[Computerized oculomotor training in dyslexia: A randomized, crossover clinical trial in pediatric population]. / Rééducation oculomotrice informatisée dans la dyslexie : essai clinique randomisé en crossover en population pédiatrique.

OBJECTIVE: Several studies have reported abnormal oculomotor capacities leading to reading/writing difficulties among dyslexic children. However, no randomized clinical trial has been conducted to determine whether oculomotor training improves reading/writing skills of these children. The present study aims to evaluate the efficacy of computer-based oculomotor training among dyslexic children. METHOD: Crossover randomized trial with enrollment from January 12, 2015 to July 24, 2015, and follow-up to February 4, 2016. Eleven children (aged 7 to 12 years old) with dyslexia were included in a French psychiatric unit. The computer-based oculomotor training consisted of exercises focused on control of saccadic movements (reflexes and voluntary saccades), vergences and visual attention and memory. At baseline, 3 and 6 months, participants were assessed on reading and writing skills as well as phonological skills, visuo-attentional skills and verbal memory using the French batterie analytique du langage écrit (BALE). Saccadic and antisaccadic ocular movements (latencies and gains) were recorded using a specific device. Several Anova models were performed to test whether oculomotor training improves reading, writing and phonological, verbal memory and visuo-attentional skills. Our analyses were considered exploratory (alpha at 5%). RESULTS: No effect of oculomotor training was found on reading skills. However, oculomotor training was associated with a short-term effect (after 3 months of training) on several tests measuring phonological skills (syllabic suppression; P-value=0.022), visuo-attentional skills (search of anarchic verbal cues; P-value=0.035) and verbal memory (digit span backward; P-value=0.022) and with a long-term effect (3 months after the end of the 3 months of training) on a measure of writing skills (regular words; P-value=0.019). Finally, training was associated with an increase of saccadic latencies indicating an increase of visuo-attentional skills (P-value=0.026). CONCLUSIONS: Our results suggested that computer-based oculomotor training might be effective on writing skills and several cognitive skills among dyslexic children, but future clinical trials are needed to confirm our results.

Effects of transcranial magnetic stimulation of the posterior parietal cortex on saccades and vergence.

Previous studies showed that transcranial magnetic stimulation (TMS) of the posterior parietal cortex (PPC) prolongs the latency of intentional saccades. We examined whether a similar effect exists for reflexive saccades and vergence. To elicit reflexive movements, a gap paradigm was used; lateral saccades and vergence along the median plane were interleaved. TMS was applied on the right PPC 80 ms after target onset. Blocks without TMS were performed and a control experiment with TMS over the primary motor cortex. The latter had no effect on the latency of any type of movements. In contrast, stimulation of the PPC increased the latency of both saccades and vergence, suggesting that the PPC is involved in the triggering of reflexive movements both in direction and in depth.

Immediate saccade amplitude disconjugacy induced by unequal images.

We tested the ability of normal subjects to make changes in the conjugacy of their saccades. Subjects dichoptically viewed a grid the size of which was 10% larger in one eye. The grids were centred onto a flat screen at 57 cm or 1 m from the subject. Horizontal saccades immediately became larger in the eye viewing the larger grid. For some subjects this disconjugacy persisted even under subsequent monocular viewing. Such persistent changes occurred mainly in the field where the required disconjugacy was divergent for centrifugal saccades, convergent for centripetal saccades. Vertical saccades also developed compensatory disconjugacy; its amplitude was smaller but less variable. To explain these results we propose a fast associative learning mechanism that pairs peripheral disparity with saccades and is capable of producing saccade disconjugacy even in the absence of disparity. For horizontal saccades a secondary conditioning of monocular depth cues by the disparity would also be involved.

Disconjugate adaptation of the vertical oculomotor system.

Conjugate post-saccadic eye drift can be induced in normal humans if a visual pattern is made to drift after every saccade. This study examines the ability of normal humans to create disconjugate vertical post-saccadic drift. Identical fuseable patterns were presented dichoptically, one to each eye. At the end of each vertical saccade one pattern drifted up and the other down, by 5% of the saccade amplitude. Five subjects were trained for 2-3 hr. Eye movements were recorded with eye coils. Normal vertical saccades along the midline were remarkably conjugate and post-saccadic drift was minimal. Training produced only small disconjugate post-saccadic drift (0.14 deg) but substantial saccade amplitude disconjugacy (0.70 deg). For several subjects, the induced disconjugacies persisted even for saccades in the dark indicating that adaptive changes occurred in the binocular coordination of vertical saccades. Apparently vertical disparate post-saccadic retinal slip is not sufficient to stimulate significantly the saccade pulse-step matching mechanism which is believed to control post-saccadic eye drift. The changes we observed aimed to reduce position disparity and not retinal slip in each eye.

Disconjugate oculomotor learning caused by feeble image-size inequality: differences between secondary and tertiary positions.

In order to examine the minimum value of image-size inequality capable of inducing lasting disconjugacy of the amplitude of saccades, six normal emmetropic subjects were exposed for 16 min to 2% image size inequality. Subjects were seated at 1 m in front of a screen where a random-dot pattern was projected and made saccades of 7.5 and 15 deg along the horizontal and vertical principal meridians and to tertiary positions in the upper and lower field. During the training period, compensatory disconjugacy of the amplitude of the saccades occurred for the principal horizontal and vertical meridians; such increased disconjugacy persisted after training, suggesting learning. In contrast, for horizontal saccades to or from tertiary positions made in the upper and lower field, no consistent changes in the disconjugacy occurred, either during training or after the training condition. In an additional experiment, three subjects read sequences of words with the 2% magnifier in front of their dominant eye: in such a task, horizontal saccades to or from tertiary positions at the upper or lower field showed appropriate and lasting disconjugacy for two of the three subjects. We conclude that even a 2% image size inequality stimulates oculomotor learning, leading to persistent disconjugacy of saccades. The small disparity created by the image-size inequality is thus compensated by the oculomotor system rather than tolerated by the sensory system (e.g. by enlarging the Panum's area).

Impairment of the binocular coordination of saccades in strabismus.

To examine the link between binocular vision and binocular coordination of saccades we studied subjects with convergent strabismus since childhood with mild or no amblyopia: three subjects had small squint (< 10 prism D) and preserved peripheral binocular visual function with gross stereopsis; four subjects had larger squint (18-35 prism D) and no detectable stereopsis. A standard paradigm was used to elicit horizontal saccades; binocular recordings were made with the IRIS device. For subjects with small strabismus, saccades were disconjugate (unequal between the two eyes) typically by 1 deg. Subjects with larger strabismus exhibited even larger and more variable disconjugacy (typically 1.8 deg). Post-saccadic eye drift was consistently divergent in subjects with small strabismus and tended to reduce the convergent squint angle. In contrast, in subjects with large strabismus drift was convergent. The impairment of the binocular control of saccades is attributed to the deficiency of disconjugate oculomotor adaptive capabilities necessary to compensate for the natural asymmetries or changes in the two oculomotor plants; such deficiency would be more severe in subjects with large strabismus who have neither central nor peripheral binocular vision.

Deficiency of adaptive control of the binocular coordination of saccades in strabismus.

Disconjugate (different in the two eyes) oculomotor adaptation is driven by the need to maintain binocular vision. Since binocular vision is deficient in strabismus, we wondered whether oculomotor disconjugate adaptive capabilities are deficient in such subjects. We studied eight adult subjects with constant, long-standing convergent strabismus of variable angles (4-30 prism D). No subject had severe amblyopia. Binocular vision was evaluated with stereoacuity tests. Two subjects had peripheral binocular vision and gross stereopsis; two other subjects had abnormal retinal correspondence and abnormal or pseudo gross stereopsis. In the other subjects binocular vision and stereopsis were absent. To stimulate disconjugate changes of saccades, subjects viewed for 20 min an image that was magnified in one eye (aniseikonia). Subjects with residual peripheral binocular vision and even subjects with pseudo or abnormal binocular vision showed disconjugate changes of the binocular coordination of their saccades; these changes reduced the disparity resulting from the aniseikonia. In contrast, for subjects without binocular vision the changes were not correlated with the disparity induced by the aniseikonia. Rather, these changes served to improve fixation of one or the other eye individually.

Fast disconjugate adaptations of saccades in microstrabismic subjects.

In normal subjects, saccade amplitude inequality can be induced almost immediately when the image is made larger for one eye. This disconjugacy allows binocular fusion at the point of regard despite the image size inequality. It persists under subsequent monocular viewing which suggests a fast adaptive mechanism. This study tests whether such disconjugacy can be induced in subjects with microstrabismus who do not have foveal fusion. Three microstrabismic subjects viewed a random dot pattern the size of which was 10% larger in one eye. Within 40 sec horizontal saccades became larger in the eye viewing the larger image by 4-10%; the induced disconjugacy persisted under subsequent monocular viewing. Thus, fast disconjugate adaptation is possible in microstrabismus demonstrating that foveal fusion is not necessary to achieve it.

Impairment of saccadic eye movements by scopolamine treatment.

The effects of Scopolamine on the dynamics of saccadic eye movements, stimulated over a random time interval, have been investigated in humans. A 0.5-mg dose of the drug (intramuscular injection) had various influences on the basic saccadic parameters. For all subjects duration increased and peak velocity decreased, while for 50% of the subjects saccades became hypometric and latency increased. Standard deviation increased consistently too. Moreover, the Scopolamine treatment affected postsaccadic fixation; at the end of many saccades, the eye drifted considerably, but stability was recovered after a few seconds.

Disconjugate vertical memory-guided saccades to disparate targets.

We studied the binocular coordination of normal memory-guided saccades and the possibility of inducing memory-based disconjugate learning. First, we report that normal vertical memory-guided saccades to non-disparate targets are yoked vertically in the two eyes as well as visually guided vertical saccades. To induce disconjugate vertical learning, at each trial we flashed a target that was disparate (i.e. 8% more elevated or more depressed for one eye); the memory delay was 1 s. Memory-guided vertical saccades developed a vertical disconjugacy that was appropriate for the disparity of the remembered target. After 15 min of repetition, this vertical disconjugacy persisted even when the target to be remembered was no longer disparate; this indicates disconjugate vertical learning based on short-term memory. However, this was observed only for a few individual cases and its amplitude was small. This contrasts with prior findings on horizontal saccades associated with horizontal disparities. We conclude that vertical memory-based disconjugate learning is possible but very limited. Together with other studies, this study suggests that the natural vertical conjugacy of vertical saccades relies little on rapid learning mechanisms. Rather it seems to be built-in, and this is consistent with earlier electrophysiological findings.

Disconjugate memory-guided saccades to disparate targets: temporal aspects.

Memory-guided saccades to disparate targets (i.e., more eccentric for one eye) flashed 1 s earlier become disconjugate (i.e., of different amplitude for the two eyes) after only about 30 trials. After about 225 trials the disconjugacy persists even when the target to remember is no longer disparate. This suggests fast learning based on short-term memorization of disparity. Learning, however, fails to occur if during the training the memory delay for each trial is increased to 2 s. The purpose of the present study was to test the importance of the frequency of stimulus presentation and thereby the rate of saccades. The same memory-guided saccade paradigm was used as in the prior study and a short training period of 225 trials was applied. For each training trial, the memory delay was again 2 s, but the time allocated for fixation of the central dot and the time allocated for fixation of the remembered target in the dark was reduced to increase the frequency of saccades made. Saccades became rapidly disconjugate and their disconjugacy was retained in a subsequent neutral condition using non-disparate targets. These findings indicate that stimulus frequency and thereby saccade frequency is important for disconjugate oculomotor learning based on disparity memorization. Nevertheless, additional experiments using longer memory delays of 3 s or 4 s show a definite failure of memorization and disconjugate learning.

Motor execution is necessary to memorize disparity.

Binocular saccades in response to briefly flashed, memorized disparate targets (different for the two eyes) become disconjugate following repeated trials. After 15 min of such training, the disconjugacy persists, even when the target to memorize is no longer disparate. This study examines the hypothesis that disparity memorization has a motor basis. We report here three experiments in which subjects were trained for 15-min periods. In experiment 1, subjects made no saccade after target presentation (static training); in experiment 2 subjects intended to make a saccade, but they actually made a saccade in only 10% or 20% of the trials; in experiment 3 subjects made anti-saccades. For all three experiments, the flashed target was disparate and the memory delay for each trial was 1 s. To examine the effects of learning for all three experiments, before and after training, we recorded memory-guided saccades to non-disparate targets (monocular viewing). Experiments 1 and 2 produced inconsistent (before/after training) changes in the disconjugacy of saccades. Thus, the disparity of potential saccade targets had no lasting effect on the disconjugacy of saccades if a saccade was not made. In contrast, the anti-saccades in experiment 3 developed a disconjugacy opposite to the disparity of the remembered target. These findings indicate that the execution of the saccade is necessary to memorize disparity of the target.

Vertical memory-based disconjugate learning for downward saccades at a viewing distance of 70 cm: relation to horizontal vergence and to vertical phoria.

The goal of this study was to examine vertical disconjugate learning based on memorization of vertical disparity at a viewing distance of 70 cm; such a distance is common in many visual ergonomic conditions, including car driving. For a period of 15 min, eight subjects made downward saccades to a memorized target. The target was rendered disparate with the use of a magnifier placed in front of one eye. Learning occurred in only four of the subjects: saccades became disconjugate and the disconjugacy was retained when the target was not disparate. These observations extend a prior study dealing with a longer distance (1 m) and indicate that such learning is subject dependent for both viewing distances. Importantly, the present study shows, for the first time, that vertical disconjugate learning is related to two other phenomena: (a) the horizontal vergence present during vertical saccades and (b) the degree of vertical phoria normal subjects exhibit.

Disconjugate memory-guided saccades to disparate targets: evidence for 3D sensitivity.

The saccadic system has been traditionally regarded as two-dimensional (horizontal, vertical) and basically conjugate in the two eyes. However, saccades to disparate targets (e.g., targets in real three-dimensional space that are located in different directions and at different distances) are naturally disconjugate. We report here that memory-guided saccades to a disparate target flashed 1 s earlier become disconjugate following repeated trials. After 15 min of repetition, the disconjugacy persists even when the target to be remembered is no longer disparate. This suggests fast memory-based learning. Learning, however, fails to occur if, during the repetition trials, the memory delay is 2 s. These findings suggest that the saccadic system has access to a 3D representation of targets and is gifted with 3D short-term memory and learning capacity.