Eye movement analysis: Reading and moving target pursuit

The design and application of an extensive and general software-based system for the study and analysis of eye movements in human subjects is described. The system can find application in a number of specialties in medicine, particularly clinical neurophysiology, as well as in studies of eye movement dynamics, including reading dynamics, in dyslexia. It is designed to run on the PDP 11 family of computers with standard peripherals and operating under the RT 11 executive.     

Eye Movements Reveal Effects of Visual Content on Eye Guidance and Lexical Access during Reading

Background

Normal reading requires eye guidance and activation of lexical representations so that words in text can be identified accurately. However, little is known about how the visual content of text supports eye guidance and lexical activation, and thereby enables normal reading to take place.

Methods and Findings

To investigate this issue, we investigated eye movement performance when reading sentences displayed as normal and when the spatial frequency content of text was filtered to contain just one of 5 types of visual content: very coarse, coarse, medium, fine, and very fine. The effect of each type of visual content specifically on lexical activation was assessed using a target word of either high or low lexical frequency embedded in each sentence

Results

No type of visual content produced normal eye movement performance but eye movement performance was closest to normal for medium and fine visual content. However, effects of lexical frequency emerged early in the eye movement record for coarse, medium, fine, and very fine visual content, and were observed in total reading times for target words for all types of visual content.

Conclusion

These findings suggest that while the orchestration of multiple scales of visual content is required for normal eye-guidance during reading, a broad range of visual content can activate processes of word identification independently. Implications for understanding the role of visual content in reading are discussed.     

The Relation between Reading Skills and Eye Movement Patterns in Adolescent Readers: Evidence from a Regular Orthography

Over the past decades, the relation between reading skills and eye movement behavior has been well documented in English-speaking cohorts. As English and German differ substantially with regard to orthographic complexity (i.e. grapheme-phoneme correspondence), we aimed to delineate specific characteristics of how reading speed and reading comprehension interact with eye movements in typically developing German-speaking (Austrian) adolescents. Eye movements of 22 participants (14 females; mean age = 13;6 years;months) were tracked while they were performing three tasks, namely silently reading words, texts, and pseudowords. Their reading skills were determined by means of a standardized German reading speed and reading comprehension assessment (Lesegeschwindigkeits- und -verständnistest für Klassen 6−12). We found that (a) reading skills were associated with various eye movement parameters in each of the three reading tasks; (b) better reading skills were associated with an increased efficiency of eye movements, but were primarily linked to spatial reading parameters, such as the number of fixations per word, the total number of saccades and saccadic amplitudes; (c) reading speed was a more reliable predictor for eye movement parameters than reading comprehension; (d) eye movements were highly correlated across reading tasks, which indicates consistent reading performances. Contrary to findings in English-speaking cohorts, the reading skills neither consistently correlated with temporal eye movement parameters nor with the number or percentage of regressions made while performing any of the three reading tasks. These results indicate that, although reading skills are associated with eye movement patterns irrespective of language, the temporal and spatial characteristics of this association may vary with orthographic consistency.     

Eye Movement Patterns in Natural Reading: A Comparison of Monolingual and Bilingual Reading of a Novel

Introduction and Method

This paper presents a corpus of sentence level eye movement parameters for unbalanced bilingual first language (L1) and second-language (L2) reading and monolingual reading of a complete novel (56 000 words). We present important sentence-level basic eye movement parameters of both bilingual and monolingual natural reading extracted from this large data corpus.

Results and Conclusion

Bilingual L2 reading patterns show longer sentence reading times (20%), more fixations (21%), shorter saccades (12%) and less word skipping (4.6%), than L1 reading patterns. Regression rates are the same for L1 and L2 reading. These results could indicate, analogous to a previous simulation with the E-Z reader model in the literature, that it is primarily the speeding up of lexical access that drives both L1 and L2 reading development. Bilingual L1 reading does not differ in any major way from monolingual reading. This contrasts with predictions made by the weaker links account, which predicts a bilingual disadvantage in language processing caused by divided exposure between languages.     

Causal Inference for Spatial Constancy across Saccades

Our ability to interact with the environment hinges on creating a stable visual world despite the continuous changes in retinal input. To achieve visual stability, the brain must distinguish the retinal image shifts caused by eye movements and shifts due to movements of the visual scene. This process appears not to be flawless: during saccades, we often fail to detect whether visual objects remain stable or move, which is called saccadic suppression of displacement (SSD). How does the brain evaluate the memorized information of the presaccadic scene and the actual visual feedback of the postsaccadic visual scene in the computations for visual stability? Using a SSD task, we test how participants localize the presaccadic position of the fixation target, the saccade target or a peripheral non-foveated target that was displaced parallel or orthogonal during a horizontal saccade, and subsequently viewed for three different durations. Results showed different localization errors of the three targets, depending on the viewing time of the postsaccadic stimulus and its spatial separation from the presaccadic location. We modeled the data through a Bayesian causal inference mechanism, in which at the trial level an optimal mixing of two possible strategies, integration vs. separation of the presaccadic memory and the postsaccadic sensory signals, is applied. Fits of this model generally outperformed other plausible decision strategies for producing SSD. Our findings suggest that humans exploit a Bayesian inference process with two causal structures to mediate visual stability.     

Background Speech Effects on Sentence Processing during Reading: An Eye Movement Study

Effects of background speech on reading were examined by playing aloud different types of background speech, while participants read long, syntactically complex and less complex sentences embedded in text. Readers’ eye movement patterns were used to study online sentence comprehension. Effects of background speech were primarily seen in rereading time. In Experiment 1, foreign-language background speech did not disrupt sentence processing. Experiment 2 demonstrated robust disruption in reading as a result of semantically and syntactically anomalous scrambled background speech preserving normal sentence-like intonation. Scrambled speech that was constructed from the text to-be read did not disrupt reading more than scrambled speech constructed from a different, semantically unrelated text. Experiment 3 showed that scrambled speech exacerbated the syntactic complexity effect more than coherent background speech, which also interfered with reading. Experiment 4 demonstrated that both semantically and syntactically anomalous speech produced no more disruption in reading than semantically anomalous but syntactically correct background speech. The pattern of results is best explained by a semantic account that stresses the importance of similarity in semantic processing, but not similarity in semantic content, between the reading task and background speech.     

What We Can Learn about Reading Development from the Analysis of Eye Movements

The paper presents the results of the study on reading mechanisms in children of primary school age performed using eye tracking. The participants were 36 second-grade pupils. Eye movements were registered when reading a specially developed set of sentences containing words with controlled length and frequency. Neuropsychological assessment and reading of words with regular and irregular spelling were also performed. The results confirm the data of reading analysis obtained in other languages and show that characteristics of eye movements during reading depend on the length and frequency of the word. The results indicate a close relationship between the characteristics of the oculomotor activity and the level of the development of reading skills. Analysis of the relationship of eye movements and neuropsychological assessments of the cognitive abilities of children shows that the executive functions and functions for visuospatial information processing are the most important in the second year of reading aquisition. The role of auditory information processing functions requires further investigation.     

Error Correcting Mechanisms during Antisaccades: Contribution of Online Control during Primary Saccades and Offline Control via Secondary Saccades

Errors in eye movements can be corrected during the ongoing saccade through in-flight modifications (i.e., online control), or by programming a secondary eye movement (i.e., offline control). In a reflexive saccade task, the oculomotor system can use extraretinal information (i.e., efference copy) online to correct errors in the primary saccade, and offline retinal information to generate a secondary corrective saccade. The purpose of this study was to examine the error correction mechanisms in the antisaccade task. The roles of extraretinal and retinal feedback in maintaining eye movement accuracy were investigated by presenting visual feedback at the spatial goal of the antisaccade. We found that online control for antisaccade is not affected by the presence of visual feedback; that is whether visual feedback is present or not, the duration of the deceleration interval was extended and significantly correlated with reduced antisaccade endpoint error. We postulate that the extended duration of deceleration is a feature of online control during volitional saccades to improve their endpoint accuracy. We found that secondary saccades were generated more frequently in the antisaccade task compared to the reflexive saccade task. Furthermore, we found evidence for a greater contribution from extraretinal sources of feedback in programming the secondary “corrective” saccades in the antisaccade task. Nonetheless, secondary saccades were more corrective for the remaining antisaccade amplitude error in the presence of visual feedback of the target. Taken together, our results reveal a distinctive online error control strategy through an extension of the deceleration interval in the antisaccade task. Target feedback does not improve online control, rather it improves the accuracy of secondary saccades in the antisaccade task.     

The Main Sequence of Saccades Optimizes Speed-accuracy Trade-off

In primates, it is well known that there is a consistent relationship between the duration, peak velocity and amplitude of saccadic eye movements, known as the ‘main sequence’. The reason why such a stereotyped relationship evolved is unknown. We propose that a fundamental constraint on the deployment of foveal vision lies in the motor system that is perturbed by signal-dependent noise (proportional noise) on the motor command. This noise imposes a compromise between the speed and accuracy of an eye movement. We propose that saccade trajectories have evolved to optimize a trade-off between the accuracy and duration of the movement. Taking a semi-analytical approach we use Pontryagin’s minimum principle to show that there is an optimal trajectory for a given amplitude and duration; and that there is an optimal duration for a given amplitude. It follows that the peak velocity is also fixed for a given amplitude. These predictions are in good agreement with observed saccade trajectories and the main sequence. Moreover, this model predicts a small saccadic dead-zone in which it is better to stay eccentric of target than make a saccade onto target. We conclude that the main sequence has evolved as a strategy to optimize the trade-off between accuracy and speed.     

Slow Cortical Potentials Preceeding Visually Guided Saccades in Schizophrenics

The parameters of saccades and presaccadic slow potentials were studied in right-handed men with a dominant right eye, including 19 schizophrenics and 12 healthy subjects. For visual stimulation, three light-emitting diodes were used, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli). Two stimulation protocols were used: with a simultaneous switching off of the central fixation stimulus and switching on of the peripheral stimuli (test 1) and with an interstimulus gap of 200 ms (test 2). According to the latency, saccades were divided into anticipatory, express, and regular. Slow EEG potentials preceding regular saccades were analyzed. It was found that the proportion of anticipatory saccades is considerably higher than the normal value in schizophrenia. The analysis of the presaccadic potentials demonstrated a significant decrease in the amplitude of negative potentials in the vertex region at early stages of presaccadic preparation and its increase in the occipital region at late stages. Test 2 in the patients demonstrated an increase in the positivity focus in the frontal region of the right hemisphere. It was assumed that the alterations found in schizophrenia result from the deficit of frontal cortical fields.     

Response Suppression Delays the Planning of Subsequent Stimulus-Driven Saccades

The completion of an antisaccade selectively increases the reaction time (RT) of a subsequent prosaccade: a result that has been interpreted to reflect the residual inhibition of stimulus-driven saccade networks [1], [2]. In the present investigation we sought to determine whether the increase in prosaccade RT is contingent on the constituent antisaccade planning processes of response suppression and vector inversion or is limited to response suppression. To that end, in one block participants alternated between pro- and antisaccades after every second trial (task-switching block), and in another block participants completed a series of prosaccades that were randomly (and infrequently) interspersed with no-go catch-trials (go/no-go block). Notably, such a design provides a framework for disentangling whether response suppression and/or vector inversion delays the planning of subsequent prosaccades. As expected, results for the task-switching block showed that antisaccades selectively increased the RTs of subsequent prosaccades. In turn, results for the go/no-go block showed that prosaccade RTs were increased when preceded by a no-go catch-trial. Moreover, the magnitude of the RT ‘cost’ was equivalent across the task-switching and go/no-go blocks. That prosaccades preceded by an antisaccade or a no-go catch-trial produced equivalent RT costs indicates that the conjoint processes of response suppression and vector inversion do not drive the inhibition of saccade planning mechanisms. Rather, the present findings indicate that a general consequence of response suppression is a residual inhibition of stimulus-driven saccade networks.     

Smoothing Spline ANOVA Decomposition of Arbitrary Splines: An Application to Eye Movements in Reading

The Smoothing Spline ANOVA (SS-ANOVA) requires a specialized construction of basis and penalty terms in order to incorporate prior knowledge about the data to be fitted. Typically, one resorts to the most general approach using tensor product splines. This implies severe constraints on the correlation structure, i.e. the assumption of isotropy of smoothness can not be incorporated in general. This may increase the variance of the spline fit, especially if only a relatively small set of observations are given. In this article, we propose an alternative method that allows to incorporate prior knowledge without the need to construct specialized bases and penalties, allowing the researcher to choose the spline basis and penalty according to the prior knowledge of the observations rather than choosing them according to the analysis to be done. The two approaches are compared with an artificial example and with analyses of fixation durations during reading.     

Saccades Improve Postural Control: A Developmental Study in Normal Children

Introduction

Dual-task performance is known to affect postural stability in children. This study focused on the effect of oculomotor tasks like saccadic eye movements on postural stability, studied in a large population of children by recording simultaneously their eye movements and posture.

Materials and Methods

Ninety-five healthy children from 5.8 to 17.6 years old were examined. All children were free of any vestibular, neurological, ophtalmologic and orthoptic abnormalities. Postural control was measured with a force platform TechnoConcept®, and eye movements with video oculography (MobilEBT®). Children performed two oculomotor tasks: fixation of a stable central target and horizontal saccades. We measured the saccade latency and the number of saccades during fixation as well as the surface, length and mean velocity of the center of pressure.

Results

During postural measurement, we observed a correlation between the age on the one hand and a decrease in saccade latency as well as an improvement in the quality of fixation on the other. Postural sway decreases with age and is reduced in the dual task (saccades) in comparison with a simple task of fixation.

Discussion - Conclusion

These results suggest a maturation of neural circuits controlling posture and eye movements during childhood. This study also shows the presence of an interaction between the oculomotor system and the postural system. Engaging in oculomotor tasks results in a reduction of postural sway.     

Blink Perturbation Effects on Saccades Evoked by Microstimulation of the Superior Colliculus

Current knowledge of saccade-blink interactions suggests that blinks have paradoxical effects on saccade generation. Blinks suppress saccade generation by attenuating the oculomotor drive command in structures like the superior colliculus (SC), but they also disinhibit the saccadic system by removing the potent inhibition of pontine omnipause neurons (OPNs). To better characterize these effects, we evoked the trigeminal blink reflex by delivering an air puff to one eye as saccades were evoked by sub-optimal stimulation of the SC. For every stimulation site, the peak and average velocities of stimulation with blink movements (SwBMs) were lower than stimulation-only saccades (SoMs), supporting the notion that the oculomotor drive is weakened in the presence of a blink. In contrast, the duration of the SwBMs was longer, consistent with the hypothesis that the blink-induced inhibition of the OPNs could prolong the window of time available for oculomotor commands to drive an eye movement. The amplitude of the SwBM could also be larger than the SoM amplitude obtained from the same site, particularly for cases in which blink-associated eye movements exhibited the slowest kinematics. The results are interpreted in terms of neural signatures of saccade-blink interactions.     

Neural Activity in the Macaque Putamen Associated with Saccades and Behavioral Outcome

It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour.     

How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization

Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.     

Spatial Interactions between Successive Eye and Arm Movements: Signal Type Matters

Spatial interactions between consecutive movements are often attributed to inhibition of return (IOR), a phenomenon in which responses to previously signalled locations are slower than responses to unsignalled locations. In two experiments using peripheral target signals offset by 0°, 90°, or 180°, we show that consecutive saccadic (Experiment 1) and reaching (Experiment 3) responses exhibit a monotonic pattern of reaction times consistent with the currently established spatial distribution of IOR. In contrast, in two experiments with central target signals (i.e., arrowheads pointing at target locations), we find a non-monotonic pattern of reaction times for saccades (Experiment 2) and reaching movements (Experiment 4). The difference in the patterns of results observed demonstrates different behavioral effects that depend on signal type. The pattern of results observed for central stimuli are consistent with a model in which neural adaptation is occurring within motor networks encoding movement direction in a distributed manner.