Microsaccadic Eye Movements Research Articles

Microsaccade behavior associated with inhibitory control in athletes in the antisaccade task.

The ability to achieve a state of readiness before upcoming tasks, known as a preparatory set, is critical for athletic performance. Here, we investigated these preparatory processes associated with inhibitory control using the anti-saccade paradigm, in which participants are instructed, prior to target appearance, either to automatically look at the target (pro-saccade) or to suppress this automatic response and intentionally look in the opposite direction (anti-saccade). We focused on microsaccadic eye movements that happen before the response saccade in either pro- or anti-saccade tasks, as these microsaccades reflect ongoing preparatory processes during saccade planning before execution. We hypothesized that athletes, compared to non-athletes, would demonstrate better preparation, given research generally indicating higher inhibitory control in athletes. Our findings showed that microsaccade rates decreased before target appearance, with lower rates observed during anti-saccade preparation compared to pro-saccade preparation. However, microsaccade rates and metrics did not differ significantly between athletes and non-athletes. Moreover, reduced microsaccade rates were associated with improved task performance in non-athletes, leading to higher accuracy and faster saccade reaction times (SRTs) in trials without microsaccades. For athletes, only SRTs were affected by microsaccade occurrence. Moreover, the modulation of microsaccadic inhibition on accuracy was more pronounced in non-athletes compared to athletes, though this effect was only marginally significant. In conclusion, while microsaccade responses were modulated by task preparation, differences between athletes and non-athletes were non-significant. These findings, for the first time, highlight the potential of using microsaccades as an online objective index to study preparatory sets in sports science research.

About the Possibility of Using Fixation Microsaccades to Improve the Quality of Visible Images in the Foveal Zone

The article is devoted to the description and analysis of a computer model that was created by D. S. Lebedev to demonstrate the possibility of a positive effect of fixation microsaccadic eye movements on the perception of small stimuli. The model is based on the assumption that in the process of fixing the gaze on the test stimulus, several “neural images” of this stimulus, resulting from microsaccades, are summed up in the brain. The series of summed neural images correspond to a sequence of shifted positions of the optical image of a stimulus on the retina. To accurately superimpose neural images on each other, a mechanism for compensating fixation saccadic microshifts is introduced into the model, identical to the mechanism that ensures the constancy of spatial perception in the case of macrosaccades, i.e. when turning the eyes to view large objects or scenes. The author of the model assessed the possibility of improving the quality of visible images by increasing the signal-to-noise ratio, which can be achieved using realistic spatiotemporal parameters of test images, neural noise and eye micromovements, selected bу means of literature analysis. Results of model calculation obtained for the specific parameters of the retina and eye movements showed that the considered summation mechanism with compensation for saccadic shifts can progressively improve the quality of visible test stimuli when the number of summed neural images increases to approximately seven or eight, after which the positive effect practically does not increase. In this article, based on the material of recordings of eye movements in relevant experiments, the degree of realism of this model is discussed.

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.

Microsaccadic Eye Movements but not Pupillary Dilation Response Characterizes the Crossmodal Freezing Effect.

In typical spatial orienting tasks, the perception of crossmodal (e.g., audiovisual) stimuli evokes greater pupil dilation and microsaccade inhibition than unisensory stimuli (e.g., visual). The characteristic pupil dilation and microsaccade inhibition has been observed in response to “salient” events/stimuli. Although the “saliency” account is appealing in the spatial domain, whether this occurs in the temporal context remains largely unknown. Here, in a brief temporal scale (within 1 s) and with the working mechanism of involuntary temporal attention, we investigated how eye metric characteristics reflect the temporal dynamics of perceptual organization, with and without multisensory integration. We adopted the crossmodal freezing paradigm using the classical Ternus apparent motion. Results showed that synchronous beeps biased the perceptual report for group motion and triggered the prolonged sound-induced oculomotor inhibition (OMI), whereas the sound-induced OMI was not obvious in a crossmodal task-free scenario (visual localization without audiovisual integration). A general pupil dilation response was observed in the presence of sounds in both visual Ternus motion categorization and visual localization tasks. This study provides the first empirical account of crossmodal integration by capturing microsaccades within a brief temporal scale; OMI but not pupillary dilation response characterizes task-specific audiovisual integration (shown by the crossmodal freezing effect).

How is visual salience computed in the brain? Insights from behaviour, neurobiology and modelling

Inherent in visual scene analysis is a bottleneck associated with the need to sequentially sample locations with foveating eye movements. The concept of a ‘saliency map’ topographically encoding stimulus conspicuity over the visual scene has proven to be an efficient predictor of eye movements. Our work reviews insights into the neurobiological implementation of visual salience computation. We start by summarizing the role that different visual brain areas play in salience computation, whether at the level of feature analysis for bottom-up salience or at the level of goal-directed priority maps for output behaviour. We then delve into how a subcortical structure, the superior colliculus (SC), participates in salience computation. The SC represents a visual saliency map via a centre-surround inhibition mechanism in the superficial layers, which feeds into priority selection mechanisms in the deeper layers, thereby affecting saccadic and microsaccadic eye movements. Lateral interactions in the local SC circuit are particularly important for controlling active populations of neurons. This, in turn, might help explain long-range effects, such as those of peripheral cues on tiny microsaccades. Finally, we show how a combination of in vitro neurophysiology and large-scale computational modelling is able to clarify how salience computation is implemented in the local circuit of the SC.This article is part of the themed issue ‘Auditory and visual scene analysis’.

Alteration of the microsaccadic velocity-amplitude main sequence relationship after visual transients: implications for models of saccade control.

Microsaccades occur during gaze fixation to correct for miniscule foveal motor errors. The mechanisms governing such fine oculomotor control are still not fully understood. In this study, we explored microsaccade control by analyzing the impacts of transient visual stimuli on these movements' kinematics. We found that such kinematics can be altered in systematic ways depending on the timing and spatial geometry of visual transients relative to the movement goals. In two male rhesus macaques, we presented peripheral or foveal visual transients during an otherwise stable period of fixation. Such transients resulted in well-known reductions in microsaccade frequency, and our goal was to investigate whether microsaccade kinematics would additionally be altered. We found that both microsaccade timing and amplitude were modulated by the visual transients, and in predictable manners by these transients' timing and geometry. Interestingly, modulations in the peak velocity of the same movements were not proportional to the observed amplitude modulations, suggesting a violation of the well-known "main sequence" relationship between microsaccade amplitude and peak velocity. We hypothesize that visual stimulation during movement preparation affects not only the saccadic "Go" system driving eye movements but also a "Pause" system inhibiting them. If the Pause system happens to be already turned off despite the new visual input, movement kinematics can be altered by the readout of additional visually evoked spikes in the Go system coding for the flash location. Our results demonstrate precise control over individual microscopic saccades and provide testable hypotheses for mechanisms of saccade control in general.NEW & NOTEWORTHY Microsaccadic eye movements play an important role in several aspects of visual perception and cognition. However, the mechanisms for microsaccade control are still not fully understood. We found that microsaccade kinematics can be altered in a systematic manner by visual transients, revealing a previously unappreciated and exquisite level of control by the oculomotor system of even the smallest saccades. Our results suggest precise temporal interaction between visual, motor, and inhibitory signals in microsaccade control.

Evaluation of the Tobii EyeX Eye tracking controller and Matlab toolkit for research

The Tobii Eyex Controller is a new low-cost binocular eye tracker marketed for integration in gaming and consumer applications. The manufacturers claim that the system was conceived for natural eye gaze interaction, does not require continuous recalibration, and allows moderate head movements. The Controller is provided with a SDK to foster the development of new eye tracking applications. We review the characteristics of the device for its possible use in scientific research. We develop and evaluate an open source Matlab Toolkit that can be employed to interface with the EyeX device for gaze recording in behavioral experiments. The Toolkit provides calibration procedures tailored to both binocular and monocular experiments, as well as procedures to evaluate other eye tracking devices. The observed performance of the EyeX (i.e. accuracy < 0.6°, precision < 0.25°, latency < 50 ms and sampling frequency ≈55 Hz), is sufficient for some classes of research application. The device can be successfully employed to measure fixation parameters, saccadic, smooth pursuit and vergence eye movements. However, the relatively low sampling rate and moderate precision limit the suitability of the EyeX for monitoring micro-saccadic eye movements or for real-time gaze-contingent stimulus control. For these applications, research grade, high-cost eye tracking technology may still be necessary. Therefore, despite its limitations with respect to high-end devices, the EyeX has the potential to further the dissemination of eye tracking technology to a broad audience, and could be a valuable asset in consumer and gaming applications as well as a subset of basic and clinical research settings.

The effect of speed of processing training on microsaccade amplitude.

Older adults experience cognitive deficits that can lead to driving errors and a loss of mobility. Fortunately, some of these deficits can be ameliorated with targeted interventions which improve the speed and accuracy of simultaneous attention to a central and a peripheral stimulus called Speed of Processing training. To date, the mechanisms behind this effective training are unknown. We hypothesized that one potential mechanism underlying this training is a change in distribution of eye movements of different amplitudes. Microsaccades are small amplitude eye movements made when fixating on a stimulus, and are thought to counteract the “visual fading” that occurs when static stimuli are presented. Due to retinal anatomy, larger microsaccadic eye movements are needed to move a peripheral stimulus between receptive fields and counteract visual fading. Alternatively, larger microsaccades may decrease performance due to neural suppression. Because larger microsaccades could aid or hinder peripheral vision, we examine the distribution of microsaccades during stimulus presentation. Our results indicate that there is no statistically significant change in the proportion of large amplitude microsaccades during a Useful Field of View-like task after training in a small sample of older adults. Speed of Processing training does not appear to result in changes in microsaccade amplitude, suggesting that the mechanism underlying Speed of Processing training is unlikely to rely on microsaccades.

The characteristics of microsaccadic eye movements varied with the change of strategy in a match-to-sample task.

The characteristics of microsaccadic eye movements varied with the change of strategy in a match-to-sample task.

Bayesian selection of Markov models for symbol sequences: application to microsaccadic eye movements.

Complex biological dynamics often generate sequences of discrete events which can be described as a Markov process. The order of the underlying Markovian stochastic process is fundamental for characterizing statistical dependencies within sequences. As an example for this class of biological systems, we investigate the Markov order of sequences of microsaccadic eye movements from human observers. We calculate the integrated likelihood of a given sequence for various orders of the Markov process and use this in a Bayesian framework for statistical inference on the Markov order. Our analysis shows that data from most participants are best explained by a first-order Markov process. This is compatible with recent findings of a statistical coupling of subsequent microsaccade orientations. Our method might prove to be useful for a broad class of biological systems.

Effect of image statistics on fixational eye movements

Under natural viewing conditions, small movements of the eyes prevent the maintenance of a steady direction of gaze. It is unclear how the spatiotemporal content of the fixated scene has an impact on the properties of miniatures, fixational eye movements. We have investigated the characteristics of fixational eye movements recorded while human subjects are instructed to fixate natural statistics random textures (Motion Clouds) in which we manipulated the spatial frequency content. We used long presentations (5 sec) of Motion Clouds stimuli (Schrater et al. 2000) of varying spatial frequency bandwidths (Bsf) around different central spatial frequency (Sf0). We found that central spatial frequency has an effect upon microsaccadic eye movements. In particular, smaller saccadic amplitudes were associated with high spatial frequencies, and larger saccades with low spatial frequencies. Broadening the spatial frequency bandwidth also changed the distribution of microsaccade amplitudes. A lower spatial frequencies, larger Bsf resulted in a large reduction of microsaccades amplitude while fixation behavior for high spatial frequencies texture was not affected. Relationship between microsaccade rate and intersaccadic timing was also dependent upon Bsf. These results suggest that the spatial frequency content of the fixated images have a strong impact upon fixation instability. Paul R. Schrater, David C. Knill and Eero P. Simoncelli (2000) " Mechanisms of visual motion detection" Nature Neuroscience 3, 64 - 68. Meeting abstract presented at VSS 2012

Temporal Encoding of Spatial Information during Active Visual Fixation

Humans and other species continually perform microscopic eye movements, even when attending to a single point. These movements, which include drifts and microsaccades, are under oculomotor control, elicit strong neural responses, and have been thought to serve important functions. The influence of these fixational eye movements on the acquisition and neural processing of visual information remains unclear. Here, we show that during viewing of natural scenes, microscopic eye movements carry out a crucial information-processing step: they remove predictable correlations in natural scenes by equalizing the spatial power of the retinal image within the frequency range of ganglion cells' peak sensitivity. This transformation, which had been attributed to center-surround receptive field organization, occurs prior to any neural processing and reveals a form of matching between the statistics of natural images and those of normal eye movements. We further show that the combined effect of microscopic eye movements and retinal receptive field organization is to convert spatial luminance discontinuities into synchronous firing events, beginning the process of edge detection. Thus, microscopic eye movements are fundamental to two goals of early visual processing: redundancy reduction and feature extraction.

Coding of Microsaccades in Three-Dimensional Space by Premotor Saccadic Neurons

Microsaccades are small, involuntary eye movements that are produced during fixation. While accurate visual perception requires precise binocular coordination during fixation, previous studies of the neural control of microsaccades measured the movement of one eye only. Here we show how premotor saccadic neurons control these small fixational eye movements in three-dimensional space. Microsaccadic eye movements, produced by monkeys trained to fixate targets presented at different depths, were similarly distributed in three-dimensional space during both near and far viewing. Single unit recordings of the neural activity of premotor neurons further revealed that the brainstem saccadic circuitry controls these minute disconjugate shifts of gaze by preferentially encoding the dynamic movement of an individual eye (i.e., integrated control of conjugate and vergence motion). These findings challenge the traditional notion that microsaccades are strictly conjugate and have important implications for studies that use microsaccades to evaluate visual and attentional processing, as well as certain neurological disorders.

A pilot study on characteristics of microsaccadic eye-movements in anisometropic amblyopia

To quantitatively investigate the characteristics of the microsaccadic eye-movements in anisometropic amblyopia and to evaluate the using value of high-speed eye-movement recording in objective and quantitative evaluation and diagnosis of amblyopia. From September in 2010 to March in 2011, 19 cases of anisometropic amblyopic patients (19 amblyopic eyes as group AM and 19 their sound eyes as group AS) and 19 cases of subjects with normal corrected visual acuities (19 dominant eyes as group ND and 19 non-dominant eyes as group NN) were recruited from the outpatient clinic at Tianjin Eye Hospital. A high-speed eye-movement recording system was used to monocularly record the fixational eye-movements of subjects' both eyes. A Matlab routine was used to detect and analyze the microsaccadic components of eye-movement waveforms. The microsaccadic amplitudes, peak velocities, occurrence rates, inter-microsaccadic intervals, cumulative probabilities of all groups were analyzed and compared using Origin8.0 and Matlab2008 statistics toolbox. The mean microsaccadic amplitude of group AM (0.76 ± 0.07)° was larger than groups AS, ND and NN (F = 49.95, P = 0.000). The mean peak velocity of group AM (79.72 ± 5.64)°/s was faster than groups AS, ND and NN (F = 4.93, P = 0.004). The mean occurrence rate of group AM (1.52 ± 0.08) Hz was less than groups AS, ND and NN (F = 120.39, P = 0.000). The mean inter-microsaccadic interval of group AM (537.40 ± 65.47) ms was longer than groups AS, ND and NN (F = 4.41, P = 0.007). The amplitude dependent cumulative probability curve of group AM shifted to right compared with other groups and its amplitude 0.67° ± 0.06° at half cumulative probability was obviously increased compared with other groups (F = 203.05, P = 0.000). Microsaccadic amplitude, peak velocity, occurrence rate, inter-microsaccadic interval and cumulative probability could be used as the parameters for objective and quantitative evaluation of eye-movement function in amblyopia. High-speed eye-movement recording could provide useful assistance in evaluation of eye-movements in amblyopic patients.

Microsaccadic eye movements during ocular pursuit

Microsaccadic eye movements during ocular pursuit

Visibility states modulate microsaccade rate and direction

We investigated how the perceptual visibility of a target influences the pattern of microsaccadic eye movements expressed during generalized flash suppression. We found that the microsaccade rate was highly dependent on the reported visibility of the target. In the visible trials, the microsaccade rate promptly rebounded to the pre-onset level, whereas on the invisible trials the rate remained low, reaching pre-onset levels hundreds of milliseconds later. In addition, the directional distributions of microsaccades were biased to the target positions in the visible condition. The present findings indicate that the microsaccade behavior is highly correlated with the perceptual state of target visibility, and suggest that the measured microsaccade rate and direction are reliable indicators of the perception.

Microsaccades Counteract Visual Fading during Fixation

Our 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.

A simple hydro-elastic model of the dynamics of a vitreous membrane

We study the motion of a fluid within a rigid spherical container subject to small-amplitude periodic rotations. The sphere is divided into two equal portions by an impermeable stretched elastic membrane whose boundary is attached to the container wall. The model aims to represent in a simplified fashion the dynamics of a vitreous membrane subject to microsaccadic movements of the human eye, assuming the vitreous to be liquefied. The vitreous is modelled as a Newtonian, incompressible fluid in irrotational motion and the problem is linearized, taking advantage of the hypothesis of small-amplitude eye rotations. Results show that, due to the presence of the fluid, the natural frequencies of oscillation of the membrane decrease significantly with respect to the case of a free membrane. Moreover, oscillations of a stretched membrane are found to be resonantly excited by rotations of the sphere with frequencies which are typical of microsaccadic eye movements. This study suggests the possibility that oscillations of vitreous membranes may induce the development of large tensile stresses capable of producing a retinal detachment. Such a conclusion will have to be further substantiated by more refined analyses accounting for further effects, such as nonlinearity and the possible viscoelastic behaviour of the vitreous located on one or both sides of the membrane.

Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys

Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys

Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys.

When viewing a stationary object, we unconsciously make small, involuntary eye movements or 'microsaccades'. If displacements of the retinal image are prevented, the image quickly fades from perception. To understand how microsaccades sustain perception, we studied their relationship to the firing of cells in primary visual cortex (V1). We tracked eye movements and recorded from V1 cells as macaque monkeys fixated. When an optimally oriented line was centered over a cell's receptive field, activity increased after microsaccades. Moreover, microsaccades were better correlated with bursts of spikes than with either single spikes or instantaneous firing rate. These findings may help explain maintenance of perception during normal visual fixation.