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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 com-bined results indicate that microsaccades may be a useful metric of covert attentional processes in applied and ecologically valid settings.

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. References Alexander, R.G., Macknik, S.L., & Martinez-Conde, S. (2018). Microsaccade characteristics in neurological and ophthalmic disease. Frontiers in Neurology, 9:144. Engbert, R. & Kliegl, R. (2003). Microsaccades uncover the orientation of covert attention. Vision Research, 43, 1035–1045. Hafed, Z. M. & Clark, J. J. (2002). Microsaccades as an overt measure of covert attention shifts. Vision Research, 42, 2533–2545. Martinez-Conde, S., Macknik, S.L., & Hubel, D.H. (2004). The role of fixational eye movements in visual perception. Nature Reviews Neuroscience, 5(3), 229-40.

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.

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.

Video stream: https://vimeo.com/365522806 The human ability for visualization extends far beyond the physical items that surround us. We are able to dismiss the constant influx of photons hitting our retinas, and instead picture the layout of our kindergarten classroom, envision the gently swaying palm trees of our dream vacation, or foresee the face of a yet-to-be-born child. As we inspect imaginary objects and people with our mind’s eye, our corporeal eyeballs latch onto the fantasy. Research has found that our eyes can move as if seeing, even when there is nothing to look at. Thus, gaze explorations in the absence of actual vision have been reported in many contexts, including in visualization and memory tasks, and perhaps even during REM sleep. This symposium will present the manifold aspects of gaze dynamics in conditions when the visual input is impoverished or altogether absent. Presentations will address the characteristics of large and small eye movements during imagined and remembered scenes, the impact of visual field deficits on oculomotor control, and the role of eye movements in the future development of neural prosthetics for the blind.

Supported by guidance from training during residency programs, radiologists learn clinically relevant visual features by viewing thousands of medical images. Yet the precise visual features that expert radiologists use in their clinical practice remain unknown. Identifying such features would allow the development of perceptual learning training methods targeted to the optimization of radiology training and the reduction of medical error. Here we review attempts to bridge current gaps in understanding with a focus on computational saliency models that characterize and predict gaze behavior in radiologists. There have been great strides toward the accurate prediction of relevant medical information within images, thereby facilitating the development of novel computer-aided detection and diagnostic tools. In some cases, computational models have achieved equivalent sensitivity to that of radiologists, suggesting that we may be close to identifying the underlying visual representations that radiologists use. However, because the relevant bottom-up features vary across task context and imaging modalities, it will also be necessary to identify relevant top-down factors before perceptual expertise in radiology can be fully understood. Progress along these dimensions will improve the tools available for educating new generations of radiologists, and aid in the detection of medically relevant information, ultimately improving patient health.

Whereas optogenetic techniques have proven successful in their ability to manipulate neuronal populations—with high spatial and temporal fidelity—in species ranging from insects to rodents, significant obstacles remain in their application to nonhuman primates (NHPs). Robust optogenetics-activated behavior and long-term monitoring of target neurons have been challenging in NHPs. Here, we present a method for all-optical interrogation (AOI), integrating optical stimulation and simultaneous two-photon (2P) imaging of neuronal populations in the primary visual cortex (V1) of awake rhesus macaques. A red-shifted channel-rhodopsin transgene (ChR1/VChR1 [C1V1]) and genetically encoded calcium indicators (genetically encoded calmodulin protein [GCaMP]5 or GCaMP6s) were delivered by adeno-associated viruses (AAVs) and subsequently expressed in V1 neuronal populations for months. We achieved optogenetic stimulation using both single-photon (1P) activation of neuronal populations and 2P activation of single cells, while simultaneously recording 2P calcium imaging in awake NHPs. Optogenetic manipulations of V1 neuronal populations produced reliable artificial visual percepts. Together, our advances show the feasibility of precise and stable AOI of cortical neurons in awake NHPs, which may lead to broad applications in high-level cognition and preclinical testing studies., Author summary This report details the first successful application of long-term all-optical interrogation techniques in monkeys. We have overcome obstacles that prevented the combination of single- and two-photon (1P and 2P) optogenetic stimulation with 2P imaging in awake-behaving monkeys, retesting targeted individual cells and neuronal ensembles over periods that extended beyond 6 months. Our strategy results in repeatable primary visual cortex (V1) neuronal stimulation of the same neurons and produces reliable visual percepts, which monkeys report behaviorally in a visual–motor task. The animals’ behavioral responses to their optogenetic-induced perceptions are comparable to their responses to real visual stimulation. These technical advances establish the feasibility of combined long-term optogenetic manipulation and 2P imaging of neocortical neurons in awake-behaving monkeys. Our approach may be applied to investigate the molecular and circuit-level mechanistic pathways that are unique to primate neural function. These methods also provide a roadmap for preclinical testing of human optogenetic therapies and may serve as the basis for optogenetic studies involving sensorimotor functions relevant to human perception, cognition, behavior, and neurological/psychiatric disorders.

Alfred Lukyanovich Yarbus (1914–1986) pioneered the study of stabilized retinal images, miniature eye movements, and the cognitive influences that act on visual scanning. Yarbus’s studies of these different topics have remained fundamentally disconnected and independent of each other, however. In this review, we propose that Yarbus’s various research lines are instead deeply and intrinsically interconnected, as are the small eye movements produced during visual fixation and the large-scale scanning patterns associated with visual exploration of objects and scenes. Such apparently disparate viewing behaviors may represent the extremes of a single continuum of oculomotor performance that operates across spatial scales when we search the visual world.

During attempted visual fixation, small involuntary eye movements –called fixational eye movements--continuously change of our gaze’s position. Disagreement between the left and right eye positions during such motions can produce diplopia (double vision). Thus, the ability to properly coordinate the two eyes during gaze fixation is critical for stable perception. For the last 50 years, researchers have studied the binocular characteristics of fixational eye movements. Here we review classical and recent studies on the binocular coordination (i.e. degree of conjugacy) of each fixational eye movement type: microsaccades, drift and tremor, and its perceptual contribution to increasing or reducing binocular disparity. We also discuss how amblyopia and other visual pathologies affect the binocular coordination of fixational eye movements.

Neurons in primary visual cortex (V1) are frequently classified based on their response linearity: the extent to which their visual responses to drifting gratings resemble a linear replica of the stimulus. This classification is supported by the finding that response linearity is bimodally distributed across neurons in area V1 of anesthetized animals. However, recent studies suggest that such bimodal distribution may not reflect two neuronal types but a nonlinear relationship between the membrane potential and the spike output. A main limitation of these previous studies is that they measured response linearity in anesthetized animals, where the distance between the neuronal membrane potential and the spike threshold is artificially increased by anesthesia. Here, we measured V1 response linearity in the awake brain and its correlation with the neuronal spontaneous firing rate, which is related to the distance between membrane potential and threshold. Our results demonstrate that response linearity is bimodally distributed in awake V1 but that it is poorly correlated with spontaneous firing rate. In contrast, the spontaneous firing rate is best correlated to the response selectivity and response latency to stimuli.

During visual fixation, human eyes are never still. Instead, they constantly produce involuntary "fixational eye movements." Fixational eye movements overcome neural adaptation and prevent visual fading: thus they are an important tool to understand how the brain makes the environment visible. The last decade has seen a growing interest in the analysis of fixational eye movements in humans and primates, as well as in their perceptual and physiological consequences. However, no comprehensive comparison of fixational eye movements across species has been offered. Here we review five decades of fixational eye movement studies in non-human vertebrates, and we discuss the existing evidence concerning their physiological and perceptual effects. We also provide a table that summarizes the physical parameters of the different types of fixational eye movements described in non-human vertebrates.

Artificial scotomas positioned within peripheral dynamic noise fade perceptually during visual fixation (that is, the surrounding dynamic noise appears to fill-in the scotoma). Because the scotomas' edges are continuously refreshed by the dynamic noise background, this filling-in effect cannot be explained by low-level adaptation mechanisms (such as those that may underlie classical Troxler fading). We recently showed that microsaccades counteract Troxler fading and drive first-order visibility during fixation (S. Martinez-Conde, S. L. Macknik, X. G. Troncoso, & T. A. Dyar, 2006). Here we set out to determine whether microsaccades may counteract the perceptual filling-in of artificial scotomas and thus drive second-order visibility. If so, microsaccades may not only counteract low-level adaptation but also play a role in higher perceptual processes. We asked subjects to indicate, via button press/release, whether an artificial scotoma presented on a dynamic noise background was visible or invisible at any given time. The subjects' eye movements were simultaneously measured with a high precision video system. We found that increases in microsaccade production counteracted the perception of filling-in, driving the visibility of the artificial scotoma. Conversely, decreased microsaccades allowed perceptual filling-in to take place. Our results show that microsaccades do not solely overcome low-level adaptation mechanisms but they also contribute to maintaining second-order visibility during fixation.

The Alternating Brightness Star (ABS) is an illusion that provides insight into the relationship between brightness perception and corner angle. Recent psychophysical studies of this illusion have shown that corner salience varies parametrically with corner angle, with sharp angles leading to strong illusory percepts and shallow angles leading to weak percepts. It is hypothesized that the illusory effects arise because of an interaction between surface corners and the shape of visual receptive fields: sharp surface corners may create hotspots of high local contrast due to processing by center–surround and other early receptive fields. If this hypothesis is correct, early visual neurons should respond powerfully to sharp corners and curved portions of surface edges. Indeed, the primary role of early visual neurons may be to localize the discontinuities along the edges of surfaces. If so, all early visual areas should show greater BOLD responses to sharp corners than to shallow corners. On the other hand, if corner processing is exclusively constrained to certain areas of the brain, only those specific areas will show greater responses to sharp vs shallow corners. To address this we explored the BOLD correlates of the ABS illusion in the human visual cortex using fMRI. We found that BOLD signal varies parametrically with corner angle throughout the visual cortex, offering the first neurophysiological correlates of the ABS illusion. This finding provides a neurophysiological basis for the previously reported psychophysical data that showed that corner salience varied parametrically with corner angle. We propose that all early visual areas localize discontinuities along the edges of surfaces, and that specific cortical corner-processing circuits further establish the specific nature of those discontinuities, such as their orientation.

Vasarely's ‘nested-squares’ illusion shows that 90° corners can be more salient perceptually than straight edges. On the basis of this illusion we have developed a novel visual illusion, the ‘Alternating Brightness Star’, which shows that sharp corners are more salient than shallow corners (an effect we call ‘corner angle salience variation’) and that the same corner can be perceived as either bright or dark depending on the polarity of the angle (ie whether concave or convex: ‘corner angle brightness reversal’). Here we quantify the perception of corner angle salience variation and corner angle brightness reversal effects in twelve naive human subjects, in a two-alternative forced-choice brightness discrimination task. The results show that sharp corners generate stronger percepts than shallow corners, and that corner gradients appear bright or dark depending on whether the corner is concave or convex. Basic computational models of center – surround receptive fields predict the results to some degree, but not fully.

During attempted visual fixation, saccades of a range of sizes occur. These "fixational saccades" include microsaccades, which are not apparent in regular clinical tests, and "saccadic intrusions", predominantly horizontal saccades that interrupt accurate fixation. Square-wave jerks (SWJs), the most common type of saccadic intrusion, consist of an initial saccade away from the target followed, after a short delay, by a "return saccade" that brings the eye back onto target. SWJs are present in most human subjects, but are prominent by their increased frequency and size in certain parkinsonian disorders and in recessive, hereditary spinocerebellar ataxias. Here we asked whether fixational saccades showed distinctive features in various parkinsonian disorders and in recessive ataxia. Although some saccadic properties differed between patient groups, in all conditions larger saccades were more likely to form SWJs, and the intervals between the first and second saccade of SWJs were similar. These findings support the proposal of a common oculomotor mechanism that generates all fixational saccades, including microsaccades and SWJs. The same mechanism also explains how the return saccade in SWJs is triggered by the position error that occurs when the first saccadic component is large, both in the healthy brain and in neurological disease.

International audience; Our eyes move constantly, even when we try to fixate our gaze. Fixational eye movements prevent and restore visual loss during fixation, yet the relative impact of each type of fixational eye movement remains controversial. For over five decades, the debate has focused on microsaccades, the fastest and largest fixational eye movements. Some recent studies have concluded that microsaccades counteract visual fading during fixation. Other studies have disputed this idea, contending that microsaccades play no significant role in vision. The disagreement stems from the lack of methods to determine the precise effects of microsaccades on vision versus those of other eye movements, as well as a lack of evidence that microsaccades are relevant to foveal vision. Here we developed a novel generalized method to determine the precise quantified contribution and efficacy of human microsaccades to restoring visibility compared with other eye movements. Our results indicate that microsaccades are the greatest eye movement contributor to the restoration of both foveal and peripheral vision during fixation. Our method to calculate the efficacy and contribution of microsaccades to perception can determine the strength of connection between any two physiological and/or perceptual events, providing a novel and powerful estimate of causal influence; thus, we anticipate wide-ranging applications in neuroscience and beyond.

Certain repetitive arrangements of luminance gradients elicit the perception of strong illusory motion. Among them, the “Rotating Snakes Illusion” has generated a large amount of interest in the visual neurosciences, as well as in the public. Prior evidence indicates that the Rotating Snakes illusion depends critically on eye movements, yet the specific eye movement types involved and their associated neural mechanisms remain controversial. According to recent reports, slow ocular drift—a nonsaccadic type of fixational eye movement—drives the illusion, whereas microsaccades produced during attempted fixation fail to do so. Here, we asked human subjects to indicate the presence or absence of rotation during the observation of the illusion while we simultaneously recorded their eye movements with high precision. We found a strong quantitative link between microsaccade and blink production and illusory rotation. These results suggest that transient oculomotor events such as microsaccades, saccades, and blinks, rather than continuous drift, act to trigger the illusory motion in the Rotating Snakes illusion.

The eyes do not stay perfectly still during attempted fixation; fixational eye movements and saccadic intrusions (SIs) continuously change the position of gaze. The most common type of SI, square-wave jerks (SWJs), consists of saccade pairs that appear purely horizontal on clinical inspection: the first saccade moves the eye away from the fixation target, and after a short interval, the second saccade brings it back toward the target. SWJs are prevalent in certain neurological disorders, including progressive supranuclear palsy (PSP). Here, we developed an objective method to identify SWJs. We found that SWJs are more frequent, larger, and more markedly horizontal in PSP patients than in healthy human subjects. Furthermore, the loss of a vertical component in fixational saccades and SWJs was the eye movement feature that best distinguished PSP patients from controls. We moreover determined that, in PSP patients and controls, the larger the saccade the more likely it was part of a SWJ. Furthermore, saccades produced by PSP patients had equivalent properties whether they were part of a SWJ or not, suggesting that normal fixational saccades (microsaccades) are rare in PSP. We propose that fixational saccades and SIs are generated by the same neural circuit and that, both in PSP patients and in controls, SWJs result from a coupling mechanism that generates a second corrective saccade shortly after a large fixation saccade. Because of brainstem and/or cerebellum impairment, fixational saccades in PSP are abnormally large and thus more likely to trigger a corrective saccade, giving rise to SWJs.

Microsaccades are known to occur during prolonged visual fixation, but it is a matter of controversy whether they also happen during free-viewing. Here we set out to determine: 1) whether microsaccades occur during free visual exploration and visual search, 2) whether microsaccade dynamics vary as a function of visual stimulation and viewing task, and 3) whether saccades and microsaccades share characteristics that might argue in favor of a common saccade-microsaccade oculomotor generator. Human subjects viewed naturalistic stimuli while performing various viewing tasks, including visual exploration, visual search, and prolonged visual fixation. Their eye movements were simultaneously recorded with high precision. Our results show that microsaccades are produced during the fixation periods that occur during visual exploration and visual search. Microsaccade dynamics during free-viewing moreover varied as a function of visual stimulation and viewing task, with increasingly demanding tasks resulting in increased microsaccade production. Moreover, saccades and microsaccades had comparable spatiotemporal characteristics, including the presence of equivalent refractory periods between all pair-wise combinations of saccades and microsaccades. Thus our results indicate a microsaccade-saccade continuum and support the hypothesis of a common oculomotor generator for saccades and microsaccades.

SummaryOur eyes move continually, even while we fixate our gaze on an object. If fixational eye movements are counteracted, our perception of stationary objects fades completely, due to neural adaptation. Some studies have suggested that fixational microsaccades refresh retinal images, thereby preventing adaptation and fading. However, other studies disagree, and so the role of microsaccades remains unclear. Here, we correlate visibility during fixation to the occurrence of microsaccades. We asked subjects to indicate when Troxler fading of a peripheral target occurs, while simultaneously recording their eye movements with high precision. We found that before a fading period, the probability, rate, and magnitude of microsaccades decreased. Before transitions toward visibility, the probability, rate, and magnitude of microsaccades increased. These results reveal a direct link between suppression of microsaccades and fading and suggest a causal relationship between microsaccade production and target visibility during fixation.