Microsaccade Rate Research Articles

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

Visual fixation as equilibrium: evidence from superior colliculus inactivation.

During visual fixation, the image of an object is maintained within the fovea. Previous studies have shown that such maintenance involves the deep superior colliculus (dSC). However, the mechanisms by which the dSC supports visual fixation remain controversial. According to one view, activity in the rostral dSC maintains gaze direction by preventing neurons in the caudal dSC from issuing saccade commands. An alternative hypothesis proposes that gaze direction is achieved through equilibrium of target position signals originating from the two dSCs. Here, we show in monkeys that artificially reducing activity in the rostral half of one dSC results in a biased estimate of target position during fixation, consistent with the second hypothesis, rather than an inability to maintain gaze fixation as predicted by the first hypothesis. After injection of muscimol at rostral sites in the dSC, fixation became more stable since microsaccade rate was reduced rather than increased. Moreover, the scatter of eye positions was offset relative to preinactivation baselines. The magnitude and the direction of the offsets depended on both the target size and the injected site in the collicular map. Other oculomotor parameters, such as the accuracy of saccades to peripheral targets and the amplitude and velocity of fixational saccades, were largely unaffected. These results suggest that the rostral half of the dSC supports visual fixation through a distributed representation of behaviorally relevant target position signals. The inactivation-induced fixation offset establishes the foveal visual stimulation that is required to restore the balance of activity between the two dSCs.

Computational modeling of collicular integration of perceptual responses and attention in microsaccades.

During visual fixation on a target object, our eyes are not motionless but generate slow fixational eye movements and microsaccades. Effects of visual attention have been observed in both microsaccade rates and spatial directions. Experimental results, however, range from early (<200 ms) to late (>600 ms) effects combined with cue-congruent as well as cue-incongruent microsaccade directions. On the basis of well characterized neural circuitry in superior colliculus, we construct a dynamical model of neural activation that is modulated by perceptual input and visual attention. Our results show that additive integration of low-level perceptual responses and visual attention can explain microsaccade rate and direction effects across a range of visual cueing tasks. These findings suggest that the patterns of microsaccade direction observed in experiments are compatible with a single dynamical mechanism. The basic principles of the model are highly relevant to the general problem of integration of low-level perception and top-down selective attention.

Looking at Op Art: Gaze Stability and Motion Illusions

Various Op artists have used simple geometrical patterns to create the illusion of motion in their artwork. One explanation for the observed illusion involves retinal shifts caused by small involuntary eye movements that observers make while they try to maintain fixation. Earlier studies have suggested a prominent role of the most conspicuous of these eye movements, small rapid position shifts called microsaccades. Here, we present data that could expand this view with a different interpretation. In three experiments, we recorded participants' eye movements while they tried to maintain visual fixation when being presented with variants of Bridget Riley's Fall, which were manipulated such as to vary the strength of induced motion. In the first two experiments, we investigated the properties of microsaccades for a set of stimuli with known motion strengths. In agreement with earlier observations, microsaccade rates were unaffected by the stimulus pattern and, consequently, the strength of induced motion illusion. In the third experiment, we varied the stimulus pattern across a larger range of parameters and asked participants to rate the perceived motion illusion. The results revealed that motion illusions in patterns resembling Riley's Fall are perceived even in the absence of microsaccades, and that the reported strength of the illusion decreased with the number of microsaccades in the trial. Together, the three experiments suggest that other sources of retinal image instability than microsaccades, such as slow oculomotor drift, should be considered as possible factors contributing to the illusion.

Inhibition of microsaccade rate caused by increase in visual attention

Inhibition of microsaccade rate caused by increase in visual attention

Saccadic facilitation by modulation of microsaccades in natural backgrounds

Saccades move objects of interest into the center of the visual field for high-acuity visual analysis. White, Stritzke, and Gegenfurtner (Current Biology, 18, 124–128, 2008) have shown that saccadic latencies in the context of a structured background are much shorter than those with an unstructured background at equal levels of visibility. This effect has been explained by possible preactivation of the saccadic circuitry whenever a structured background acts as a mask for potential saccade targets. Here, we show that background textures modulate rates of microsaccades during visual fixation. First, after a display change, structured backgrounds induce a stronger decrease of microsaccade rates than do uniform backgrounds. Second, we demonstrate that the occurrence of a microsaccade in a critical time window can delay a subsequent saccadic response. Taken together, our findings suggest that microsaccades contribute to the saccadic facilitation effect, due to a modulation of microsaccade rates by properties of the background.Electronic supplementary materialThe online version of this article (doi:10.3758/s13414-011-0107-9) contains supplementary material, which is available to authorized users.

Motion-induced blindness and microsaccades: Cause and effect

It has been suggested that subjective disappearance of visual stimuli results from a spontaneous reduction of microsaccade rate causing image stabilization, enhanced adaptation, and a consequent fading. In motion-induced blindness (MIB), salient visual targets disappear intermittently when surrounded by a moving pattern. We investigated whether changes in microsaccade rate can account for MIB. We first determined that the moving mask does not affect microsaccade metrics (rate, magnitude, and temporal distribution). We then compared the dynamics of microsaccades during reported illusory disappearance (MIB) and physical disappearance (Replay) of a salient peripheral target. We found large modulations of microsaccade rate following perceptual transitions, whether illusory (MIB) or real (Replay). For MIB, the rate also decreased prior to disappearance and increased prior to reappearance. Importantly, MIB persisted in the presence of microsaccades although sustained microsaccade rate was lower during invisible than visible periods. These results suggest that the microsaccade system reacts to changes in visibility, but microsaccades also modulate MIB. The latter modulation is well described by a Poisson model of the perceptual transitions assuming that the probability for reappearance and disappearance is modulated following a microsaccade. Our results show that microsaccades counteract disappearance but are neither necessary nor sufficient to account for MIB.

Gamma in motion: Pattern reversal elicits stronger gamma-band responses than motion

Previous studies showed higher gamma-band responses (GBRs, ≈40Hz) of the electroencephalogram (EEG) for moving compared to stationary stimuli. However, it is unclear whether this modulation by motion reflects a special responsiveness of the GBR to the stimulus feature “motion,” or whether GBR enhancements of similar magnitude can be elicited also by a salient change within a static stimulus that does not include motion.Therefore, we measured the EEG of healthy subjects watching stationary square wave gratings of high contrast that either started to move or reversed their black and white pattern shortly after their onset. The strong contrast change of the pattern reversal represented a salient but motionless change within the grating that was compared to the onset of the stationary grating and the motion onset. Induced and evoked GBRs were analyzed for all three display conditions. In order to assess the influenceof fixational eye movements on the induced GBRs, we also examined the time courses of microsaccade rates during the three display conditions.Amplitudes of both evoked and induced GBRs were stronger for pattern reversal than for motion onset. There was no significant amplitude difference between the onsets of the stationary and moving gratings. However, mean frequencies of the induced GBR were ~10Hz higher in response to the onsets of moving compared to stationary gratings. Furthermore, the modulations of the induced GBR did not parallel the modulations of microsaccade rate, indicating that our induced GBRs reflect neuronal processes.These results suggest that, within the gamma-band range, the encoding of moving gratings in early visual cortex is primarily based on an upward frequency shift, whereas contrast changes within static gratings are reflected by amplitude enhancement.

What determines the direction of microsaccades?

During visual fixation, our eyes are not entirely still. Instead, small eye movements, such as microsaccades, can be observed. We here investigate what determines the direction and frequency of these microsaccades, as this information might help to clarify what purpose they serve. The relative contribution of three possible factors was examined: (1) the orienting of covert attention, (2) the spatial distribution of possible target locations, and (3) whether monocular or binocular microsaccades are considered. The orienting of covert attention and the distribution of possible target locations had a relatively weak effect on microsaccade rates and directions. In contrast, the classification of micro-saccades as binocular (occurring in both eyes simultaneously) or monocular (observed in one eye only) strongly affected both the rate and the direction of microsaccades. The results are discussed in the context of existing findings.

Microsaccades are different from saccades in scene perception

Eye-fixation durations are among the best and most widely used measures of ongoing cognition in visual tasks, e.g., reading, visual search or scene perception. However, fixations are characterized by ongoing motor activity (or fixational eye movements) with microsaccades as their most pronounced components. Recent work demonstrated the similarities of microsaccades and inspection saccades. Here, we show that distinct properties of microsaccades and inspection saccades can be found in a scene perception task, based on descriptive measures (e.g., a bimodal amplitude distribution) as well as functional characteristics (e.g., inter saccadic-event intervals and generating processes). Besides these specific differences, microsaccade rates produced by individual participants in a fixation paradigm are correlated with microsaccade rates extracted from fixations in scene perception, indicating a common neurophysiological basis. Finally, we observed that slow fixational eye movements, called drift, are significantly reduced during long fixations in scene viewing, which informs about the control of eye movements in scene viewing.

Rare but precious: Microsaccades are highly informative about attentional allocation

To clarify the relation between attention and microsaccades, we monitored microsaccades while observers performed tasks with different attentional demand. In four high-demand conditions, observers shifted attention covertly to a peripheral location, or focused attention at fixation. Three corresponding low-demand conditions on physically identical displays provided a basis for comparison. Our results revealed two distinct effects of attentional load: higher loads were associated consistently with lower microsaccade rates, but also with increased directional selectivity (up to 98% congruent). In short, when microsaccades were most rare, the direction of microsaccades proved most informative about the location of the attention focus. The detailed time-courses of the two effects differed, however, suggesting that they may reflect independent processes.

BOLD signal in both ipsilateral and contralateral retinotopic cortex modulates with perceptual fading.

Under conditions of visual fixation, perceptual fading occurs when a stationary object, though present in the world and continually casting light upon the retina, vanishes from visual consciousness. The neural correlates of the consciousness of such an object will presumably modulate in activity with the onset and cessation of perceptual fading.MethodIn order to localize the neural correlates of perceptual fading, a green disk that had been individually set to be equiluminant with the orange background, was presented in one of the four visual quadrants; Subjects indicated with a button press whether or not the disk was subjectively visible as it perceptually faded in and out.ResultsBlood oxygen-level dependent (BOLD) signal in V1 and ventral retinotopic areas V2v and V3v decreases when the disk subjectively disappears, and increases when it subjectively reappears. This effect occurs in early visual areas both ipsilaterally and contralaterally to the fading figure. That is, it occurs regardless of whether the fading stimulus is presented inside or outside of the corresponding portion of visual field. In addition, we find that the microsaccade rate rises before and after perceptual transitions from not seeing to seeing the disk, and decreases before perceptual transitions from seeing to not seeing the disk. These BOLD signal changes could be driven by a global process that operates across contralateral and ipsilateral visual cortex or by a confounding factor, such as microsaccade rate.

Eye movements under various conditions of image fading.

Under normal viewing conditions, the image on the retina is always in motion. Images fade and may eventually disappear when the physiological motion of the retinal stimulus is reduced or eliminated. According to a widespread theory, microsaccades are responsible for maintaining visibility during fixation. However, while it is clear that the sudden changes in visual input caused by microsaccades are sufficient to restore visibility, it has long been questioned whether this effect might be an epiphenomenon, rather than an important function of microsaccades. In this study, we compared the eye movements measured under conditions that either simulated or induced loss of visibility to those recorded when fading did not occur. Both drifts and microsaccades were unaffected by changes in the stimulus contrast and bandwidth that recreated the percept experienced during image fading. Under retinal stabilization, a condition in which observers reported fading, microsaccade rates decreased, instead of increasing as predicted by the fading prevention hypothesis. While image fading had no influence on oculomotor activity, eye movements were instead strongly modulated by the onset of the stimulus and by the requested precision of fixation. Microsaccades occurred more frequently and were more corrective for preceding drifts during accurate fixation on a cue than during relaxed fixation on a region of the screen. These results do not support a causal relationship between image fading and microsaccade production and show that the precision of required fixation is a major contributor to microsaccades.

Microsaccade Rate Varies with Subjective Visibility during Motion-Induced Blindness

Motion-induced blindness (MIB) occurs when a dot embedded in a motion field subjectively vanishes. Here we report the first psychophysical data concerning effects of microsaccade/eyeblink rate upon perceptual switches during MIB. We find that the rate of microsaccades/eyeblink rises before and after perceptual transitions from not seeing to seeing the dot, and decreases before perceptual transitions from seeing it to not seeing it. In addition, event-related fMRI data reveal that, when a dot subjectively reappears during MIB, the blood oxygen-level dependent (BOLD) signal increases in V1v and V2v and decreases in contralateral hMT+. These BOLD signal changes observed upon perceptual state changes in MIB could be driven by the change of perceptual states and/or a confounding factor, such as the microsaccade/eyeblink rate.

Microsaccadic inhibition and P300 enhancement in a visual oddball task

It has recently been demonstrated that the presentation of visual oddballs induces a prolonged inhibition of microsaccades. The amplitude of the P300 component in event-related potentials (ERPs) has been shown to be sensitive to the category (target vs. nontarget) of the eliciting stimulus, its overall probability, and the preceding stimulus sequence. In the present study we further specify the functional underpinnings of the prolonged microsaccadic inhibition in the visual oddball task, showing that the stimulus category, the frequency of a stimulus, and the preceding stimulus sequence influence microsaccade rate. Furthermore, by co-recording ERPs and eye movements, we were able to demonstrate that, despite being largely sensitive to the same experimental manipulation, the amplitude of P300 and the microsaccadic inhibition predict each other only weakly.

A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus

During fixation, the eyes are not still but often exhibit microsaccadic movements. The function of microsaccades is controversial, largely because the neural mechanisms responsible for their generation are unknown. Here, we show that the superior colliculus (SC), a retinotopically organized structure involved in voluntary-saccade target selection, plays a causal role in microsaccade generation. Neurons in the foveal portion of the SC increase their activity before and during microsaccades with sizes of only a few minutes of arc and exhibit selectivity for the direction and amplitude of these movements. Reversible inactivation of these neurons significantly reduces microsaccade rate without otherwise compromising fixation. These results, coupled with computational modeling of SC activity, demonstrate that microsaccades are controlled by the SC and explain the link between microsaccades and visual attention.

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 drive illusory motion in theEnigmaillusion

Visual images consisting of repetitive patterns can elicit striking illusory motion percepts. For almost 200 years, artists, psychologists, and neuroscientists have debated whether this type of illusion originates in the eye or in the brain. For more than a decade, the controversy has centered on the powerful illusory motion perceived in the painting Enigma, created by op-artist Isia Leviant. However, no previous study has directly correlated the Enigma illusion to any specific physiological mechanism, and so the debate rages on. Here, we show that microsaccades, a type of miniature eye movement produced during visual fixation, can drive illusory motion in Enigma. We asked subjects to indicate when illusory motion sped up or slowed down during the observation of Enigma while we simultaneously recorded their eye movements with high precision. Before "faster" motion periods, the rate of microsaccades increased. Before "slower/no" motion periods, the rate of microsaccades decreased. These results reveal a direct link between microsaccade production and the perception of illusory motion in Enigma and rule out the hypothesis that the origin of the illusion is purely cortical.

Microsaccade-induced prolongation of saccade latencies depends on microsaccade amplitude

Fixations consist of small movements including microsaccades, i.e., rapid flicks in eye position that replace the retinal image by up to 1 degree of visual angle. Recently, we showed in a delayed-saccade task (1) that the rate of microsaccades decreased in the course of saccade preparation and (2) that microsaccades occurring around the time of a go signal were associated with prolonged saccade latencies (Rolfs et al., 2006). A re-analysis of the same data set revealed a strong dependence of these findings on microsaccade amplitude. First, microsaccade amplitude dropped to a minimum just before the generation of a saccade. Second, the delay of response saccades was a function of microsaccade amplitude: Microsaccades with larger amplitudes were followed by longer response latencies. These finding were predicted by a recently proposed model that attributes microsaccade generation to fixation-related activity in a saccadic motor map that is in competition with the generation of large saccades (Rolfs et al., 2008). We propose, therefore, that microsaccade statistics provide a behavioral correlate of fixation-related activity in the oculomotor system.

Toward a model of microsaccade generation: The case of microsaccadic inhibition

Microsaccades are one component of the small eye movements that constitute fixation. Their implementation in the oculomotor system is unknown. To better understand the physiological and mechanistic processes underlying microsaccade generation, we studied microsaccadic inhibition, a transient drop of microsaccade rate, in response to irrelevant visual and auditory stimuli. Quantitative descriptions of the time course and strength of inhibition revealed a strong dependence of microsaccadic inhibition on stimulus characteristics. In Experiment 1, microsaccadic inhibition occurred sooner after auditory than after visual stimuli and after luminance-contrast than after color-contrast visual stimuli. Moreover, microsaccade amplitude strongly decreased during microsaccadic inhibition. In Experiment 2, the latency of microsaccadic inhibition increased with decreasing luminance contrast. We develop a conceptual model of microsaccade generation in which microsaccades result from fixation-related activity in a motor map coding for both fixation and saccades. In this map, fixation is represented at the central site. Saccades are generated by activity in the periphery, their amplitude increasing with eccentricity. The activity at the central, fixation-related site of the map predicts the rate of microsaccades as well as their amplitude and direction distributions. This model represents a framework for understanding the dynamics of microsaccade behavior in a broad range of tasks.