Assessment of binocular fixational eye movements including cyclotorsion with split-field binocular scanning laser ophthalmoscopy.

Fixational eye movements are a hallmark of human gaze behavior, yet little is known about how they interact between fellow eyes. Here, we designed, built and validated a split-field binocular scanning laser ophthalmoscope to record high-resolution eye motion traces from both eyes of six observers during fixation in different binocular vergence conditions. In addition to microsaccades and drift, torsional eye motion could be extracted, with a spatial measurement error of less than 1 arcmin. Microsaccades were strongly coupled between fellow eyes under all conditions. No monocular microsaccade occurred and no significant delay between microsaccade onsets across fellow eyes could be detected. Cyclotorsion was also firmly coupled between both eyes, occurring typically in conjugacy, with gradual changes during drift and abrupt changes during saccades.

Binocular coordination in response to two-dimensional, three-dimensional and stereoscopic visual stimuli.

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.

Do standard optometric measures predict binocular coordination during reading?

In reading, binocular eye movements are required for optimal visual processing and thus, in case of asthenopia or reading problems, standard orthoptic and optometric routines check individual binocular vision by a variety of tests. The present study therefore examines the predictive value of such standard measures of heterophoria, accommodative and vergence facility, AC/A-ratio, NPC and symptoms for binocular coordination parameters during read-ing. Binocular eye movements were recorded (EyeLink II) for 65 volunteers during a typical reading task and linear regression analyses related all parameters of binocular coordination to all above-mentioned optometric measures: while saccade disconjugacy was weakly pre-dicted by vergence facility (15% explained variance), vergence facility, AC/A and symp-toms scores predicted vergence drift (31%). Heterophoria, vergence facility and NPC ex-plained 31% of fixation disparity and first fixation duration showed minor relations to symp-toms (18%). In sum, we found only weak to moderate relationships, with expected, selective associations: dynamic parameter related to optometric tests addressing vergence dynamics, whereas the static parameter (fixation disparity) related mainly to heterophoria. Most sur-prisingly, symptoms were only loosely related to vergence drift and fixation duration, re-flecting associations to a dynamic aspect of binocular eye movements in reading and poten-tially non-specific, overall but slight reading deficiency. Thus, the efficiency of optometric tests to predict binocular coordination during reading was low - questioning a simple, straightforward extrapolation of such test results to an overlearned, complex task.

Objective vs subjective measures of fixation disparity for short and long fixation periods.

PURPOSE: Fixation disparity, i.e. the vergence error for stationary fusion stimuli, can be measured objectively with eye trackers and subjectively with nonius lines. Between these two measures, previous studies found differences that tended to be proportional to the amount of forced vergence, i.e. the discrepancy between vergence and accommodative stimulus. We investigate whether objective and subjective fixation disparity might be similar without forced vergence. METHOD: We simultaneously measured fixation disparity with the EyeLink II system and with flashed dichoptic nonius lines in 17 subjects who observed targets at a vergence stimulus of 6 deg in an haploscope with 60 cm viewing distance. RESULTS: We found individual differences in objective fixation disparity in a range of about 20 (eso) to -60 (exo) min arc which was considerably larger than the range of subjective fixation disparity. Results were similar for long fixation periods (about 15 s) and short fixation periods (about 1.5 s) between 5 deg saccadic gaze shifts. Further, objective fixation disparity was correlated with objective heterophoria, i.e. the vergence state without a fusion stimulus (r = 0.8, p < 0.001). CONCLUSION: Subjective fixation disparity explained only about 25% of the inter-individual variability in objective fixation disparity. The discrepancy between these two measures might be explained by sensory shifts in retinal correspondence, also in the present condition without forced vergence.

Periodic letter strokes within a word affect fixation disparity during reading.

We investigated the way in which binocular coordination in reading is affected by the spatial structure of text. Vergence eye movements were measured (EyeLink II) in 32 observers while they read 120 single German sentences (Potsdam Sentence Corpus) silently for comprehension. The similarity in shape between the neighboring strokes of component letters, as measured by the first peak in the horizontal auto-correlation of the images of the words, was found to be associated with (i) a smaller minimum fixation disparity (i.e. vergence error) during fixation; (ii) a longer time to reach this minimum disparity and (iii) a longer overall fixation duration. The results were obtained only for binocular reading: no effects of auto-correlation could be observed for monocular reading. The findings help to explain the longer reading times reported for words and fonts with high auto-correlation and may also begin to provide a causal link between poor binocular control and reading difficulties.

Binocular advantages in reading revisited: attenuating effects of individual horizontal heterophoria.

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.

Relation between fixation disparity and the asymmetry between convergent and divergent disparity step responses.

The neural network model of Patel et al. [Patel, S. S., Jiang, B. C., & Ogmen, H. (2001). Vergence dynamics predict fixation disparity. Neural Computation, 13(7), 1495-1525] predicts that fixation disparity, the vergence error for a stationary fusion stimulus, is the result of asymmetrical dynamic properties of disparity vergence mechanisms: faster (slower) convergent than divergent responses give rise to an eso (exo) fixation disparity, i.e., over-convergence (under-convergence) in stationary fixation. This hypothesis was tested in the present study with an inter-individual approach: in 16 subjects we estimated the vergence step response to a 1deg disparity stimulus with a subjective nonius procedure. Dichoptic nonius lines were flashed for 100ms with various amounts of delay after the disparity step stimulus (0, 100, 200, 300, 400, and 1000ms). Measured fixation disparity was significantly correlated with the prediction of Patel et al. (2001) based on the asymmetry in convergent and divergent vergence velocity (r=.7, n=14), which explained about 50% (r(2)) of the inter-individual variability in fixation disparity. All subjects with an exo fixation disparity (i.e., static under-convergence) had a weaker dynamic response for convergent than for divergent step stimuli. This confirms a relation between static vergence and asymmetric dynamic vergence, which both are idiosyncratic vergence parameters.

Ocular accommodation and cognitive demand: an additional indicator besides pupil size and cardiovascular measures?

BACKGROUND: The aim of the present study was to assess accommodation as a possible indicator of changes in the autonomic balance caused by altered cognitive demand. Accounting for accommodative responses from a human factors perspective may be motivated by the interest of designing virtual image displays or by establishing an autonomic indicator that allows for remote measurement at the human eye. Heart period, pulse transit time, and the pupillary response were considered as reference for possible closed-loop accommodative effects. Cognitive demand was varied by presenting monocularly numbers at a viewing distance of 5 D (20 cm) which had to be read, added or multiplied; further, letters were presented in a "n-back" task. RESULTS: Cardiovascular parameters and pupil size indicated a change in autonomic balance, while error rates and reaction time confirmed the increased cognitive demand during task processing. An observed decrease in accommodation could not be attributed to the cognitive demand itself for two reasons: (1) the cognitive demand induced a shift in gaze direction which, for methodological reasons, accounted for a substantial part of the observed accommodative changes. (2) Remaining effects disappeared when the correctness of task processing was taken into account. CONCLUSION: Although the expectation of accommodation as possible autonomic indicator of cognitive demand was not confirmed, the present results are informative for the field of applied psychophysiology noting that it seems not to be worthwhile to include closed-loop accommodation in future studies. From a human factors perspective, expected changes of accommodation due to cognitive demand are of minor importance for design specifications - of, for example, complex visual displays.

Binocular advantages for parafoveal processing in reading.

During reading, binocular visual input results in superior performance and is particularly important in the pre-processing of parafoveal text prior to direct fixation. It is not yet clear whether binocular vision in the parafovea is necessary for accurate saccadic targeting, or for efficient pre-processing of upcoming text, prior to direct fixation. In the present sentence reading experiment, we used a dichoptic gaze-contingent moving window paradigm in order to establish 1) how much parafoveal binocular input is necessary for fluent reading and 2) which aspect of parafoveal processing is more reliant on binocular vision. Eye movement measures revealed that reading was disrupted unless word N + 1 was entirely binocular in the parafovea, though no additional benefit was observed when word N + 2 was also binocular. Additionally, while fixation durations and reading times were clearly affected by the manipulation, similarly pronounced changes in binocular saccadic parameters such as accuracy, speed, amplitude and velocity were not observed. We concluded that the disruption to reading caused by presenting monocular text to the right of fixation cannot be attributed to difficulties in targeting binocular saccacdes, but instead results from a decreased efficiency in the pre-processing of parafoveal text. These results provide further demonstration for the importance of binocular vision during written text processing.

Does text contrast mediate binocular advantages in reading?

Humans typically make use of both of their eyes in reading and efficient processes of binocular vision provide a stable, single percept of the text. Binocular reading also comes with an advantage: reading speed is high and word frequency effects (i.e., faster lexical processing of words that are more often encountered in a language) emerge during fixations, which is not the case for monocular reading (Jainta, Blythe, & Liversedge, 2014). A potential contributor to this benefit is the reduced contrast in monocular reading: reduced text contrasts in binocular reading are known to slow down reading and word identification (Reingold & Rayner, 2006). To investigate whether contrast reduction mediates the binocular advantage, we first replicated increased reading time and nullified frequency effects for monocular reading (Experiment 1). Next, we reduced the contrast for binocular but whole sentences to 70% (Weber-contrast); this reading condition resembled monocular reading, but found no effect on reading speed and word identification (Experiment 2). A reasonable conclusion, therefore, was that a reduction in contrast is not the (primary) factor that mediates less efficient lexical processing under monocular reading. In a third experiment (Experiment 3) we reduced the sentence contrast to 40% and the pattern of results showed that, globally, reading was slowed down but clear word frequency effects were present in the data. Thus, word identification processes during reading (i.e., the word frequency effect) were qualitatively different in monocular reading compared with effects observed when text was read with substantially reduced contrast. (PsycINFO Database Record

Using a dichoptic moving window presentation technique to investigate binocular advantages during reading.

Reading comes with a clear binocular advantage, expressed in shorter fixation times and fewer regressions in binocular relative to monocular visual presentations. Little is known, however, about whether the cost associated with monocular viewing derives primarily from the encoding of foveal information or in obtaining a preview benefit from upcoming parafoveal text. In the present sentence reading eye tracking experiment, the authors used a novel dichoptic binocular gaze-contingent moving window technique to selectively manipulate the amount of text made available to the reader both binocularly and monocularly in the fovea and parafovea on a fixation-by-fixation basis. This technique allowed the authors to quantify disruption to reading caused by prevention of binocular fusion during direct fixation of words and parafoveal preprocessing of upcoming text. Sentences were presented (a) binocularly; (b) monocularly; (c) with monocular text to the left of fixation; (d) with monocular text to the right of fixation; or (e) with all words other than the fixated word presented binocularly. A robust binocular advantage occurred for average fixation duration and regressions. Also, while there was a limited cost associated with monocular foveal processing, the restriction of parafoveal processing to monocular information was particularly disruptive. The findings demonstrate the critical importance of a unified binocular input for the efficient preprocessing text to the right of fixation. (PsycINFO Database Record

Capture of visual direction in dynamic vergence is reduced with flashed monocular lines.

The visual direction of a continuously presented monocular object is captured by the visual direction of a closely adjacent binocular object, which questions the reliability of nonius lines for measuring vergence. This was shown by Erkelens, C. J., and van Ee, R. (1997a,b) [Capture of the visual direction: An unexpected phenomenon in binocular vision. Vision Research, 37, 1193-1196; Capture of the visual direction of monocular objects by adjacent binocular objects. Vision Research, 37, 1735-1745] stimulating dynamic vergence by a counter phase oscillation of two square random-dot patterns (one to each eye) that contained a smaller central dot-free gap (of variable width) with a vertical monocular line oscillating in phase with the random-dot pattern of the respective eye; subjects adjusted the motion-amplitude of the line until it was perceived as (nearly) stationary. With a continuously presented monocular line, we replicated capture of visual direction provided the dot-free gap was narrow: the adjusted motion-amplitude of the line was similar as the motion-amplitude of the random-dot pattern, although large vergence errors occurred. However, when we flashed the line for 67 ms at the moments of maximal and minimal disparity of the vergence stimulus, we found that the adjusted motion-amplitude of the line was smaller; thus, the capture effect appeared to be reduced with flashed nonius lines. Accordingly, we found that the objectively measured vergence gain was significantly correlated (r=0.8) with the motion-amplitude of the flashed monocular line when the separation between the line and the fusion contour was at least 32 min arc. In conclusion, if one wishes to estimate the dynamic vergence response with psychophysical methods, effects of capture of visual direction can be reduced by using flashed nonius lines.

Binocular advantages in reading.

Reading, an essential skill for successful function in today's society, is a complex psychological process involving vision, memory, and language comprehension. Variability in fixation durations during reading reflects the ease of text comprehension, and increased word frequency results in reduced fixation times. Critically, readers not only process the fixated foveal word but also preprocess the parafoveal word to its right, thereby facilitating subsequent foveal processing. Typically, text is presented binocularly, and the oculomotor control system precisely coordinates the two frontally positioned eyes online. Binocular, compared to monocular, visual processing typically leads to superior performance, termed the "binocular advantage"; few studies have investigated the binocular advantage in reading. We used saccade-contingent display change methodology to demonstrate the benefit of binocular relative to monocular text presentation for both parafoveal and foveal lexical processing during reading. Our results demonstrate that denial of a unified visual signal derived from binocular inputs provides a cost to the efficiency of reading, particularly in relation to high-frequency words. Our findings fit neatly with current computational models of eye movement control during reading, wherein successful word identification is a primary determinant of saccade initiation.

Individual differences in binocular coordination are uncovered by directly comparing monocular and binocular reading conditions.

PURPOSE: We evaluated systematically binocular coordination during a reading task by comparing binocular and monocular reading, and considering the potential effects of individual heterophoria and eye dominance. METHODS: A total of 13 participants (aged 19-29 years, refractive errors -0.5 to 0.125 diopters [D]) read single sentences in a haploscope while eye movements were measured with an EyeLinkII eyetracker. RESULTS: When reading monocularly, saccade amplitudes increased by 0.04 degrees and first fixation durations became longer by approximately 10 ms. Furthermore, saccade disconjugacies increased, and compensatory vergence drifts during fixation turned into a divergent drift relative to the viewing distance. The vergence angle adjusted for the actual viewing distance became less convergent during monocular reading by 0.5 degrees. Moreover, in participants who were almost orthophoric, only the first fixation duration became longer (by 20 ms) when the reading conditions changed from binocular to monocular. For exophoric participants, all parameters of binocular coordination changed, and first fixation duration decreased by 20 ms. When reading monocularly, no differences between the dominant right eye and the nondominant left eye were found. CONCLUSIONS: Because of obvious differences in binocular coordination between monocular and binocular reading, some vergence adjustments are driven actively by fusional processes. Furthermore, higher demands on these binocular fusional processes can be uncovered only by a detailed evaluation of monocular reading conditions.

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.

Dyslexic children are confronted with unstable binocular fixation while reading.

Reading requires three-dimensional motor control: saccades bring the eyes from left to right, fixating word after word; and oblique saccades bring the eyes to the next line of the text. The angle of vergence of the two optic axes should be adjusted to the depth of the book or screen and--most importantly--should be maintained in a sustained manner during saccades and fixations. Maintenance of vergence is important as it is a prerequisite for a single clear image of each word to be projected onto the fovea of the eyes. Deficits in the binocular control of saccades and of vergence in dyslexics have been reported previously but only for tasks using single targets. This study examines saccades and vergence control during real text reading. Thirteen dyslexic and seven non-dyslexic children read the French text "L'Allouette" in two viewing distances (40 cm vs. 100 cm), while binocular eye movements were measured with the Chronos Eye-tracking system. We found that the binocular yoking of reading saccades was poor in dyslexic children (relative to non-dyslexics) resulting in vergence errors; their disconjugate drift during fixations was not correlated with the disconjugacy during their saccades, causing considerable variability of vergence angle from fixation to fixation. Due to such poor oculomotor adjustments during reading, the overall fixation disparity was larger for dyslexic children, putting larger demand on their sensory fusion processes. Moreover, for dyslexics the standard deviation of fixation disparity was larger particularly when reading at near distance. We conclude that besides documented phoneme processing disorders, visual/ocular motor imperfections may exist in dyslexics that lead to fixation instability and thus, to instability of the letters or words during reading; such instability may perturb fusional processes and might--in part--complicate letter/word identification.

Subjective fixation disparity affected by dynamic asymmetry, resting vergence, and nonius bias.

PURPOSE: This study was undertaken to investigate how subjectively measured fixation disparity can be explained by (1) the convergent-divergent asymmetry of vergence dynamics (called dynamic asymmetry) for a disparity vergence step stimulus of 1° (60 arc min), (2) the dark vergence, and (3) the nonius bias. METHODS: Fixation disparity, dark vergence, and nonius bias were measured subjectively using nonius lines. Dynamic vergence step responses (both convergent and divergent) were measured objectively. RESULTS: In 20 subjects (mean age, 24.5 ± 4.3 years, visual acuity, ≥1.0; all emmetropic except for one with myopia, wearing contact lenses), multiple regression analyses showed that 39% of the variance in subjective fixation disparity was due to the characteristic factors of physiological vergence: dynamic asymmetry (calculated from convergent and divergent velocities), and dark vergence. An additional 23% of variance was due to the subjective nonius bias (i.e., the physical nonius offset required for perceived alignment of binocularly [nondichoptically] presented nonius lines). Together, these factors explained 62% of the interindividual differences in subjectively measured fixation disparity, demonstrating the influence of oculomotor and perceptual factors. CONCLUSIONS: Clinically relevant subjective fixation disparity originates from distinct physiological sources. Dynamic asymmetry in vergence dynamics, resting vergence, and nonius bias were found to affect fixation disparity directly, not only via changes in vergence dynamics.

Binocular coordination during reading of blurred and nonblurred text.

PURPOSE: Reading a text requires vergence angle adjustments, so that the images in the two eyes fall on corresponding retinal areas. Vergence adjustments bring the two retinal images into Panum's fusional area and therefore, small remaining errors or regulations do not lead to double vision. The present study evaluated dynamic and static aspects of the binocular coordination when upcoming text was blurred. METHODS: Binocular eye movements and accommodation responses were simultaneously measured for 20 participants while reading single, nonblurred sentences and while the text was blurred as if it were seen by a person in whom the combination of refraction and accommodation deviated from the stimulus plane by 0.5 D. RESULTS: Text comprehension did not change, even though fixation times increased for reading blurred sentences. The disconjugacy during saccades was also not affected by blurred text presentations, but the vergence adjustment during fixations was reduced. Further, for blurred text, the overall vergence angle shifted in the exo direction, and this shift correlated with the individual heterophoria. Accommodation measures showed that the lag of accommodation was slightly larger for reading blurred sentences and that the shift in vergence angle was larger when the individual lag of accommodation was also larger. CONCLUSIONS: The results suggest that reading comprehension is robust against changes in binocular coordination that result from moderate text degradation; nevertheless, these changes are likely to be linked to the development of fatigue and visual strain in near reading conditions.

The Pupil Reflects Motor Preparation for Saccades - Even before the Eye Starts to Move.

The eye produces saccadic eye movements whose reaction times are perhaps the shortest in humans. Saccade latencies reflect ongoing cortical processing and, generally, shorter latencies are supposed to reflect advanced motor preparation. The dilation of the eye's pupil is reported to reflect cortical processing as well. Eight participants made saccades in a gap and overlap paradigm (in pure and mixed blocks), which we used in order to produce a variety of different saccade latencies. Saccades and pupil size were measured with the EyeLink II. The pattern in pupil dilation resembled that of a gap effect: for gap blocks, pupil dilations were larger compared to overlap blocks; mixing gap and overlap trials reduced the pupil dilation for gap trials thereby inducing a switching cost. Furthermore, saccade latencies across all tasks predicted the magnitude of pupil dilations post hoc: the longer the saccade latency the smaller the pupil dilation before the eye actually began to move. In accordance with observations for manual responses, we conclude that pupil dilations prior to saccade execution reflect advanced motor preparations and therefore provide valid indicator qualities for ongoing cortical processes.

Changes in vergence dynamics due to repetition.

Vergence insufficiency is frequent in many populations including children with vertigo in the absence of measurable vestibular dysfunction. Orthoptic exercises are typically used to improve vergence and the clinical practice suggests that simple repetition of vergence movements improves it. Objective eye movement recordings were used to asses the dynamics and spatial-temporal properties of convergence (8.7°) and divergence (2.7°) along the midline while these movements were repeated 80 times. Eight children, aged on average 13years and showing vertigo symptoms accompanied with vergence insufficiency, participated. For both, convergence and divergence the velocity increased and the overall duration decreased; the amplitude of the mean transient component of the response changed significantly. These findings are compatible with models of double mode control of vergence eye movements (transient - open-loop vs. sustained - closed loop). Due to simple repetitions a real improvement in the dynamics of vergence along the midline occurred.