Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: evidence from a reading and visual search study

Studies comparing binocular eye movements during reading and visual search in dyslexic children are, at our knowledge, inexistent. In the present study we examined ocular motor characteristics in dyslexic children versus two groups of non dyslexic children with chronological/reading age-matched. Binocular eye movements were recorded by an infrared system (mobileEBT®, e(ye)BRAIN) in twelve dyslexic children (mean age 11 years old) and a group of chronological age-matched (N = 9) and reading age-matched (N = 10) non dyslexic children. Two visual tasks were used: text reading and visual search. Independently of the task, the ocular motor behavior in dyslexic children is similar to those reported in reading age-matched non dyslexic children: many and longer fixations as well as poor quality of binocular coordination during and after the saccades. In contrast, chronological age-matched non dyslexic children showed a small number of fixations and short duration of fixations in reading task with respect to visual search task; furthermore their saccades were well yoked in both tasks. The atypical eye movement''s patterns observed in dyslexic children suggest a deficiency in the visual attentional processing as well as an immaturity of the ocular motor saccade and vergence systems interaction.     

Reading text increases binocular disparity in dyslexic children

Children with developmental dyslexia show reading impairment compared to their peers, despite being matched on IQ, socio-economic background, and educational opportunities. The neurological and cognitive basis of dyslexia remains a highly debated topic. Proponents of the magnocellular theory, which postulates abnormalities in the M-stream of the visual pathway cause developmental dyslexia, claim that children with dyslexia have deficient binocular coordination, and this is the underlying cause of developmental dyslexia. We measured binocular coordination during reading and a non-linguistic scanning task in three participant groups: adults, typically developing children, and children with dyslexia. A significant increase in fixation disparity was observed for dyslexic children solely when reading. Our study casts serious doubts on the claims of the magnocellular theory. The exclusivity of increased fixation disparity in dyslexics during reading might be a result of the allocation of inadequate attentional and/or cognitive resources to the reading process, or suboptimal linguistic processing per se.     

Binocular coordination of the eyes during reading

Saccadic eye movements and fixations are the behavioral means by which we visually sample text during reading. Human oculomotor control is governed by a complex neurophysiological system involving the brain stem, superior colliculus, and several cortical areas. A very widely held belief among researchers investigating primate vision is that the oculomotor system serves to orient the visual axes of both eyes to fixate the same target point in space. It is argued that such precise positioning of the eyes is necessary to place images on corresponding retinal locations, such that on each fixation a single, nondiplopic, visual representation is perceived. Vision works actively through a continual sampling process involving saccades and fixations. Here we report that during normal reading, the eyes do not always fixate the same letter within a word. We also demonstrate that saccadic targeting is yoked and based on a unified cyclopean percept of a whole word since it is unaffected if different word parts are delivered exclusively to each eye via a dichoptic presentation technique. These two findings together suggest that the visual signal from each eye is fused at a very early stage in the visual pathway, even when the fixation disparity is greater than one character (0.29 deg), and that saccade metrics for each eye are computed on the basis of that fused signal.     

Binocular coordination during reading]

Is there an effect on binocular coordination during reading of oculomotor imbalance (heterophoria, strabismus and inadequate convergence) and of functional lateral characteristics (eye preference and perceptually privileged visual laterality)? Recordings of the binocular eye-movements of ten-year-old children show that oculomotor imbalances occur most often among children whose left visual perceptual channel is privileged, and that these subjects can present optomotor dissociation and manifest lack of motor coordination. Close binocular motor coordination is far from being the norm in reading. The faster reader displays saccades of differing spatial amplitude and the slower reader an oculomotor hyperactivity, especially during fixations. The recording of binocular movements in reading appears to be an excellent means of diagnosing difficulties related to visual laterality and to problems associated with oculomotor imbalance.     

Effect of a dual task on postural control in dyslexic children

Several studies have examined postural control in dyslexic children; however, their results were inconclusive. This study investigated the effect of a dual task on postural stability in dyslexic children. Eighteen dyslexic children (mean age 10.3±1.2 years) were compared with eighteen non-dyslexic children of similar age. Postural stability was recorded with a platform (TechnoConcept®) while the child, in separate sessions, made reflex horizontal and vertical saccades of 10° of amplitude, and read a text silently. We measured the surface and the mean speed of the center of pressure (CoP). Reading performance was assessed by counting the number of words read during postural measures. Both groups of children were more stable while performing saccades than while reading a text. Furthermore, dyslexic children were significantly more unstable than non-dyslexic children, especially during the reading task. Finally, the number of words read by dyslexic children was significantly lower than that of non-dyslexic children and, in contrast to the non-dyslexic children. In line with the U-shaped non-linear interaction model, we suggest that the attention consumed by the reading task could be responsible for the loss of postural control in both groups of children. The postural instability observed in dyslexic children supports the hypothesis that such children have a lack of integration of multiple sensorimotor inputs.     

Effects of Prism Eyeglasses on Objective and Subjective Fixation Disparity

In optometry of binocular vision, the question may arise whether prisms should be included in eyeglasses to compensate an oculomotor and/or sensory imbalance between the two eyes. The corresponding measures of objective and subjective fixation disparity may be reduced by the prisms, or the adaptability of the binocular vergence system may diminish effects of the prisms over time. This study investigates effects of wearing prisms constantly for about 5 weeks in daily life. Two groups of 12 participants received eyeglasses with prisms having either a base-in direction or a base-out direction with an amount up to 8 prism diopters. Prisms were prescribed based on clinical fixation disparity test plates at 6 m. Two dependent variables were used: (1) subjective fixation disparity was indicated by a perceived offset of dichoptic nonius lines that were superimposed on the fusion stimuli and (2) objective fixation disparity was measured with a video based eye tracker relative to monocular calibration. Stimuli were presented at 6 m and included either central or more peripheral fusion stimuli. Repeated measurements were made without the prisms and with the prisms after about 5 weeks of wearing these prisms. Objective and subjective fixation disparity were correlated, but the type of fusion stimulus and the direction of the required prism may play a role. The prisms did not reduce the fixation disparity to zero, but induced significant changes in fixation disparity with large effect sizes. Participants receiving base-out prisms showed hypothesized effects, which were concurrent in both types of fixation disparity. In participants receiving base-in prisms, the individual effects of subjective and objective effects were negatively correlated: the larger the subjective (sensory) effect, the smaller the objective (motor) effect. This response pattern was related to the vergence adaptability, i.e. the individual fusional vergence reserves.     

Reading and Visual Search: A Developmental Study in Normal Children

Studies dealing with developmental aspects of binocular eye movement behaviour during reading are scarce. In this study we have explored binocular strategies during reading and during visual search tasks in a large population of normal young readers. Binocular eye movements were recorded using an infrared video-oculography system in sixty-nine children (aged 6 to 15) and in a group of 10 adults (aged 24 to 39). The main findings are (i) in both tasks the number of progressive saccades (to the right) and regressive saccades (to the left) decreases with age; (ii) the amplitude of progressive saccades increases with age in the reading task only; (iii) in both tasks, the duration of fixations as well as the total duration of the task decreases with age; (iv) in both tasks, the amplitude of disconjugacy recorded during and after the saccades decreases with age; (v) children are significantly more accurate in reading than in visual search after 10 years of age. Data reported here confirms and expands previous studies on children''s reading. The new finding is that younger children show poorer coordination than adults, both while reading and while performing a visual search task. Both reading skills and binocular saccades coordination improve with age and children reach a similar level to adults after the age of 10. This finding is most likely related to the fact that learning mechanisms responsible for saccade yoking develop during childhood until adolescence.     

Ocular vergence under natural conditions. II. Gaze shifts between real targets differing in distance and direction

Horizontal binocular eye movements of three subjects were recorded with the scleral sensor coil--revolving magnetic field technique during voluntary shifts of gaze between pairs of stationary, real, continuously visible targets. The target pairs were located either along the median plane (requiring symmetrical vergence), or on either side of the median plane (requiring asymmetrical vergence). Symmetrical vergence was primarily smooth, but it was often assisted by small, disjunctive saccades. Peak vergence speeds were very high; they increased from about 50 degrees s-1 for vergence changes of 5 degrees to between 150 and 200 degrees s-1 for vergence changes of 34 degrees. Differences between convergence and divergence were idiosyncratic. Asymmetrical vergence, requiring a vergence of 11 degrees combined with a version of 45 degrees, was largely saccadic. Unequal saccades mediated virtually all (95%) of the vergence required in the divergent direction, whereas 75% of the vergence required in the convergent direction was mediated by unequal saccades, with the remaining convergence mediated by smooth vergence, following completion of the saccades. Peak divergence speeds during these saccades were very high (180 degrees s-1 for a change of vergence of 11 degrees); much faster than the smooth, symmetrical vergence change of comparable size (14 degrees). Peak convergent saccadic speeds were about 20% lower. This difference in peak speed was caused by an initial, transient divergence, observed at the beginning of all horizontal saccades. The waveform of disjunctive saccades did not have the same shape as the waveform of conjugate saccades of similar size. The smaller saccade of the disjunctive pair was stretched out in time so as to have the same duration as its larger, companion saccade. These results permitted the conclusion that the subsystems controlling saccades and vergence are not independent. Vergence responses were relatively slow and incomplete with monocular viewing, which excluded disparity as a cue. Monocularly stimulated vergence decreased as a function of the increasing presbyopia of our three subjects. Subjects were able to generate some vergence in darkness towards previously seen and remembered targets. Such responses, however, were slow, irregular and evanescent. In conclusion, vergence shifts between targets, which provided all natural cues to distance, were fast and accurate; they appeared adequate to provide effective binocular vision under natural conditions. This result could not have been expected on the basis of previous observations, all of which had been made with severely reduced cues to depth.(ABSTRACT TRUNCATED AT 400 WORDS)     

Binocular coordination: reading stereoscopic sentences in depth

The present study employs a stereoscopic manipulation to present sentences in three dimensions to subjects as they read for comprehension. Subjects read sentences with (a) no depth cues, (b) a monocular depth cue that implied the sentence loomed out of the screen (i.e., increasing retinal size), (c) congruent monocular and binocular (retinal disparity) depth cues (i.e., both implied the sentence loomed out of the screen) and (d) incongruent monocular and binocular depth cues (i.e., the monocular cue implied the sentence loomed out of the screen and the binocular cue implied it receded behind the screen). Reading efficiency was mostly unaffected, suggesting that reading in three dimensions is similar to reading in two dimensions. Importantly, fixation disparity was driven by retinal disparity; fixations were significantly more crossed as readers progressed through the sentence in the congruent condition and significantly more uncrossed in the incongruent condition. We conclude that disparity depth cues are used on-line to drive binocular coordination during reading.     

Both Lexical and Non-Lexical Characters Are Processed during Saccadic Eye Movements

On average our eyes make 3–5 saccadic movements per second when we read, although their neural mechanism is still unclear. It is generally thought that saccades help redirect the retinal fovea to specific characters and words but that actual discrimination of information only occurs during periods of fixation. Indeed, it has been proposed that there is active and selective suppression of information processing during saccades to avoid experience of blurring due to the high-speed movement. Here, using a paradigm where a string of either lexical (Chinese) or non-lexical (alphabetic) characters are triggered by saccadic eye movements, we show that subjects can discriminate both while making saccadic eye movement. Moreover, discrimination accuracy is significantly better for characters scanned during the saccadic movement to a fixation point than those not scanned beyond it. Our results showed that character information can be processed during the saccade, therefore saccades during reading not only function to redirect the fovea to fixate the next character or word but allow pre-processing of information from the ones adjacent to the fixation locations to help target the next most salient one. In this way saccades can not only promote continuity in reading words but also actively facilitate reading comprehension.     

Cortical positive potentials in the period of eye fixation prior to saccades and antisaccades

The EEG of 10 right-handed healthy subjects preceding saccade and antisaccade with mean values of latency in the eye fixations period were selected and averaged. The positive potential P2 appearing on the fixation stimuly switching on and slow positive wave following after it were more prominent before antisaccades than normal saccades. Space-temporal analyses of presaccadic potentials showed that right frontal cortex was activated more before antisaccades. These findings suggest that right cortical hemisphere dominate in spatial attention and inhibition of automatic saccades to visual stimuli in the period of antisaccades preparing. During the period of central fixations "intermediate" positivity potentials, developing in 600-400 ms prior to saccade or antisaccade onset, were find out. These potentials were predominantly recorded in the left frontal and frontosagittal cortical areas. The obtained evidence suggest that "intermediate" positive potentials a period related to the process of motor attention, anticipation and decision making in the period of eyes fixation.     

Where Do the Eyes Really Go in the Hollow-Face Illusion?

The hollow-face illusion refers to the finding that people typically perceive a concave (hollow) mask as being convex, despite the presence of binocular disparity cues that indicate the contrary. Unlike other illusions of depth, recent research has suggested that the eyes tend to converge at perceived, rather than actual, depths. However, technical and methodological limitations prevented one from knowing whether disparity cues may still have influenced vergence. In the current study, we presented participants with virtual normal or hollow masks and asked them to fixate the tip of the face's nose until they had indicated whether they perceived it as pointing towards or away from them. The results showed that the direction of vergence was indeed determined by perceived depth, although vergence responses were both somewhat delayed and of smaller amplitude (by a factor of about 0.5) for concave than convex masks. These findings demonstrate how perceived depth can override disparity cues when it comes to vergence, albeit not entirely.     

Smooth Pursuit Eye Movements in Children with Strabismus and in Children with Vergence Deficits

Purpose

The objective of our study was to examine horizontal smooth pursuit performance in strabismic children and in children with vergence deficits, and to compare these data with those recorded in a group of control age-matched children.

Methods

Binocular eye movements were recorded by video-oculography in ten strabismic children (mean age: 9.8±0.8) and seven children with vergence deficits (mean age: 10.8±0.6). Data were compared to that of age-matched control children (mean age: 9.8±0.8 years).

Results

Catch-up saccades amplitude in strabismic children and in children with vergence deficits were significantly higher than in control age-matched children. Moreover, in strabismic children the amplitude of catch-up saccades was significantly higher in rightward than in leftward direction. The number of catch-up saccades was also significantly higher in rightward than in leftward direction. The gain value of pursuits in rightward direction was significantly higher in the right eye than in the left one; for the right eye, the gain value was significantly higher in rightward than in leftward direction. Binocular coordination of pursuit was better in control age-matched children than in children with vergence deficits and than in strabismic children.

Conclusions

Binocular coordination of pursuit is abnormal in children with vergence deficits and worse in strabismic children. Binocular vision plays an important role in improving binocular coordination of pursuit.     

Benefit of Bi-Ocular Visual Stimulation for Postural Control in Children with Strabismus

Vision is important for postural control as is shown by the Romberg quotient (RQ): with eyes closed, postural instability increases relative to eyes open (RQ = 2). Yet while fixating at far distance, postural stability is similar with eyes open and eyes closed (RQ = 1). Postural stability can be better with both eyes viewing than one eye, but such effect is not consistent among healthy subjects. The first goal of the study is to test the RQ as a function of distance for children with convergent versus divergent strabismus. The second goal is to test whether vision from two eyes relative to vision from one eye provides better postural stability. Thirteen children with divergent strabismus and eleven with convergent strabismus participated in this study. Posturtography was done with the Techno concept device. Experiment 1, four conditions: fixation at 40 cm and at 200 cm both with eyes open and eyes covered (evaluation of RQ). Experiment 2, six conditions: fixation at 40 cm and at 200 cm, with both eyes viewing or under monocular vision (dominant and non-dominant eye). For convergent strabismus, the groups mean value of RQ was 1.3 at near and 0.94 at far distance; for divergent, it was 1.06 at near and 1.68 at far. For all children, the surface of body sway was significantly smaller under both eyes viewing than monocular viewing (either eye). Increased RQ value at near for convergent and at far for divergent strabismus is attributed to the influence of the default strabismus angle and to better use of ocular motor signals. Vision with the two eyes improves postural control for both viewing distances and for both types of strabismus. Such benefit can be due to complementary mechanisms: larger visual field, better quality of fixation and vergence angle due to the use of visual inputs from both eyes.     

Start position strongly influences fixation patterns during face processing: difficulties with eye movements as a measure of information use

Fixation patterns are thought to reflect cognitive processing and, thus, index the most informative stimulus features for task performance. During face recognition, initial fixations to the center of the nose have been taken to indicate this location is optimal for information extraction. However, the use of fixations as a marker for information use rests on the assumption that fixation patterns are predominantly determined by stimulus and task, despite the fact that fixations are also influenced by visuo-motor factors. Here, we tested the effect of starting position on fixation patterns during a face recognition task with upright and inverted faces. While we observed differences in fixations between upright and inverted faces, likely reflecting differences in cognitive processing, there was also a strong effect of start position. Over the first five saccades, fixation patterns across start positions were only coarsely similar, with most fixations around the eyes. Importantly, however, the precise fixation pattern was highly dependent on start position with a strong tendency toward facial features furthest from the start position. For example, the often-reported tendency toward the left over right eye was reversed for the left starting position. Further, delayed initial saccades for central versus peripheral start positions suggest greater information processing prior to the initial saccade, highlighting the experimental bias introduced by the commonly used center start position. Finally, the precise effect of face inversion on fixation patterns was also dependent on start position. These results demonstrate the importance of a non-stimulus, non-task factor in determining fixation patterns. The patterns observed likely reflect a complex combination of visuo-motor effects and simple sampling strategies as well as cognitive factors. These different factors are very difficult to tease apart and therefore great caution must be applied when interpreting absolute fixation locations as indicative of information use, particularly at a fine spatial scale.     

Spatial and temporal measurements of eye movement in children with dyslexia

This paper presents the first reading data in Croatian collected with an eye-tracking device. The eye-tracking method allows for research into two crucial levels underlying reading: the visual and the cognitive. The aim of this paper is to show the differences in eye movements in children with dyslexia using the principles of cognitive-control view. Despite the well-known definitions and vast literature on dyslexia, the neural basis of dyslexia varies greatly on the individual level. The three children studied in this paper were tested behaviorally using set of language tests for language behavior assessment on all language levels: phonology, morphology, syntax, lexicon and pragmatics. Two children had low scores on most language tests, and all three children had poor reading and writing level. Each of the children had to read two texts silently while their eye movements were recorded by means of an infrared eye-tracking system. We analyzed the number, position, and duration of fixations and the number and position of regressive (or back) saccades. Our results show intergroup differences (between a typically developing child and the three children with dyslexia), and intragroup differences (among all three children with dyslexia). The great number of fixations, longer duration of fixations, and great number of regression saccades are the main features that differentiate the children with dyslexia form the typically developing child. The only difference found between language and visual subtypes of dyslexia was a shorter duration of fixations for the child with a visual processing disorder.     

Postural control during the Stroop test in dyslexic and non dyslexic teenagers

Postural control in quiet stance although simple still requires some cognitive resources; dual cognitive tasks influence further postural control. The present study examines whether or not dyslexic teenagers experience postural instability when performing a Stroop dual task for which their performances are known to be poor. Fifteen dyslexics and twelve non-dyslexics (14 to 17 years old) were recruited from the same school. They were asked to perform three tasks: (1) fixate a target, (2) perform an interference Stroop test (naming the colour or the word rather than reading the word), (3) performing flexibility Stroop task: the subject performed the interference task as in (2) except when the word was in a box, in which case he had to read the word. Postural performances were measured with a force platform. The results showed a main task effect on the variance of speed of body sway only: such variance was higher in the flexibility task than for the other two tasks. No group effect was found for any of the parameters of posture (surface, mediolateral and anteroposterior sway, variance of speed). Further wavelet analysis in the time-frequency domain revealed an increase in the spectral power of the medium frequency range believed to be related to cerebellum control; an accompanying increase in the cancellation time of the high frequency band related to reflexive loops occurred for non-dyslexics only. These effects occurred for the flexibility task and could be due to its high cognitive difficulty. Dyslexics displayed shorter cancellation time for the medium frequency band for all tasks, suggesting less efficient cerebellar control, perhaps of eye fixation and attention influencing body sway. We conclude that there is no evidence for a primary posture deficit in 15 year old teenagers who come from the general population and who were recruited in schools.     

An Eye Movement Study on the Role of the Visual Field Defect in Pure Alexia

Pure alexia is a severe impairment of word reading which is usually accompanied by a right-sided visual field defect. Patients with pure alexia exhibit better preserved writing and a considerable word length effect, claimed to result from a serial letter processing strategy. Two experiments compared the eye movements of four patients with pure alexia to controls with simulated visual field defects (sVFD) when reading single words. Besides differences in response times and differential effects of word length on word reading in both groups, fixation durations and the occurrence of a serial, letter-by-letter fixation strategy were investigated. The analyses revealed quantitative and qualitative differences between pure alexic patients and unimpaired individuals reading with sVFD. The patients with pure alexia read words slower and exhibited more fixations. The serial, letter-by-letter fixation strategy was observed only in the patients but not in the controls with sVFD. It is argued that the VFD does not cause pure alexic reading.     

Sensorimotor Integration in Dyslexic Children under Different Sensory Stimulations

Dyslexic children, besides difficulties in mastering literacy, also show poor postural control that might be related to how sensory cues coming from different sensory channels are integrated into proper motor activity. Therefore, the aim of this study was to examine the relationship between sensory information and body sway, with visual and somatosensory information manipulated independent and concurrently, in dyslexic children. Thirty dyslexic and 30 non-dyslexic children were asked to stand as still as possible inside of a moving room either with eyes closed or open and either lightly touching a moveable surface or not for 60 seconds under five experimental conditions: (1) no vision and no touch; (2) moving room; (3) moving bar; (4) moving room and stationary touch; and (5) stationary room and moving bar. Body sway magnitude and the relationship between room/bar movement and body sway were examined. Results showed that dyslexic children swayed more than non-dyslexic children in all sensory condition. Moreover, in those trials with conflicting vision and touch manipulation, dyslexic children swayed less coherent with the stimulus manipulation compared to non-dyslexic children. Finally, dyslexic children showed higher body sway variability and applied higher force while touching the bar compared to non-dyslexic children. Based upon these results, we can suggest that dyslexic children are able to use visual and somatosensory information to control their posture and use the same underlying neural control processes as non-dyslexic children. However, dyslexic children show poorer performance and more variability while relating visual and somatosensory information and motor action even during a task that does not require an active cognitive and motor involvement. Further, in sensory conflict conditions, dyslexic children showed less coherent and more variable body sway. These results suggest that dyslexic children have difficulties in multisensory integration because they may suffer from integrating sensory cues coming from multiple sources.     

Saccades and vergence performance in a population of children with vertigo and clinically assessed abnormal vergence capabilities

Purpose

Early studies reported some abnormalities in saccade and vergence eye movements in children with vertigo and vergence deficiencies. The purpose of this study was to further examine saccade and vergence performance in a population of 44 children (mean age: 12.3±1.6 years) with vertigo symptoms and with different levels of vergence abnormalities, as assessed by static orthoptic examination (near point of convergence, prism bar and cover-uncover test).

Methods

Three groups were identified on the basis of the orthoptic tests: group 1 (n = 13) with vergence spasms and mildly perturbed orthoptic scores, group 2 (n = 14) with moderately perturbed orthoptic scores, and group 3 (n = 17) with severely perturbed orthoptic scores. Data were compared to those recorded from 28 healthy children of similar ages. Latency, accuracy and peak velocity of saccades and vergence movements were measured in two different conditions: gap (fixation offset 200 ms prior to target onset) and simultaneous paradigms. Binocular horizontal movements were recorded by a photoelectric device.

Results

Group 2 of children with vergence abnormalities showed significantly longer latency than normal children in several types of eye movements recorded. For all three groups of children with vergence abnormalities, the gain was poor, particularly for vergence movement. The peak velocity values did not differ between the different groups of children examined.

Interpretation

Eye movement measures together with static orthoptic evaluation allowed us to better identify children with vergence abnormalities based on their slow initiation of eye movements. Overall, these findings support the hypothesis of a central deficit in the programming and triggering of saccades and vergence in these children.