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Given the increased evidence suggesting the presence of binocular coordination deficits in dyslexia, investigations of binocular eye movements are beneficial to clarify the underlying causes of reading difficulties. This systematic review aims to (a) synthesize the literature through the examination of binocular coordination in children with dyslexia by describing the normative development of stable binocular control and (b) outline future directions. Boolean expressions in the PubMed search were used to define papers. Following a literature search and selection process, 25 papers were included. Studies using binocular eye tracking during linguistic and nonlinguistic tasks in children with dyslexia and typical development 5-17 years of age are reviewed. The studies reviewed provided consistent evidence of poor binocular coordination in children with dyslexia, but the results associated with different task characteristics were less consistent. The relation between binocular coordination deficits and reading difficulties needs to be further elucidated in longitudinal studies which may provide future treatments targeting the binocular viewing system in dyslexia., (© 2022. The Author(s), under exclusive licence to The International Dyslexia Association.)

The development of high magnification retinal imaging has brought with it the ability to track eye motion with a precision of less than an arc minute. Previously these systems have provided only monocular records. Here we describe a modification to the Tracking Scanning Laser Ophthalmoscope (Sheehy et al., 2012) that splits the optical path in a way that slows the left and right retinas to be scanned almost simultaneously by a single system. A mirror placed at a retinal conjugate point redirects half of each horizontal scan line to the fellow eye. The collected video is a split image with left and right retinas appearing side by side in each frame. Analysis of the retinal motion in the recorded video provides an eye movement trace with very high temporal and spatial resolution. Results are presented from scans of subjects with normal ocular motility that fixated steadily on a green laser dot. The retinas were scanned at 4° eccentricity with a 2° square field. Eye position was extracted offline from recorded videos with an FFT based image analysis program written in Matlab. The noise level of the tracking was estimated to range from 0.25 to 0.5arcmin SD for three subjects. In the binocular recordings, the left eye/right eye difference was 1-2arcmin SD for vertical motion and 10-15arcmin SD for horizontal motion, in agreement with published values from other tracking techniques., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Knowledge of cognitive and neural architecture and processes that control eye movements has advanced enough to allow precise and quantitative analysis of hitherto unsolved phenomena. In this review, we revisit from a neuropsychological viewpoint Hering vs. Helmholtz' hypotheses on binocular coordination. Specifically, we reexamine the behavior and the neural bases of saccade-vergence movement, to move the gaze in both direction and depth under natural conditions. From the psychophysical viewpoint, neo-Heringian and neo-Helmholtzian authors have accumulated arguments favoring distinct conjugate (for saccades) and disconjugate (for vergence) systems, as well as advocating for monocularly programmed eye movements. From the neurophysiological viewpoint, which reports brain cell recordings during the execution of a given task, neo-Heringian and neo-Helmholtzian physiologists have also provided arguments in favor of both hypotheses at the level of the brainstem premotor circuitry. Bridging the two, we propose that Hering and Helmholtz were both right. The emphasis placed by the latter on adaptive processes throughout life cycle is compatible with the importance of neurobiological constraints pointed out by the former. In the meanwhile, the study of saccade-vergence eye movements recalls how much the psychophysical definition of the task determines the interpretation that is made from neurophysiological data., (Copyright © 2014 Elsevier Masson SAS. All rights reserved.)

Reading with two eyes necessitates efficient processes of binocular vision, which provide a single percept of the text. These processes come with a binocular advantage: binocular reading shows shorter average fixation durations and sentence reading times when compared to monocular reading. A couple of years ago, we showed for a small sample (N=13) that binocular advantages critically relate to the individual heterophoria (the resting state of vergence). In the present, large-scale replication we collected binocular eye movements (Eyelink II) for 94 participants who read 20 sentences monocularly and 20 sentences binocularly. Further, individual heterophorias were determined using three different optometric standards: objective eye tracking (EyeLink II at 60 cm), Maddox wing test (at 30 cm) and measures following the "Guidelines for the application of the Measuring and Correcting Methodology after H.-J. Haase" (MCH; at 6 m). Binocular eye movements showed typical pattern and we replicated (1) binocular advantages of about 25 ms for average fixation durations and (2) a reduction in binocular advantages when heterophoria increased - but only when heterophoria was identified by EyeLink II or Maddox wing measures; MCH measures of heterophoria did not affect binocular advantages in reading. For large heterophorias binocular reading even turned into a disadvantage. Implications for effect estimations and optometric testing will be discussed. [ABSTRACT FROM AUTHOR]

Humans have two, frontally placed eyes and during reading oculomotor and sensory processes are needed to combine the two inputs into a unified percept of the text. Generally, slight vergence errors, i.e., fixation disparities, occur but do not cause double vision since disparate retinal inputs fall into Panum’s fusional area, that is, a range of disparity wherein sensory fusion of the two retinal images is achieved. In this study, we report benchmark data with respect to the mean magnitude and range of vertical compared to horizontal fixation disparities for natural reading. Our data clearly fit to an elliptical pattern of Panum’s fusional area that corresponds with theoretical estimates. Furthermore, when we examined disparity-driven vergence adjustments during fixations by comparing monocular with binocular reading conditions, we found that only horizontal fixation disparities increased significantly under conditions of monocular stimulation. Also, no significant vertical fine-tuning (vergence adjustment) was observed for vergence eye movements during reading fixations. Thus, horizontal and vertical fixation disparities and vergence adjustments during reading showed quite different characteristics, and this dissociation is directly related to the functional role of vergence adjustments: vertical fusion – and vertical vergence – subserve the maintenance of a single percept and stereopsis by keeping the eyes in register and allowing for horizontal fusional processes to successfully operate over a vertically aligned input. A reliable and stable vertical alignment is, thus, a pre-requisite over which horizontal fusional responses (and depth perception) can work most efficiently – even in a task like reading. [ABSTRACT FROM AUTHOR]

Among the eye movements during fixation, the function of small saccades occuring quite commonly at fixation is still unclear. It has been reported that a substantial number of these microsaccades seem to occur in only one of the eyes. The aim of the present study is to investigate microsaccades in monocular stimulation conditions. Although this is an artificial test condition which does not occur in natural vision, this monocular presentation paradigm allows for a critical test of a presumptive monocular mechanism of saccade generation. Results in these conditions can be compared with the normal binocular stimulation mode. We checked the statistical properties of microsaccades under monocular stimulation conditions and found no indication for specific interactions for monocularly detected small saccades, which might be present if they were based on a monocular physiological activation mechanism.

Neuropsychology examines the relationship between cognitive activity and corresponding cerebral conditions. At one end, psychophysics meticulously describes the details of behavior. At the other, physiology records brain cell activity during cognitive tasks. Bridging the two, neuropsychology establishes the neural correlate of behaviour when correlation methods are used, and extends to the critical neural substrate when a causal relationship can be established. Here we revisit the Hering-versus-Helmholtz controversy on binocular coordination from the psychophysician's description of combined saccade-vergence eye movements to the neurophysiological recording of motor and premotor neurons of the oculomotor neural circuitry. Whilst neo-Heringian psychophysicians and physiologists have accumulated arguments for separate saccade and vergence systems, at both the behavioral and the neural premotor levels, neo-Helmholtzians have also provided evidence for monocular programmed eye movements and commands at the premotor level. Bridging the two, we conclude that Hering and Helmholtz were both right. Importantly, the latter's viewpoint brings to the fore the importance of adaptive processes throughout life, in view of the neurobiological constraints emphasized by the former. [ABSTRACT FROM AUTHOR]

Previous studies examining binocular coordination during reading have reported conflicting results in terms of the nature of disparity (e.g. Kliegl, Nuthmann, & Engbert (Journal of Experimental Psychology General 135:12-35, ); Liversedge, White, Findlay, & Rayner (Vision Research 46:2363-2374, ). One potential cause of this inconsistency is differences in acquisition devices and associated analysis technologies. We tested this by directly comparing binocular eye movement recordings made using SR Research EyeLink 1000 and the Fourward Technologies Inc. DPI binocular eye-tracking systems. Participants read sentences or scanned horizontal rows of dot strings; for each participant, half the data were recorded with the EyeLink, and the other half with the DPIs. The viewing conditions in both testing laboratories were set to be very similar. Monocular calibrations were used. The majority of fixations recorded using either system were aligned, although data from the EyeLink system showed greater disparity magnitudes. Critically, for unaligned fixations, the data from both systems showed a majority of uncrossed fixations. These results suggest that variability in previous reports of binocular fixation alignment is attributable to the specific viewing conditions associated with a particular experiment (variables such as luminance and viewing distance), rather than acquisition and analysis software and hardware. [ABSTRACT FROM AUTHOR]

Highlights: [•] While reading a text the saccade amplitude is similar for patients with vergence insufficiency compared to controls children. [•] Also, the duration of the fixations is the same for both groups of children. [•] However patients show poor binocular coordination during and after the saccades. [•] After oculomotor training therapy, an improvement of the binocular coordination during and after the saccades is found. [ABSTRACT FROM AUTHOR]

Citation information: Blythe HI, Holliman NS, Jainta S, Tbaily LW & Liversedge SP. Binocular coordination in response to two-dimensional, three-dimensional and stereoscopic visual stimuli. Ophthalmic Physiol Opt 2012, 32, 397-411. doi:10.1111/j.1475-1313.2012.00926.x Abstract Purpose: We were particularly interested in whether binocular coordination when viewing stereoscopic images would be more comparable to when viewing a 2D representation, or when viewing a real stimulus array in depth. Methods: Data are reported from an experiment examining binocular coordination in response to stereoscopically presented stimuli. Movements of both eyes were recorded as participants viewed LED stimuli in a real scene with depth, a 2D image of the scene, and a stereoscopic image of the scene. Results: When viewing real LEDs, vergence during saccades re-aligned the eyes in depth where necessary, with smaller adjustments during the following fixation. In contrast, when viewing the stereoscopic representation, vergence during saccades did not re-align the eyes in depth. The only effect of target depth on vergence occurred during the following fixation. Conclusions: We conclude that disparity in parafoveal objects, in isolation from other depth cues (and, minimally, conflicting with blur), was insufficient for the visual system to target saccades appropriately in depth. [ABSTRACT FROM AUTHOR]

Abstract: We investigated the effective fusional range for written stimuli in children and adults in a natural viewing situation. We recorded binocular eye movements in children and adults during processing of stereoscopically presented words in a lexical decision task. The effect of disparity magnitude on ease of fusion caused decreased response accuracy, increasing numbers of fixations and increased trial viewing times when retinal disparity exceeded one character space. The data suggest that retinal inputs of a word that are disparate by up to one character (0.37°) fall within the effective fusional range such that lexical decisions are not impaired. [Copyright &y& Elsevier]

Abstract: We examined the influence of a variety of visual factors on binocular coordination during saccadic orienting. Some experimental conditions placed similar demands on the oculomotor system as those that occur during reading, but in the absence of linguistic processing. We examined whether saccade target extent, preceding saccade magnitude, preceding saccade direction, and parafoveal availability of saccade target influenced fixation disparity. Disparities similar in magnitude and frequency to those obtained in previous binocular reading experiments occurred. Saccade magnitude had a robust influence upon fixation disparities. The results are very similar to those obtained in investigations of binocular coordination during reading, and indicate that similar patterns occur during reading-like eye scanning behaviour, in the absence of linguistic processing. [Copyright &y& Elsevier]

Abstract: Disconjugate oculomotor adaptation is driven by the need to maintain binocular vision. Since binocular vision in Duane Retraction Syndrome (DRS) patients is normal in half of their horizontal field of gaze (i.e., sound-side of gaze), we wondered whether oculomotor adaptive capabilities are efficient despite such a severe impairment of eye motility towards the other half of the horizontal field of gaze (i.e., affected-side gaze). We compared properties of horizontal saccades of patients with congenital unilateral Duane Retraction Syndrome type I in binocular viewing and monocular viewing conditions by simultaneously recording both eyes with the search coil technique. Our results show a mismatch between the pulse and the step signal of the innervation for saccades. When tested in the affected eye viewing condition (sound eye covered), the eyes showed not only similarly-directed increases of the saccadic gain (pulse signal) in the two eyes but also disjunctive post-saccadic drifts (step signal). This behavior suggests that visuomotor errors presented only to the affected eye were transferred to the sound eye, producing conjugate changes of the saccadic command. The post-saccadic command remained unchanged, however, and controlled the final position of each eye separately. This suggests that monocular adaptation is possible only for the step of innervation (i.e., controlling the final eye position) but not for the pulse of innervation (i.e., controlling the saccadic gain), even though the peculiarity of unilateral DRS type I offers a clear advantage for separate pathways of control for the two eyes. [Copyright &y& Elsevier]

Abstract: Fine binocular coordination of vertical saccades is a complex process requiring appropriate distribution of innervations to all six extraocular muscles. Loss of such coordination causes vertical binocular disparities that are particularly bothersome. We studied the quality of binocular control of vertical saccades in healthy subjects, 11 young adults (20–28 years) and 11 elderly adults (63–75 years). We used LED targets at 7.5° or 15° from the center (fixation), up or down in four conditions: gap and overlap tasks, each done at two distances—near (40cm) and far (150cm). Vertical eye movements were recorded with video-oculography (CHRONOS). The results showed: aged subjects performed vertical saccades as accurately as young subjects. Importantly, the binocular coordination of vertical saccades was well preserved in the elderly; the mean difference of vertical saccades between the two eyes was 0.10° and 0.09° in young and elderly subjects, respectively. Upward saccades were associated with divergence, downward ones with convergence. This secondary phenomenon was also the same and of the similar amplitude for young (1.30°) and elderly (1.25°) subjects. Thus, despite its complexity, the quality of binocular coordination of vertical saccades remains intact with age. The other observations are mostly dependent of several aspects on the direction (up/down), viewing distances and eccentricities; the horizontal vergence during or after vertical saccades was found to be larger for downward saccades than for upward saccades, for saccades at far distance than at close, and for the more eccentric targets (15° versus 7.5°). All these phenomena are the same for both young and elderly subjects. We conclude that the accuracy and the binocular coordination of vertical saccades, at least for target steps less than 15°, are preserved in elderly subjects <75 years who maintain good physical and intellectual form. The data are consistent with the idea of the existence of non-aging system function in the human CNS. [Copyright &y& Elsevier]

Abstract: Recent evidence indicates that each eye does not always fixate the same letter during reading and there has been some suggestion that processing difficulty may influence binocular coordination. We recorded binocular eye movements from children and adults reading sentences containing a word frequency manipulation. We found disparities of significant magnitude between the two eyes for all participants, with greater disparity magnitudes in children than adults. All participants made fewer crossed than uncrossed fixations. However, children made a higher proportion of crossed fixations than adults. We found no influence of word frequency on children’s fixations and on binocular coordination in adults. [Copyright &y& Elsevier]

Abstract: Binocular coordination of the eyes during reading was examined. Fixation disparity greater than one character occurred on 47% of fixations, with the disparity being predominantly uncrossed (39%), though a small proportion of fixations were crossed. The average magnitude of disparity, measured at the end of fixation, was 1.1 characters for all fixations. For the 47% of non-aligned fixations the average magnitude of disparity was 1.9 characters. Vergence movements that reduced fixation disparity occurred during fixations, and their magnitude was positively correlated with fixation duration. Finally, eye dominance did not modulate fixation disparity magnitude or the proportion of disparate fixations. [Copyright &y& Elsevier]

Abstract: The purpose of the present study was to examine in 7 years old normal children who just learnt to read, saccade and fixation characteristics during reading single words. Eight children were studied and their results were compared to those of eight normal adults doing the same task. For each group word reading data were also compared with data in a task requiring saccades and fixations to target-LEDs. Horizontal saccades from both eyes were recorded with a photoelectric device (Oculometer, Bouis). Latencies of saccades both to words and to LEDs presented at predictable location were similar, and they were also similar between children and adults. In contrast, disconjugacy of saccades was significantly increased for children and similar in the two tasks (LEDs or words). Disconjugate post-saccadic drift and its velocity were also significantly higher in children and similar in the two tasks. Substantial conjugate leftward drift was present for children only, and for the word task only. Finally, fixation duration on words was significantly longer in children than in adults. We conclude that binocular coordination and fixation stability is poor in children and that it could be partially responsible for the long fixation duration. Binocular coordination does not depend on the task (LEDs or words) neither for adults, nor for children; this contrasts prior reports. [Copyright &y& Elsevier]

Stabilization of images on the fovea during either fore/aft translation of a subject or fore/aft movement of a visual target in front of a stationary observer imposes complex geometrical requirements that depend upon the eccentricity of the object of interest with respect to the eyes. Each eye needs to be rotated independently with varying proportions of conjugate (version) and disconjugate (vergence) eye movements to maintain fixation of the target. Here, we describe binocular coordination in the early response to translational movements of normal subjects along their naso-occipital axis. We recorded the responses evoked by small (about 4 cm), abrupt (about 0.7 g), fore/aft translations in four normal subjects while they viewed a near target. In the forward and backward starting positions the target was 15 or 10.5 cm away, respectively. Each subject was tested with the target centered between the eyes, aligned on the right eye, and placed to the right of the right eye by ∼3 cm. The three conditions differed only in the lateral eccentricity of the target, yet the geometrical requirements for image stabilization are very different: pure vergence, one eye still, or mostly version. We found that the eye-movement responses closely matched what was needed for visual stabilization of the target, though responses to stimuli calling for divergence were less accurate than those for convergence. The latency of these responses ranged from 40 to 65 ms and achieved about 80% of the ideal response by 90 to 100 ms after the onset of the stimulus. Next, we asked whether these eye movements were generated by the vestibular system or by high-level strategies for image stabilization, such as pursuit. Thus, in a second set of experiments we used the mean profile of fore\aft body motion computed for each subject to drive a small visual target across the same distances and in the same eccentricities used during body translations. We found that visually driven responses had longer latencies (by at least 80 ms, ranging from 144 to 155 ms) and slower dynamics (with significantly lower peak eye velocities), highlighting the different subsystems producing the two types of responses. Saccades were also an important component of the response to both visual and vestibular stimuli, less frequent during the centered- target configuration and more frequent during viewing of eccentric targets. Visual stimuli evoked saccadic corrections more often and at shorter latencies than did vestibular stimuli. Both smooth and saccadic eye movements were appropriately disconjugate and their pattern depended on whether the eyes were converging or diverging. [ABSTRACT FROM AUTHOR]

We examined three-dimensional binocular positions in the alert and sleepy monkeys. In contrast to the tightly yoked eye movements observed in alertness, the eyes were usually converged, vertically misaligned and had a much larger torsional variability during light sleep. While in alertness eye position vectors were confined to fronto-parallel planes, the corresponding planes were rotated temporally (e.g. leftward for the left eye) in light sleep. There was no correlation between temporal rotation of the eye position planes and horizontal vergence. All these observations can be explained by randomly innervated extraocular muscles that are rotating the two eyes about anatomically determined axes. [Copyright &y& Elsevier]