J. Eye Mov. Res., Volume 12, Issue 6 (October 2019) – 15 articles

Recent technical developments and increased affordability of high-speed eye tracking devices have brought microsaccades to the forefront of research in many areas of sensory, perceptual, and cognitive processes. The present thematic issue on “Microsaccades: Empirical Research and Methodological Advances” invited authors to submit original research and reviews encompassing measurements and data analyses in fundamental, translational, and applied studies. We present the first volume of this special issue, comprising 14 articles by research teams around the world. Contributions include the characterization of fixational eye movements and saccadic intrusions in neurological impairments and in visual disease, methodological developments in microsaccade detection, the measurement of fixational eye movements in applied and ecological scenarios, and advances in the current understanding of the relationship between microsaccades and cognition. When fundamental research on microsaccades experienced a renaissance at the turn of the millennium (c.f. Martinez-Conde, Macknik, & Hubel, 2004), one could hardly have been so bold as to predict the manifold applications of research on fixational eye movements in clinic and practice. Through this great variety of areas of focus, some main topics emerge. One such theme is the applicability of microsaccade measures to neurological and visual disease. Whereas microsaccade quantifications have been largely limited to participants with intact visual and oculomotor systems, recent research has extended this interest into the realm of neural and ophthalmic impairment (see Alexander, Macknik, & Martinez-Conde, 2018, for a review). In this volume, Becker et al. analyze “Saccadic intrusions in amyotrophic lateral sclerosis (ALS)” and Kang et al. study “Fixational eye movement waveforms in amblyopia”, delving into the characteristics of fast and slow eye movements. Two other articles focus on how the degradation of visual information, which is relevant to many ophthalmic pathologies, affects microsaccadic features. Tang et al. investigate the “Effects of visual blur on microsaccades on visual exploration” and conclude that the precision of an image on the fovea plays an important role in the calibration of microsaccade amplitudes during visual scanning. Otero-Millan et al. use different kinds of visual stimuli and viewing tasks in the presence or absence of simulated scotomas, to determine the contributions of foveal and peripheral visual information to microsaccade production. They conclude that “Microsaccade generation requires a foveal anchor”. The link between microsaccadic characteristics and cognitive processes has been a mainstay of microsaccade research for almost two decades, since studies in the early 2000s connected microsaccade directions to the spatial location of covert attentional cues (Engbert & Kliegl, 2003; Hafed & Clark, 2002). In the present volume, Dalmaso et al. report that “Anticipation of cognitive conflict is reflected in microsaccades”, providing new insights about the top-down modulation of microsaccade dynamics. Ryan et al. further examine the relationship between “Microsaccades and covert attention” during the performance of a continuous, divided-attention task, and find preliminary evidence that microsaccades track the ongoing allocation of spatial attention. Krueger et al. discover that microsaccade rates modulate with visual attention demands and report that “Microsaccades distinguish looking from seeing”. Taking the ecological validity of microsaccade investigations one step further, Barnhart et al. evaluate microsaccades during the observation of magic tricks and conclude that “Microsaccades reflect the dynamics of misdirected attention in magic”. Two articles examine the role of individual differences and intraindividual variability over time on microsaccadic features. In “Reliability and correlates of intra-individual variability in the oculomotor system” Perquin and Bompas find evidence for intra-individual reliability over different time points, while cautioning that its use to classify self-reported individual differences remains unclear. Stafford et al. provide a counterpoint in “Can microsaccade rate predict drug response?” by supporting the use of microsaccade occurrence as both a trait measure of individual differences and as a state measure of response to caffeine administration. Methodological and technical advances are the subjects of three papers in this volume. In “Motion tracking of iris features to detect small eye movements” Chaudhary and Pelz describe a new video-based eye tracking methodology that relies on higher-order iris texture features, rather than on lower-order pupil center and corneal reflection features, to detect microsaccades with high confidence. Munz et al. present an open source visual analytics system called “VisME: Visual microsaccades explorer” that allows users to interactively vary microsaccade filter parameters and evaluate the resulting effects on microsaccade behavior, with the goal of promoting reproducibility in data analyses. In “What makes a microsaccade? A review of 70 years research prompts a new detection method” Hauperich et al. review the microsaccade properties reported between the 1940s and today, and use the stated range of parameters to develop a novel method of microsaccade detection. Lastly, Alexander et al. switch the focus from the past of microsaccade research to its future, by discussing the recent and upcoming applications of fixational eye movements to ecologically-valid and real-world scenarios. Their review “Microsaccades in applied environments: real-world applications of fixational eye movement measurements” covers the possibilities and challenges of taking microsaccade measurements out of the lab and into the field. Microsaccades have engaged the interest of scientists from different backgrounds and disciplines for many decades and will certainly continue to do so. One reason for this fascination might be microsaccades’ role as a link between basic sensory processes and high-level cognitive phenomena, making them an attractive focus of interdisciplinary research and transdisciplinary applications. Thus, research on microsaccades will not only endure, but keep evolving as the present knowledge base expands. Part 2 of the special issue on microsaccades is already in progress with articles currently under review and will be published in 2021. Full article

Visual scene characteristics can affect various aspects of saccade and microsaccade dynamics. For example, blank visual scenes are known to elicit diminished saccade and microsaccade production, compared to natural scenes. Similarly, microsaccades are less frequent in the dark. Yet, the extent to which foveal versus peripheral visual information contribute to microsaccade production remains unclear: because microsaccade directions are biased towards covert attention locations, it follows that peripheral visual stimulation could suffice to produce regular microsaccade dynamics, even without foveal stimulation being present. Here we determined the characteristics of microsaccades as a function of foveal and/or peripheral visual stimulation, while human subjects conducted four types of oculomotor tasks (fixation, free viewing, guided viewing and passive viewing). Foveal information was either available, or made unavailable, by the presentation of simulated scotomas. We found foveal stimulation to be critical for microsaccade production, and peripheral stimulation, by itself, to be insufficient to yield normal microsaccades. In each oculomotor task, microsaccade production decreased when scotomas blocked foveal stimulation. Across comparable foveal stimulation conditions, the type of peripheral stimulation (static versus dynamic) moreover affected microsaccade production, with dynamic backgrounds resulting in lower microsaccadic rates than static backgrounds. These results indicate that a foveal visual anchor is necessary for normal microsaccade generation. Whereas peripheral visual stimulation, on its own, does not suffice for normal microsaccade production, it can nevertheless modulate microsaccadic characteristics. These findings extend our current understanding of the links between visual input and ocular motor control, and may therefore help improve the diagnosis and treatment of ophthalmic conditions that degrade central vision, such as age-related macular degeneration. Full article

Across a wide variety of research environments, the recording of microsaccades and other fixational eye movements has provided insight and solutions into practical problems. Here we review the literature on fixational eye movements—especially microsaccades—in applied and ecologically-valid scenarios. Recent technical advances allow noninvasive fixational eye movement recordings in real-world contexts, while observers perform a variety of tasks. Thus, fixational eye movement measures have been obtained in a host of real-world scenarios, such as in connection with driver fatigue, vestibular sensory deprivation in astronauts, and elite athletic training, among others. Here we present the state of the art in the practical applications of fixational eye movement research, examine its potential future uses, and discuss the benefits of including microsaccade measures in existing eye movement detection technologies. Current evidence supports the inclusion of fixational eye movement measures in real-world contexts, as part of the development of new or improved oculomotor assessment tools. The real-world applications of fixational eye movement measurements will only grow larger and wider as affordable high-speed and high-spatial resolution eye trackers become increasingly prevalent. Full article

A new method for detecting microsaccades in eye-movement data is presented, following a review of reported microsaccade properties between the 1940s and today. The review focuses on the parameter ranges within which certain physical markers of microsaccades are thought to occur, as well as any features of microsaccades that have been stably reported over time. One feature of microsaccades, their binocularity, drives the new microsaccade detection method. The binocular correlation method for microsaccade detection is validated on two datasets of binocular eye-movements recorded using video-based systems: one collected as part of this study, and one from Nyström et al., 2017. Comparisons between detection methods are made using precision-recall statistics. This confirms that the binocular correlation method performs well when compared to manual coders and performs favourably compared to the commonly used Engbert & Kliegl (2003) method with subsequent modifications (Engbert & Mergenthaler, 2006). The binocular correlation microsaccade detection method is easy to implement and MATLAB code is made available to download. Full article

This work presents a visual analytics approach to explore microsaccade distributions in high-frequency eye tracking data. Research studies often apply filter algorithms and parameter values for microsaccade detection. Even when the same algorithms are employed, different parameter values might be adopted across different studies. In this paper, we present a visual analytics system (VisME) to promote reproducibility in the data analysis of microsaccades. It allows users to interactively vary the parametric values for microsaccade filters and evaluate the resulting influence on microsaccade behavior across individuals and on a group level. In particular, we exploit brushing-and-linking techniques that allow the microsaccadic properties of space, time, and movement direction to be extracted, visualized, and compared across multiple views. We demonstrate in a case study the use of our visual analytics system on data sets collected from natural scene viewing and show in a qualitative usability study the usefulness of this approach for eye tracking researchers. We believe that interactive tools such as VisME will promote greater transparency in eye movement research by providing researchers with the ability to easily understand complex eye tracking data sets; such tools can also serve as teaching systems. VisME is provided as open source software. Full article

In 22 human subjects we measured microsaccade count across 60 brief fixation trials both pre- and post- administration of 300 mg of caffeine. There was a statistically significant reduction in average microsaccade count post-caffeine administration, with a moderate effect size (Cohen’s d of 0.42). Microsaccade count was stable within individuals across time points (Pearson’s r of 0.89). Sensitivity analysis suggests that the pre/post caffeine effect size is robust to choice of parameters used to identify microsaccades. Bootstrap resampling suggests that both the pre/post-caffeine difference and the across-time stability within individuals could be reliably assessed with far fewer trials. The results support the use of microsaccade count as both a trait measure of individual differences and a state measure of caffeine response. We discuss the results in the context of the theory that the superior colliculus is central to the generation of microsaccades and hence that microsaccade rate may be a useful assay for at least some drug-induced changes at the level of the colliculus: a potentially useful tool in the development of therapies for disorders that may involve collicular dysfunction such as ADHD. Full article

Even if all external circumstances are kept equal, the oculomotor system shows intraindividual variability over time, affecting measures such as microsaccade rate, blink rate, pupil size, and gaze position. Recently, some of these measures have been associated with ADHD on a between-subject level. However, it remains unclear to what extent these measures constitute stable individual traits. In the current study, we investigate the intraindividual reliability of these oculomotor features. Combining results over three experiments (>100 healthy participants), we find that most measures show good intra-individual reliability over different time points (repeatability) as well as over different conditions (generalisation). However, we find evidence against any correlation with self-assessed ADHD tendencies, mind wandering, and impulsivity. As such, the oculomotor system shows reliable intra-individual reliability, but its benefit for investigating self-assessed individual differences in healthy subjects remains unclear. With our results, we highlight the importance of reliability and statistical power when studying between-subject differences. Full article

The attempt to quietly fixate at a small visual object is continuously interrupted by a variety of fixational eye movements comprising, among others, a continuum of saccadic intrusions (SI) which range in size from microsaccades with amplitudes ≤0.25° to larger refixation saccades of up to about 2°. The size and frequency of SI varies considerably among individuals and is known to increase in neurodegenerative diseases such as progressive supranuclear palsy (PSP), and amyotrophic lateral sclerosis (ALS). However, studies of ALS disagree whether also the frequency of SI increases. We undertook an analysis of SI in 119 ALS patients and 47 age-matched healthy controls whose eye movements during fixation and tests of executive functions (e.g., antisaccades) had been recorded by video-oculography according to standardised procedures. SI were categorised according to their spatio-temporal patterns as stair case, back-and-forth and square wave jerks (a subcategory of back-and-forth). The SI of patients and controls were qualitatively similar (same direction preferences, similar differences between patterns), but were enlarged in ALS. Notably however, no increase of SI frequency could be demonstrated. Yet, there were clear correlations with parameters such as eye blink rate or errors in a delayed saccade task that suggest an impairment of inhibitory mechanisms, in keeping with the notion of a frontal dysfunction in ALS. However, it remains unclear how the impairment of inhibitory mechanisms in ALS could selectively increase the amplitude of intrusions without changing their frequency of occurrence. Full article

Microsaccades shift the image on the fovea and counteract visual fading. They also serve as an optimal sampling strategy while viewing complex visual scenes. Microsaccade production relies on the amount of retinal error or acuity demand of a visual task. The goal of this study was to assess the effects of blur induced by uncorrected refractive error on visual search. Eye movements were recorded in fourteen healthy subjects with uncorrected and corrected refractive error while they performed (a) visual fixation (b) blankscene viewing (c) visual search (spot the difference) tasks. Microsaccades, saccades, correctly identified differences and reaction times were analyzed. The frequency of microsaccades and correctly identified differences were lower in the uncorrected refractive error during visual search. No similar change in microsaccades was seen during blank-scene viewing and gaze holding tasks. These findings suggest that visual blur, hence the precision of an image on the fovea, has an important role in calibrating the amplitude of microsaccades during visual scanning. Full article

Fixational eye movements comprise of fast microsaccades alternating with slow intersaccadic drifts. These physiologic eye movements play an important role in visual perception. Amblyopic patients are known to have fixation instability, particularly of the amblyopic eye. We examined eye movement abnormalities that contribute to this instability. We found that fixation stability is affected by the presence of fusion maldevelopment nystagmus (FMN). However, some amblyopes can have nystagmus without nasally directed slow phases and reversal in direction of the quick phase on ocular occlusion, features seen in FMN. In patients without nystagmus, we found increased amplitude of fixational saccades and inter-saccadic drifts. We categorized amblyopia patients by type (anisometropic, strabismic, or mixed) and eye movement waveform (no nystagmus, nystagmus without FMN, and FMN). We found specific fast and slow eye movement abnormalities of the fellow and amblyopic eye during fellow, amblyopic and both eyes viewing conditions across eye movement waveforms and types of amblyopia. These eye movement abnormalities can serve as biomarkers that can predict the impact of amblyopia as measured by visual acuity and stereopsis. Evaluation of fixational eye movements in amblyopia could be important to diagnose these common eye diseases and predict treatment effectiveness. Full article

The methods of magicians provide powerful tools for enhancing the ecological validity of laboratory studies of attention. The current research borrows a technique from magic to explore the relationship between microsaccades and covert attention under near-natural viewing conditions. We monitored participants’ eye movements as they viewed a magic trick where a coin placed beneath a napkin vanishes and reappears beneath another napkin. Many participants fail to see the coin move from one location to the other the first time around, thanks to the magician’s misdirection. However, previous research was unable to distinguish whether or not participants were fooled based on their eye movements. Here, we set out to determine if microsaccades may provide a window into the efficacy of the magician’s misdirection. In a multi-trial setting, participants monitored the location of the coin (which changed positions in half of the trials), while engaging in a delayed match-to-sample task at a different spatial location. Microsaccades onset times varied with task difficulty, and microsaccade directions indexed the locus of covert attention. Our combined results indicate that microsaccades may be a useful metric of covert attentional processes in applied and ecologically valid settings. Full article

A substantial question in understanding expert behavior is isolating where experts look, and which aspects of their environment they process. While tracking the position of gaze provides some insight into this process, our ability to attend covertly to regions of space other than the current point of fixation, severely limits the diagnostic power of such data. Over the past decade, evidence has emerged suggesting that microscopic eye movements present during periods of fixation may be linked to the spatial distribution of covert attention, potentially offering a powerful tool for studying expert behavior. To date, the majority of studies in this field have tested the link under the constraints of a trial by trial, forced-response task. In the current study we sought to examine the effect when participants performed a continuous, divided-attention task, with the hope of bridging the gap to a range of more ecological, real-world tasks. We report various aspects of the eye movement and response data including (i) the relationship between microsaccades and drift correction, (ii) response behavior in brief time periods immediately following a microsaccade, (iii) response behavior briefly preceding a microsaccade. Analysis failed to reveal a link between task accuracy and the direction of a microsaccade. Most striking however, we found evidence for a timelocked relationship between the side of space responded to and the direction of the most recent microsaccade. The paper hence provides preliminary evidence that microsaccades may indeed be used to track the ongoing allocation of spatial attention. Full article

Understanding our visual world requires both looking and seeing. Dissociation of these processes can result in the phenomenon of inattentional blindness or ‘looking without seeing’. Concomitant errors in applied settings can be serious, and even deadly. Current visual data analysis cannot differentiate between just ‘looking’ and actual processing of visual information, i.e., ‘seeing’. Differentiation may be possible through the examination of microsaccades; the involuntary, small-magnitude saccadic eye movements that occur during processed visual fixation. Recent work has suggested that microsaccades are post-attentional biosignals, potentially modulated by task. Specifically, microsaccade rates decrease with increased mental task demand, and increase with growing visual task difficulty. Such findings imply that there are fundamental differences in microsaccadic activity between visual and nonvisual tasks. To evaluate this proposition, we used a high-speed eye tracker to record participants in looking for differences between two images or, doing mental arithmetic, or both tasks in combination. Results showed that microsaccade rate was significantly increased in conditions that require high visual attention, and decreased in conditions that require less visual attention. The results support microsaccadic rate reflecting visual attention, and level of visual information processing. A measure that reflects to what extent and how an operator is processing visual information represents a critical step for the application of sophisticated visual assessment to real world tasks. Full article

The inability of current video-based eye trackers to reliably detect very small eye movements has led to confusion about the prevalence or even the existence of monocular microsaccades (small, rapid eye movements that occur in only one eye at a time). As current methods often rely on precisely localizing the pupil and/or corneal reflection on successive frames, current microsaccade-detection algorithms often suffer from signal artifacts and a low signal-to-noise ratio. We describe a new video-based eye tracking methodology which can reliably detect small eye movements over 0.2 degrees (12 arcmins) with very high confidence. Our method tracks the motion of iris features to estimate velocity rather than position, yielding a better record of microsaccades. We provide a more robust, detailed record of miniature eye movements by relying on more stable, higher-order features (such as local features of iris texture) instead of lower-order features (such as pupil center and corneal reflection), which are sensitive to noise and drift. Full article

Microsaccade frequency has recently been shown to be sensitive to high-level cognitive processes such as attention and memory. In the present study we explored the effects of anticipated cognitive conflict. Participants were administered a variant of the flanker task, which is known to elicit cognitive interference. At the beginning of each trial, participants received a colour cue providing information about the upcoming target frame. In two thirds of the trials, the cue reliably informed the participants that in the upcoming trial the flankers either matched the central target letter or not. Hence, participants could accurately anticipate whether cognitive conflict would arise or not. On neutral trials, the cue provided no useful information. The results showed that microsaccadic rate time-locked to cue onset was reduced on trials in which an upcoming cognitive conflict was expected. These findings provide new insights about top-down modulations of microsaccade dynamics. Full article