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.     

Kinematics of Visually-Guided Eye Movements

One of the hallmarks of an eye movement that follows Listing’s law is the half-angle rule that says that the angular velocity of the eye tilts by half the angle of eccentricity of the line of sight relative to primary eye position. Since all visually-guided eye movements in the regime of far viewing follow Listing’s law (with the head still and upright), the question about its origin is of considerable importance. Here, we provide theoretical and experimental evidence that Listing’s law results from a unique motor strategy that allows minimizing ocular torsion while smoothly tracking objects of interest along any path in visual space. The strategy consists in compounding conventional ocular rotations in meridian planes, that is in horizontal, vertical and oblique directions (which are all torsion-free) with small linear displacements of the eye in the frontal plane. Such compound rotation-displacements of the eye can explain the kinematic paradox that the fixation point may rotate in one plane while the eye rotates in other planes. Its unique signature is the half-angle law in the position domain, which means that the rotation plane of the eye tilts by half-the angle of gaze eccentricity. We show that this law does not readily generalize to the velocity domain of visually-guided eye movements because the angular eye velocity is the sum of two terms, one associated with rotations in meridian planes and one associated with displacements of the eye in the frontal plane. While the first term does not depend on eye position the second term does depend on eye position. We show that compounded rotation - displacements perfectly predict the average smooth kinematics of the eye during steady- state pursuit in both the position and velocity domain.     

Eye Movements in Ephedrone-Induced Parkinsonism

Patients with ephedrone parkinsonism (EP) show a complex, rapidly progressive, irreversible, and levodopa non-responsive parkinsonian and dystonic syndrome due to manganese intoxication. Eye movements may help to differentiate parkinsonian syndromes providing insights into which brain networks are affected in the underlying disease, but they have never been systematically studied in EP. Horizontal and vertical eye movements were recorded in 28 EP and compared to 21 Parkinson''s disease (PD) patients, and 27 age- and gender-matched healthy subjects using standardized oculomotor tasks with infrared videooculography. EP patients showed slow and hypometric horizontal saccades, an increased occurrence of square wave jerks, long latencies of vertical antisaccades, a high error rate in the horizontal antisaccade task, and made more errors than controls when pro- and antisaccades were mixed. Based on oculomotor performance, a direct differentiation between EP and PD was possible only by the velocity of horizontal saccades. All remaining metrics were similar between both patient groups. EP patients present extensive oculomotor disturbances probably due to manganese-induced damage to the basal ganglia, reflecting their role in oculomotor system.     

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

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

Dissonant Representations of Visual Space in Prefrontal Cortex during Eye Movements

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A Role of Eye Vergence in Covert Attention

Covert spatial attention produces biases in perceptual and neural responses in the absence of overt orienting movements. The neural mechanism that gives rise to these effects is poorly understood. Here we report the relation between fixational eye movements, namely eye vergence, and covert attention. Visual stimuli modulate the angle of eye vergence as a function of their ability to capture attention. This illustrates the relation between eye vergence and bottom-up attention. In visual and auditory cue/no-cue paradigms, the angle of vergence is greater in the cue condition than in the no-cue condition. This shows a top-down attention component. In conclusion, observations reveal a close link between covert attention and modulation in eye vergence during eye fixation. Our study suggests a basis for the use of eye vergence as a tool for measuring attention and may provide new insights into attention and perceptual disorders.     

Saccadic Eye Movements in Anorexia Nervosa

Background

Anorexia Nervosa (AN) has a mortality rate among the highest of any mental illness, though the factors involved in the condition remain unclear. Recently, the potential neurobiological underpinnings of the condition have become of increasing interest. Saccadic eye movement tasks have proven useful in our understanding of the neurobiology of some other psychiatric illnesses as they utilise known brain regions, but to date have not been examined in AN. The aim of this study was to investigate whether individuals with AN differ from healthy individuals in performance on a range of saccadic eye movements tasks.

Methods

24 females with AN and 25 healthy individuals matched for age, gender and premorbid intelligence participated in the study. Participants were required to undergo memory-guided and self-paced saccade tasks, and an interleaved prosaccade/antisaccade/no-go saccade task while undergoing functional magnetic resonance imaging (fMRI).

Results

AN participants were found to make prosaccades of significantly shorter latency than healthy controls. AN participants also made an increased number of inhibitory errors on the memory-guided saccade task. Groups did not significantly differ in antisaccade, no-go saccade or self-paced saccade performance, or fMRI findings.

Discussion

The results suggest a potential role of GABA in the superior colliculus in the psychopathology of AN.     

On the Functions of Eye Movements

Many studies have been devoted to the investigation of eye movements. Procedures for recording eye movements (11), as well as concrete clinical (6, 7), engineering (3), and developmental investigations (9), are many and varied. However, in spite of the fact that various investigators have accumulated an enormous quantity of material, the diverse functions played by eye movements in the solution of various problems by humans have not been sufficiently discussed.     

Abnormal Fixational Eye Movements in Amblyopia

Purpose

Fixational saccades shift the foveal image to counteract visual fading related to neural adaptation. Drifts are slow eye movements between two adjacent fixational saccades. We quantified fixational saccades and asked whether their changes could be attributed to pathologic drifts seen in amblyopia, one of the most common causes of blindness in childhood.

Methods

Thirty-six pediatric subjects with varying severity of amblyopia and eleven healthy age-matched controls held their gaze on a visual target. Eye movements were measured with high-resolution video-oculography during fellow eye-viewing and amblyopic eye-viewing conditions. Fixational saccades and drifts were analyzed in the amblyopic and fellow eye and compared with controls.

Results

We found an increase in the amplitude with decreased frequency of fixational saccades in children with amblyopia. These alterations in fixational eye movements correlated with the severity of their amblyopia. There was also an increase in eye position variance during drifts in amblyopes. There was no correlation between the eye position variance or the eye velocity during ocular drifts and the amplitude of subsequent fixational saccade. Our findings suggest that abnormalities in fixational saccades in amblyopia are independent of the ocular drift.

Discussion

This investigation of amblyopia in pediatric age group quantitatively characterizes the fixation instability. Impaired properties of fixational saccades could be the consequence of abnormal processing and reorganization of the visual system in amblyopia. Paucity in the visual feedback during amblyopic eye-viewing condition can attribute to the increased eye position variance and drift velocity.     

Fetal Eye Movements on Magnetic Resonance Imaging

Objectives

Eye movements are the physical expression of upper fetal brainstem function. Our aim was to identify and differentiate specific types of fetal eye movement patterns using dynamic MRI sequences. Their occurrence as well as the presence of conjugated eyeball motion and consistently parallel eyeball position was systematically analyzed.

Methods

Dynamic SSFP sequences were acquired in 72 singleton fetuses (17–40 GW, three age groups [17–23 GW, 24–32 GW, 33–40 GW]). Fetal eye movements were evaluated according to a modified classification originally published by Birnholz (1981): Type 0: no eye movements; Type I: single transient deviations; Type Ia: fast deviation, slower reposition; Type Ib: fast deviation, fast reposition; Type II: single prolonged eye movements; Type III: complex sequences; and Type IV: nystagmoid.

Results

In 95.8% of fetuses, the evaluation of eye movements was possible using MRI, with a mean acquisition time of 70 seconds. Due to head motion, 4.2% of the fetuses and 20.1% of all dynamic SSFP sequences were excluded.Eye movements were observed in 45 fetuses (65.2%). Significant differences between the age groups were found for Type I (p = 0.03), Type Ia (p = 0.031), and Type IV eye movements (p = 0.033). Consistently parallel bulbs were found in 27.3–45%.

Conclusions

In human fetuses, different eye movement patterns can be identified and described by MRI in utero. In addition to the originally classified eye movement patterns, a novel subtype has been observed, which apparently characterizes an important step in fetal brainstem development. We evaluated, for the first time, eyeball position in fetuses. Ultimately, the assessment of fetal eye movements by MRI yields the potential to identify early signs of brainstem dysfunction, as encountered in brain malformations such as Chiari II or molar tooth malformations.     

Quantitative Linking Hypotheses for Infant Eye Movements

The study of cognitive development hinges, largely, on the analysis of infant looking. But analyses of eye gaze data require the adoption of linking hypotheses: assumptions about the relationship between observed eye movements and underlying cognitive processes. We develop a general framework for constructing, testing, and comparing these hypotheses, and thus for producing new insights into early cognitive development. We first introduce the general framework – applicable to any infant gaze experiment – and then demonstrate its utility by analyzing data from a set of experiments investigating the role of attentional cues in infant learning. The new analysis uncovers significantly more structure in these data, finding evidence of learning that was not found in standard analyses and showing an unexpected relationship between cue use and learning rate. Finally, we discuss general implications for the construction and testing of quantitative linking hypotheses. MATLAB code for sample linking hypotheses can be found on the first author''s website.     

Observations on Eye Movements in Amphibian Larvae

Observations have shown that amphibian larvae, contrary to what has been stated in the literature, have different kinds of eye movements. All of the anurans observed (Xenopus, Rana, Bufo, Hyperoleus and Bombina) have some kind of reflex eye movements effected through stimuli from the labyrinth organs as a response to movements of the body, while only Rana and Bufo have spontaneous scanning movements. Of the urodelians (Ambystoma and Triturus), larvae of Ambystoma have no observable eye movements, while Triturus larvae have reflex eye movements associated with movements of the neck, as well as spontaneous scanning movements; both kinds of movements differ from those seen in Anura.     

Saccadic Eye Movements in Depressed Elderly Patients

The primary aim of this study was to characterize oculomotor performances in elderly depressed patients. The second aim was to investigate whether cognitive inhibition measured by the antisaccade task was associated with a psychomotor retardation or rather with a more specific cognitive-motor inhibition deficit. Twenty patients with a major depressive disorder and forty-seven healthy subjects performed two eye movement tasks. Saccadic reaction time and error rates were analyzed in the prosaccade task to obtain basic parameters of eye movements. Saccade latency, error rates and correction rates were evaluated in the antisaccade task to investigate inhibition capacities. Performances were impaired in patients, who exhibited a higher reaction time and error rates compared to controls. The higher time cost of inhibition suggested that the reaction time was not related to global psychomotor retardation alone. The higher time cost of inhibition could be explained by a specific alteration of inhibition processes evaluated by the antisaccade task. These changes were associated with the severity of depression. These findings provide a new perspective on cognitive inhibition in elderly depressed patients and could have important clinical implications for our understanding of critical behaviors involving deficits in inhibitory processes in the elderly.     

Anticipatory Smooth Eye Movements in Autism Spectrum Disorder

Smooth pursuit eye movements are important for vision because they maintain the line of sight on targets that move smoothly within the visual field. Smooth pursuit is driven by neural representations of motion, including a surprisingly strong influence of high-level signals representing expected motion. We studied anticipatory smooth eye movements (defined as smooth eye movements in the direction of expected future motion) produced by salient visual cues in a group of high-functioning observers with Autism Spectrum Disorder (ASD), a condition that has been associated with difficulties in either generating predictions, or translating predictions into effective motor commands. Eye movements were recorded while participants pursued the motion of a disc that moved within an outline drawing of an inverted Y-shaped tube. The cue to the motion path was a visual barrier that blocked the untraveled branch (right or left) of the tube. ASD participants showed strong anticipatory smooth eye movements whose velocity was the same as that of a group of neurotypical participants. Anticipatory smooth eye movements appeared on the very first cued trial, indicating that trial-by-trial learning was not responsible for the responses. These results are significant because they show that anticipatory capacities are intact in high-functioning ASD in cases where the cue to the motion path is highly salient and unambiguous. Once the ability to generate anticipatory pursuit is demonstrated, the study of the anticipatory responses with a variety of types of cues provides a window into the perceptual or cognitive processes that underlie the interpretation of events in natural environments or social situations.     

Real-Time Subject-Independent Pattern Classification of Overt and Covert Movements from fNIRS Signals

Recently, studies have reported the use of Near Infrared Spectroscopy (NIRS) for developing Brain–Computer Interface (BCI) by applying online pattern classification of brain states from subject-specific fNIRS signals. The purpose of the present study was to develop and test a real-time method for subject-specific and subject-independent classification of multi-channel fNIRS signals using support-vector machines (SVM), so as to determine its feasibility as an online neurofeedback system. Towards this goal, we used left versus right hand movement execution and movement imagery as study paradigms in a series of experiments. In the first two experiments, activations in the motor cortex during movement execution and movement imagery were used to develop subject-dependent models that obtained high classification accuracies thereby indicating the robustness of our classification method. In the third experiment, a generalized classifier-model was developed from the first two experimental data, which was then applied for subject-independent neurofeedback training. Application of this method in new participants showed mean classification accuracy of 63% for movement imagery tasks and 80% for movement execution tasks. These results, and their corresponding offline analysis reported in this study demonstrate that SVM based real-time subject-independent classification of fNIRS signals is feasible. This method has important applications in the field of hemodynamic BCIs, and neuro-rehabilitation where patients can be trained to learn spatio-temporal patterns of healthy brain activity.