Fixational Eye Movements Research Articles

Saccade and Fixation Eye Movements During Walking in People With Mild Traumatic Brain Injury.

Background: Clinical and laboratory assessment of people with mild traumatic brain injury (mTBI) indicate impairments in eye movements. These tests are typically done in a static, seated position. Recently, the use of mobile eye-tracking systems has been proposed to quantify subtle deficits in eye movements and visual sampling during different tasks. However, the impact of mTBI on eye movements during functional tasks such as walking remains unknown. Objective: Evaluate differences in eye-tracking measures collected during gait between healthy controls (HC) and patients in the sub-acute stages of mTBI recovery and to determine if there are associations between eye-tracking measures and gait speed. Methods: Thirty-seven HC participants and 67individuals with mTBI were instructed to walk back and forth over 10-m, at a comfortable self-selected speed. A single 1-min trial was performed. Eye-tracking measures were recorded using a mobile eye-tracking system (head-mounted infra-red Tobbii Pro Glasses 2, 100 Hz, Tobii Technology Inc. VA, United States). Eye-tracking measures included saccadic (frequency, mean and peak velocity, duration and distance) and fixation measurements (frequency and duration). Gait was assessed using six inertial sensors (both feet, sternum, right wrist, lumbar vertebrae and the forehead) and gait velocity was selected as the primary outcome. General linear model was used to compare the groups and association between gait and eye-tracking outcomes were explored using partial correlations. Results: Individuals with mTBI showed significantly reduced saccade frequency (p = 0.016), duration (p = 0.028) and peak velocity (p = 0.032) compared to the HC group. No significant differences between groups were observed for the saccade distance, fixation measures and gait velocity (p > 0.05). A positive correlation was observed between saccade duration and gait velocity only for participants with mTBI (p = 0.025). Conclusion: Findings suggest impaired saccadic eye movement, but not fixations, during walking in individuals with mTBI. These findings have implications in real-world function including return to sport for athletes and return to duty for military service members. Future research should investigate whether or not saccade outcomes are influenced by the time after the trauma and rehabilitation.

Fixational eye movements in passive versus active sustained fixation tasks.

Human fixational eye movements are so small and precise that high-speed, accurate tools are needed to fully reveal their properties and functional roles. Where the fixated image lands on the retina and how it moves for different levels of visually demanding tasks is the subject of the current study. An Adaptive Optics Scanning Laser Ophthalmoscope (AOSLO) was used to image, track and present a variety of fixation targets (Maltese cross, disk, concentric circles, Vernier and tumbling-E letter) to healthy subjects. During these different passive (static) or active (discriminating) tasks under natural eye motion, the landing position of the target on the retina was tracked in space and time over the retinal image directly with high spatial (<1 arcmin) and temporal (960 Hz) resolution. We computed both the eye motion and the exact trajectory of the fixated target's motion over the retina. We confirmed that compared to passive tasks, active tasks elicited a partial inhibition of microsaccades, leading to longer drift periods compensated by larger corrective saccades. Consequently, the overall fixation stability during active tasks was on average 57% larger than during passive tasks. The preferred retinal locus of fixation was the same for each task and did not coincide with the location of the peak cone density.

The Study of Security Priming on Avoidant Attentional Biases: Combining Microsaccadic Eye-Movement Measurement With a Dot-Probe Task.

Microsaccades are small fixational eye movements that have shown to index covert attentional shifts. The present experiment combined microsaccades with performance measures from a dot-probe task to study influences of attachment security priming on the attentional biases of individuals high in attachment avoidance. Security priming is an experimental manipulation aimed at boosting felt security. Using a randomized, mixed design, we measured differences in attentional vigilance toward angry and neutral faces as a function of priming (neutral vs. secure) and attachment avoidance. Individuals high in avoidance habitually tend to withdraw from, or otherwise dismiss, emotionally salient stimuli. Here, we operationalized attentional withdrawal based on both task performance in the dot-probe task and microsaccadic movements. In addition, unlike previous studies where priming salience for the individual participant has been unclear, we used a standardized narrative method for attachment script assessment, securing an indication of how strongly each participant was primed. Dot-probe data significantly captured the link between avoidance and attentional disengagement, though from all facial stimuli (angry and neutral). Although microsaccadic movements did not capture avoidant attentional disengagement, they positively correlated to dot-probe data suggesting measurement convergence. Avoidance was associated with weaker security priming and no overall effect of priming on attention was found, indicating a need for further exploration of suitable priming methods to bypass avoidant deactivation. Our results provide a first indication that, as an implicit looking measure, microsaccadic movements can potentially reveal where early attention is directed at the exact moment of stimulus presentation.

Role of the frontal eye field in human microsaccade responses: A TMS study

Microsaccade is a type of fixational eye movements that is modulated by various sensory and cognitive processes, and impact our visual perception. Although studies in monkeys have demonstrated a functional role for the superior colliculus and frontal eye field (FEF) in controlling microsaccades, our understanding of the neural mechanisms underlying the generation of microsaccades is still limited. By applying continuous theta-burst stimulation (cTBS) over the right FEF and the vertex, we investigated the role of the FEF in generating human microsaccade responses evoked by salient stimuli or by changes in background luminance. We observed higher microsaccade rates prior to target appearance, and larger rebound in microsaccade occurrence following salient stimuli, when disruptive cTBS was applied over FEF compared to vertex stimulation. Moreover, the microsaccade direction modulation after changes in background luminance was disrupted with FEF stimulation. Together, our results constitute the first evidence of FEF modulation in human microsaccade responses.

Linking individual differences in fixational eye movements and visual acuity

Linking individual differences in fixational eye movements and visual acuity

Cognitive influences on fixational eye movements during visual discrimination

Cognitive influences on fixational eye movements during visual discrimination

Modulation of fixational eye movements during visual crowding

Modulation of fixational eye movements during visual crowding

From fixation to fixational eye movements – microsaccades in perceptual learning

From fixation to fixational eye movements – microsaccades in perceptual learning

Fixational eye movements and visual functions in amblyopia

Amblyopic patients have a constellation of visual function deficits including reduced visual acuity and contrast sensitivity, abnormal stereopsis, and increased fixation instability of fellow and amblyopic eye. The fixation instability arises from presence of nystagmus and altered physiologic fixation eye movements (FEMs). The purpose of the study is to examine the effects of presence of nystagmus on binocular and monocular functions of the fellow and amblyopic eye.

Fixation eye movement abnormalities and stereopsis recovery following strabismus repair

We evaluated the effects of strabismus repair on fixational eye movements (FEMs) and stereopsis recovery in patients with fusion maldevelopment nystagmus (FMN) and patients without nystagmus. Twenty-one patients with strabismus, twelve with FMN and nine without nystagmus, were tested before and after strabismus repair. Eye-movements were recorded during a gaze-holding task under monocular viewing conditions. Fast (fixational saccades and quick phases of nystagmus) and slow (inter-saccadic drifts and slow phases of nystagmus) FEMs and bivariate contour ellipse area (BCEA) were analyzed in the viewing and non-viewing eye. Strabismus repair improved the angle of strabismus in subjects with and without FMN, however patients without nystagmus were more likely to have improvement in stereoacuity. The fixational saccade amplitudes and intersaccadic drift velocities in both eyes decreased after strabismus repair in subjects without nystagmus. The slow phase velocities were higher in patients with FMN compared to inter-saccadic drifts in patients without nystagmus. There was no change in the BCEA after surgery in either group. In patients without nystagmus, the improvement of the binocular function (stereopsis), as well as decreased fixational saccade amplitude and intersaccadic drift velocity, could be due, at least partially, to central adaptive mechanisms rendered possible by surgical realignment of the eyes. The absence of improvement in patients with FMN post strabismus repair likely suggests the lack of such adaptive mechanisms in patients with early onset infantile strabismus. Assessment of fixation eye movement characteristics can be a useful tool to predict functional improvement post strabismus repair.

IDENTIFYING TRENDS IN MICROSACCADE RATE ON OCULOMOTOR TRACKER IN EARLY VS LATE STAGE PEDIATRIC CASES WITH PERSISTENT POST-CONCUSSION SYMPTOMS (PPCS)

Background:Oculomotor and visual processing deficits occur commonly after brain injury in young athletes. A subset of these concussed athletes do experience prolonged recoveries or PPCS with ongoing oculomotor deficits and visual symptoms. There have been limited studies conducted to determine the significance of oculomotor tracking (OMT) testing in the pediatric population, and even less investigating the role of microsaccades. Hence, investigations on microsaccades(MS), physiological adjustive micro eye movements critical in visual processing and central/peripheral visual integration, may provide insight on the role of visual dysfunction in PPCS course, prognosis, and management.Purpose:The purpose of this study is to identify possible MS rate trends and differences between early and late stage PPCS pediatric patients.Methods:A retrospective cohort study of 41 pediatric patients with PPCS or symptoms greater than one month from injury. Data was collected from 7/1/2018 to 12/1/2019 and the age group ranged from 8 to 21 years. For each participant, using the OMT device we measured the number of saccades generated, the size and speed of the microsaccades, the area covered and the ratio of vertical-to-horizontal direction component of the fixational eye movements, using a 250 Hz video-eye tracker mounted inside a HTC Vive VR headset. Participants were instructed to fixate on a central dot for 140 seconds, in 20-second intervals. Patients were classified into early or late stages of PPCS (early stage: 1-6 months; late stage: >6 months) to compare MS rate between stages. Exclusion criteria included history of visual disorders, learning disorders, seizure disorder, or intracranial hemorrhage.Results:27 patients were in the early stage while 14 patients were in the late stage. The early stage group had a mean MS rate of 125 beats/min while the late stage group had a mean MS rate of 116 beats/min. A two sample t-test assuming no difference between early and late stage patients resulted in a p value of 0.51.Conclusion:There is a potential trend in declining MS numbers with progressive PPCS stage. Although the t-test didn’t show statistical significance, this could be due to the small sample size of our study. Future studies are needed to validate this initial finding and to identify the significance of microsaccade patterns in concussion prognosis and management.Figure 1:

Transient perceptual enhancements resulting from selective shifts of exogenous attention in the central fovea

Exogenous attention, a powerful adaptive tool that quickly and involuntarily orients processing resources to salient stimuli, has traditionally been studied in the lower-resolution parafoveal and peripheral visual field.1-4 It is not known whether and how it operates across the 1° central fovea where visual resolution peaks.5,6 Here we investigated the dynamics of exogenous attention in the foveola. To circumvent the challenges posed by fixational eye movements at this scale, we used high-precision eye-tracking and gaze-contingent display control for retinal stabilization.7 High-acuity stimuli were briefly presented foveally at varying delays following an exogenous cue. Attended and unattended locations were just a few arcminutes away from the preferred locus of fixation. Our results show that for short temporal delays, observers' ability to discriminate fine detail is enhanced at the cued location. This enhancement is highly localized and does not extend to the nearby locations only 16' away. On a longer timescale, instead, we report an inverse effect: paradoxically, acuity is sharper at the unattended locations, resembling the phenomenon of inhibition of return at much larger eccentricities.8-10 Although exogenous attention represents a mechanism for low-cost monitoring of the environment in the extrafoveal space, these findings show that, in the foveola, it transiently modulates vision of detail with a high degree of resolution. Together with inhibition of return, it may aid visual exploration of complex foveal stimuli.11.

Phase space dynamics of eye-movement deficits in psychiatric patients

IntroductionEye movement deficits in psychiatric patients have often been investigated with linear models, which fail to fully capture the complex dynamics characterizing eye movements.ObjectivesThe present work aims to investigate the deficits in fixational eye movements in psychiatric patients according as non-linear chaotic dynamic.MethodsWe recruited 191 patients (91 males, average age 45 years) diagnosed with schizophrenia, bipolar disorder, depression and personality disorder. The control sample consisted of 22 healthy subjects (12 males, mean age 41 years). Fixational eye movements were recorded with the Eytribe infrared system and off-line analyzed using Matlab. The dynamics of fixation eye movements were investigated using a phase space graph, which refers to chaotic system analysis. This analysis allows to evaluate how the changes in space during fixation as a function of their speed.ResultsA major difference emerged: psychiatric patients showed larger and faster eye movements gravitating around a single point of density, while control subjects exhibited slower and smaller eye movements with multiple drifts and microtremors.ConclusionsIn conclusion, the dynamics of fixational eye movements in psychiatric patients seemed to be characterized by poorer efficiency in space exploration. These differences could be attributed to a worse coordination between the perceptual and the oculomotor system.DisclosureNo significant relationships.

Monocular and Binocular Visual Function Deficits in Amblyopic Patients with and without Fusion Maldevelopment Nystagmus.

PurposeThe aim of the study is to examine the association between amblyopia type and the presence of nystagmus on binocular and monocular functions of the fellow (FE) and amblyopic eye (AE).MethodsWe recruited 19 controls and 44 amblyopes (anisometropes=13, strabismic=10, mixed=21). We measured visual, grating, and vernier acuities and high/low spatial frequency (SF) contrast sensitivities in each eye using a staircase method. Stereoacuity was measured with the Titmus fly test. We recorded fixation eye movements (FEM) using high-resolution video-oculography. Subjects were classified as having either no nystagmus (n=18), fusion maldevelopment nystagmus syndrome (FMNS) (n=12), or nystagmus without any structural anomalies that does not meet the criteria for FMNS or infantile nystagmus (n=14).ResultsAnalysis of visual function by clinical amblyopia type showed that patients with strabismus/mixed amblyopia (F (2,54)=9.5, p<0.001) were more likely to have poor stereopsis while controlling for AE grating acuity deficit. The FE of patients with anisometropia had greater contrast sensitivity deficits at low (F (2,43)=4.4, p=0.018) and high SF (F (2,42)=10.1, p<0.001). Analysis of visual function by FEM characteristics (low SF: (F (3,43)=4.3, p=0.010) and high SF: (F (3,42)=7.1, p=0.001) showed that the FE of patients with FMNS had worse low and high SF contrast sensitivities, whereas those without FMNS had greater contrast sensitivity deficits only at high SF compared to controls. Patients with FMNS (F (3,54) = 12.9, p<0.001) were more likely to have poor stereopsis while controlling for AE grating acuity deficit compared to patients without FMNS. All amblyopic patients had worse high SF contrast sensitivity of the AE irrespective of type or FEM characteristics (Type = F (2,43)=8.8, p=0.001; FEM characteristics= F (3,43)=5.1, p=0.004).ConclusionThe presence of FMNS in patients with strabismic/mixed amblyopia is associated with poor/absent stereopsis. FE deficits vary across amblyopia type. Like FEM abnormalities, visual function deficits are seen in the FE of patients with and without nystagmus.

Introduction of a New Test for Standardizing and Quantifying Monocular Fixation: The Aalen-Pacific Fixation Accuracy &amp; Stability Test (AP-FAST)

Background: This is a two-part paper, in which fixational eye movements are reviewed in part one, and a new clinical test of fixational eye movement accuracy and stability is introduced in part two. Part two also contains a partial validation study and normative results for this new test. The study was designed to explore the following questions: 1. Is there a significant difference in clinically measurable fixation stability and accuracy between symptomatic individuals who have sustained mTBI versus visually normal individuals who have not sustained TBI? 2a. Could the Macular Integrity Tester (MIT) be useful as a diagnostic instrument for differentiating fixation stability and accuracy with mTBI patients versus those without TBI? 2b. If so, could introduction of a standardized test protocol (AP-FAST) allow for more reliable and descriptive quantification of monocular fixation behavior? Methods: To answer the first question posed in our study, data were compared between non-mTBIs and mTBI patients using two different fixation testing methods. One of the methods employed the eyetracker EyeLink II comparing optometry students to mTBI patients. Fixation accuracy and stability were measured with a custom fixation pattern program. Fixation results were compared for both groups. To answer question 2a, we compared fixation behavior for both groups using the MIT diagnostically by having each subject rate accuracy and stability of his/her own fixation posture. To address question 2b, a 15-point rating system protocol was created to help describe and quantify monocular fixation behavior via Haidinger’s brush perception. Two groups of test subjects: mTBI patients versus visually normal subjects were compared using the AP-FAST grid and fixation behavior survey. Results: Regarding question one, there was a significant and clinically relevant difference in monocular fixation stability and accuracy between the visual normal subject group and mTBI patient group, with normals demonstrating better accuracy and stability. Regarding questions 2a and 2b, the mTBI patient group had poorer mean ability (statistically significant) to perceive, localize, and center the Haidinger’s brush than those in the non-TBI group. Based on our results, we propose that the newly developed AP-FAST is useful for helping describe, standardize and quantify how the Haidinger’s brush entoptic phenomenon is perceived monocularly by both mTBI and nonmTBI subjects.

Strip-based digital image registration for distortion minimization and robust eye motion measurement from scanned ophthalmic imaging systems.

Retinal image-based eye motion measurement from scanned ophthalmic imaging systems, such as scanning laser ophthalmoscopy, has allowed for precise real-time eye tracking at sub-micron resolution. However, the constraints of real-time tracking result in a high error tolerance that is detrimental for some eye motion measurement and imaging applications. We show here that eye motion can be extracted from image sequences when these constraints are lifted, and all data is available at the time of registration. Our approach identifies and discards distorted frames, detects coarse motion to generate a synthetic reference frame and then uses it for fine scale motion tracking with improved sensitivity over a larger area. We demonstrate its application here to tracking scanning laser ophthalmoscopy (TSLO) and adaptive optics scanning light ophthalmoscopy (AOSLO), and show that it can successfully capture most of the eye motion across each image sequence, leaving only between 0.1-3.4% of non-blink frames untracked, while simultaneously minimizing image distortions induced from eye motion. These improvements will facilitate precise measurement of fixational eye movements (FEMs) in TSLO and longitudinal tracking of individual cells in AOSLO.

Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements.

Visual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called microsaccades, is still involved. Microsaccades are small saccades that occur when maintaining precise gaze fixation on a stationary point, and they exhibit robust modulations in peripheral cueing paradigms used to investigate covert visual selection mechanisms. These modulations consist of changes in both microsaccade directions and frequencies after cue onsets. Over the past two decades, the properties and functional implications of these modulations have been heavily studied, revealing a potentially important role for microsaccades in mediating covert visual selection effects. However, the neural mechanisms underlying cueing effects on microsaccades are only beginning to be investigated. Here we review the available causal manipulation evidence for these effects’ cortical and subcortical substrates. In the superior colliculus (SC), activity representing peripheral visual cues strongly influences microsaccade direction, but not frequency, modulations. In the cortical frontal eye fields (FEF), activity only compensates for early reflexive effects of cues on microsaccades. Using evidence from behavior, theoretical modeling, and preliminary lesion data from the primary visual cortex and microstimulation data from the lower brainstem, we argue that the early reflexive microsaccade effects arise subcortically, downstream of the SC. Overall, studying cueing effects on microsaccades in primates represents an important opportunity to link perception, cognition, and action through unaddressed cortical-subcortical neural interactions. These interactions are also likely relevant in other sensory and motor modalities during other active behaviors.

Active vision at the foveal scale in the primate superior colliculus.

The primate superior colliculus (SC) has recently been shown to possess both a large foveal representation as well as a varied visual processing repertoire. This structure is also known to contribute to eye movement generation. Here, we describe our current understanding of how SC visual and movement-related signals interact within the realm of small eye movements associated with the foveal scale of visuomotor behavior. Within the SC's foveal representation, there is a full spectrum of visual, visual-motor, and motor-related discharge for fixational eye movements. Moreover, a substantial number of neurons only emit movement-related discharge when microsaccades are visually guided, but not when similar movements are generated toward a blank. This represents a particularly striking example of integrating vision and action at the foveal scale. Beyond that, SC visual responses themselves are strongly modulated, and in multiple ways, by the occurrence of small eye movements. Intriguingly, this impact can extend to eccentricities well beyond the fovea, causing both sensitivity enhancement and suppression in the periphery. Because of large foveal magnification of neural tissue, such long-range eccentricity effects are neurally warped into smaller differences in anatomical space, providing a structural means for linking peripheral and foveal visual modulations around fixational eye movements. Finally, even the retinal-image visual flows associated with tiny fixational eye movements are signaled fairly faithfully by peripheral SC neurons with relatively large receptive fields. These results demonstrate how studying active vision at the foveal scale represents an opportunity for understanding primate vision during natural behaviors involving ever-present foveating eye movements.NEW & NOTEWORTHY The primate superior colliculus (SC) is ideally suited for active vision at the foveal scale: it enables detailed foveal visual analysis by accurately driving small eye movements, and it also possesses a visual processing machinery that is sensitive to active eye movement behavior. Studying active vision at the foveal scale in the primate SC is informative for broader aspects of active perception, including the overt and covert processing of peripheral extra-foveal visual scene locations.

Effects of subthalamic deep brain stimulation on fixational eye movements in Parkinson's disease.

Miniature yoked eye movements, fixational saccades, are critical to counteract visual fading. Fixational saccades are followed by a return saccades forming squarewaves. Present in healthy states, squarewaves, if too many or too big, affect visual stability. Parkinson's disease (PD), where visual deficits are not uncommon, is associated with the squarewaves that are excessive in number or size. Our working hypothesis is that the basal ganglia are at the epicenter of the abnormal fixational saccades and squarewaves in PD; the effects are manifested through their connections to the superior colliculus (affecting saccade frequency and amplitude) and the cerebellum (affecting velocity and amplitude). We predict that the subthalamic deep brain stimulation (DBS) variably affects the amplitude, frequency, and velocity of fixational saccade and that the effect depends on the electrode's proximity or the volume of activated tissue in the subthalamic nucleus' connections with the superior colliculus or the cerebellum. We found that DBS modulated saccade amplitude, frequency, and velocity in 11 PD patients. Although all three parameters were affected, the extent of the effects varied amongst subjects. The modulation was dependent upon the location and size of the electrically activated volume of the subthalamic region.

Micro-pursuit: A class of fixational eye movements correlating with smooth, predictable, small-scale target trajectories.

Humans generate ocular pursuit movements when a moving target is tracked throughout the visual field. In this article, we show that pursuit can be generated and measured at small amplitudes, at the scale of fixational eye movements, and tag these eye movements as micro-pursuits. During micro-pursuits, gaze direction correlates with a target's smooth, predictable target trajectory. We measure similarity between gaze and target trajectories using a so-called maximally projected correlation and provide results in three experimental data sets. A first observation of micro-pursuit is provided in an implicit pursuit task, where observers were tasked to maintain their gaze fixed on a static cross at the center of screen, while reporting changes in perception of an ambiguous, moving (Necker) cube. We then provide two experimental paradigms and their corresponding data sets: a first replicating micro-pursuits in an explicit pursuit task, where observers had to follow a moving fixation cross (Cross), and a second with an unambiguous square (Square). Individual and group analyses provide evidence that micro-pursuits exist in both the Necker and Cross experiments but not in the Square experiment. The interexperiment analysis results suggest that the manipulation of stimulus target motion, task, and/or the nature of the stimulus may play a role in the generation of micro-pursuits.