retinal image motion to prevent blur. Curiously, smooth pursuit is frequently supplemented by small catchup saccades that could reduce image clarity. Catchup saccades might only be needed to pursue small laboratory stimuli, as they are infrequent during large object pursuit. Yet large objects with central features revive them. Here, we show that voluntarily selecting a feature as the pursuit goal elicits saccades that do not help pursuit.

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Neuronal control of fixation and fixational eye movements

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0205 ◽

2017 ◽

Vol 372 (1718) ◽

pp. 20160205 ◽

Cited By ~ 59

Author(s):

Richard J. Krauzlis ◽

Laurent Goffart ◽

Ziad M. Hafed

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Brain Structures ◽

Eye Position ◽

Smooth Pursuit Eye Movements ◽

Ocular Fixation ◽

Pursuit Eye Movements ◽

Fixational Eye Movements ◽

Neuronal Control ◽

Neuronal Mechanisms

Ocular fixation is a dynamic process that is actively controlled by many of the same brain structures involved in the control of eye movements, including the superior colliculus, cerebellum and reticular formation. In this article, we review several aspects of this active control. First, the decision to move the eyes not only depends on target-related signals from the peripheral visual field, but also on signals from the currently fixated target at the fovea, and involves mechanisms that are shared between saccades and smooth pursuit. Second, eye position during fixation is actively controlled and depends on bilateral activity in the superior colliculi and medio-posterior cerebellum; disruption of activity in these circuits causes systematic deviations in eye position during both fixation and smooth pursuit eye movements. Third, the eyes are not completely still during fixation but make continuous miniature movements, including ocular drift and microsaccades, which are controlled by the same neuronal mechanisms that generate larger saccades. Finally, fixational eye movements have large effects on visual perception. Ocular drift transforms the visual input in ways that increase spatial acuity; microsaccades not only improve vision by relocating the fovea but also cause momentary changes in vision analogous to those caused by larger saccades. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.

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Improvement of Pursuit Eye Movement Alterations after Short Visuo-Attentional Training in ADHD

Brain Sciences ◽

10.3390/brainsci10110816 ◽

2020 ◽

Vol 10 (11) ◽

pp. 816

Author(s):

Simona Caldani ◽

Richard Delorme ◽

Ana Moscoso ◽

Mathilde Septier ◽

Eric Acquaviva ◽

...

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Neurodevelopmental Disorder ◽

Diagnostic Procedures ◽

Training Period ◽

Children With Adhd ◽

Attentional Training ◽

Pursuit Eye Movements ◽

Catch Up ◽

Pursuit Gain

Attention-deficit/hyperactivity disorder (ADHD) is a neurodevelopmental disorder without validated and objective diagnostic procedures. Several neurological dysfunctions in the frontal circuit, in the thalamus, and in the cerebellum have been observed in subjects with ADHD. These cortical and subcortical areas are responsible for eye movement control. Therefore, studying eye movements could be a useful tool to better understand neuronal alterations in subjects with ADHD. The aim of the present study was firstly to compare the quality of pursuit eye movements in a group of 40 children with ADHD (age 8.2 ± 1.2) and in a group of 40 sex-, IQ-, age-matched typically developing (TD) children; secondly, we aimed to examine if a short visuo-attentional training could affect pursuit performances in children with ADHD. Findings showed that children with ADHD presented a greater number of catch-up saccade and lower pursuit gain compared to TD children. Differently to TD children, in children with ADHD, the number of catch-up saccades and the pursuit gain were not significantly correlated with children’s age. Furthermore, a short visuo-attentional training period can only slightly improve pursuit performance in children with ADHD, leading to a decrease of the occurrence of catch-up saccades only, albeit the effect size was small. The absence of any improvement in pursuit performance with age could be explained by the fact that the prefrontal and fronto-cerebellar circuits responsible for pursuit triggering are still immature. Pursuit eye movements can be used as a useful tool for ADHD diagnosis. However, attentional mechanisms controlled by these cortical structures could be improved by a short visuo-attentional training period. Further studies will be necessary to explore the effects of a longer visuo-attentional training period on oculomotor tasks in order to clarify how adaptive mechanisms are able to increase the attentional capabilities in children with ADHD.

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Activity of fixation neurons in the monkey frontal eye field during smooth pursuit eye movements

Journal of Neurophysiology ◽

10.1152/jn.00816.2013 ◽

2014 ◽

Vol 112 (2) ◽

pp. 249-262 ◽

Cited By ~ 9

Author(s):

Yoshiko Izawa ◽

Hisao Suzuki

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Frontal Eye Field ◽

Smooth Pursuit Eye Movements ◽

Pursuit Eye Movements ◽

Eye Field ◽

Catch Up ◽

Discharge Patterns ◽

Reduced Activity

We recorded the activity of fixation neurons in the frontal eye field (FEF) in trained monkeys and analyzed their activity during smooth pursuit eye movements. Fixation neurons were densely located in the area of the FEF in the caudal part of the arcuate gyrus facing the inferior arcuate sulcus where focal electrical stimulation suppressed the generation of saccades and smooth pursuit in bilateral directions at an intensity lower than the threshold for eliciting electrically evoked saccades. Whereas fixation neurons discharged tonically during fixation, they showed a variety of discharge patterns during smooth pursuit, ranging from a decrease in activity to an increase in activity. Of these, more than two-thirds were found to show a reduction in activity during smooth pursuit in the ipsilateral and bilateral directions. The reduction in activity of fixation neurons began at pursuit initiation and continued during pursuit maintenance. When catch-up saccades during the initiation of pursuit were eliminated by a step-ramp target routine, the reduced activity of fixation neurons remained. The reduction in activity during pursuit was not dependent on the activity during fixation without a target. Based on these results, we discuss the role of the FEF at maintaining fixation in relation to various other brain areas. We suggest that fixation neurons in the FEF contribute to the suppression of smooth pursuit. These results suggest that FEF fixation neurons are part of a more generalized visual fixation system through which suppressive control is exerted on smooth pursuit, as well as saccades.

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Eye-position error influence over “open-loop” smooth pursuit initiation

10.1101/404491 ◽

2018 ◽

Cited By ~ 1

Author(s):

Antimo Buonocore ◽

Julianne Skinner ◽

Ziad M. Hafed

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Open Loop ◽

Position Error ◽

Visual Signals ◽

Error Signal ◽

Movement Initiation ◽

Pursuit Eye Movements ◽

Pursuit Initiation ◽

Catch Up

AbstractThe oculomotor system integrates a variety of visual signals into appropriate motor plans, but such integration can have widely varying time scales. For example, smooth pursuit eye movements to follow a moving target are slower and longer-lasting than saccadic eye movements, and it has been suggested that initiating a smooth pursuit eye movement involves an obligatory open-loop interval, in which new visual motion signals presumably cannot influence the ensuing motor plan for up to 100 ms after movement initiation. However, this view runs directly contrary to the idea that the oculomotor periphery has privileged access to short-latency visual signals. Here we show that smooth pursuit initiation is sensitive to visual inputs, even in “open-loop” intervals. We instructed male rhesus macaque monkeys to initiate saccade-free smooth pursuit eye movements, and we injected a transient, instantaneous eye position error signal at different times relative to movement initiation. We found robust short-latency modulations in eye velocity and acceleration, starting only ∼50 ms after transient signal occurrence, and even during “open-loop” pursuit initiation. Critically, the spatial direction of the injected position error signal had predictable effects on smooth pursuit initiation, with forward errors increasing eye acceleration and backwards errors reducing it. Catch-up saccade frequencies and amplitudes were also similarly altered ∼50 ms after transient signals, much like well-known effects on microsaccades during fixation. Our results demonstrate that smooth pursuit initiation is highly sensitive to visual signals, and that catch-up saccade generation is reset after a visual transient.

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