Microsaccades

During fixation of a stationary target, small involuntary eye movements exhibit an erratic trajectory - a random walk. Two types of these fixational eye movements are drift and microsaccades (small-amplitude saccades). Here, fixational eye movements and binocular coordination were investigated using a statistical analysis that had previously been applied to human posture control. This random-walk analysis uncovered two different time scales in fixational eye movements and identified specific functions for microsaccades. On a short time scale, microsaccades enhanced perception by increasing fixation errors. On a long time scale, microsaccades reduced fixation errors and binocular disparity (relative to pure drift movements). Thus, the findings clarify the role of oculomotor processes during fixation.

Microsaccades are involuntary, small-magnitude saccadic eye movements that occur during attempted visual fixation. Recent research has found that attention can modulate microsaccade dynamics, but few studies have addressed the effects of task difficulty on microsaccade parameters, and those have obtained contradictory results. Further, no study to date has investigated the influence of task difficulty on microsaccade production during the performance of non-visual tasks. Thus, the effects of task difficulty on microsaccades, isolated from sensory modality, remain unclear. Here we investigated the effects of task difficulty on microsaccades during the performance of a non-visual, mental arithmetic task with two levels of complexity. We found that microsaccade rates decreased and microsaccade magnitudes increased with increased task difficulty. We propose that changes in microsaccade rates and magnitudes with task difficulty are mediated by the effects of varying attentional inputs on the rostral superior colliculus activity map.

Persons with amblyopia, especially those with strabismus, are known to exhibit abnormal fixational eye movements. In this paper, we compared six characteristics of fixational eye movements among normal control eyes (n=16), the non-amblyopic fellow eyes and the amblyopic eyes of anisometropic (n=14) and strabismic amblyopes (n=14). These characteristics include the frequency, magnitude of landing errors, amplitude and speed of microsaccades, and the amplitude and speed of slow drifts. Fixational eye movements were recorded using retinal imaging while observers monocularly fixated a 1° cross. Eye position data were recovered using a cross-correlation procedure. We found that in general, the characteristics of fixational eye movements are not significantly different between the fellow eyes of amblyopes and controls, and that the strabismic amblyopic eyes are always different from the other groups. Next, we determined the primary factors that limit fixation stability and visual acuity i...

Until recently induced gamma-band activity (GBA) was considered a neural marker of cortical object representation. However, induced GBA in the electroencephalogram (EEG) is susceptible to artifacts caused by miniature fixational saccades. Recent studies have demonstrated that fixational saccades also reflect high-level representational processes. Do high-level as opposed to low-level factors influence fixational saccades? What is the effect of these factors on artifact-free GBA? To investigate this, we conducted separate eye tracking and EEG experiments using identical designs. Participants classified line drawings as objects or non-objects. To introduce low-level differences, contours were defined along different directions in cardinal color space: S-cone-isolating, intermediate isoluminant, or a full-color stimulus, the latter containing an additional achromatic component. Prior to the classification task, object discrimination thresholds were measured and stimuli were scaled to m...

Fixational eye movements occur involuntarily during visual fixation of stationary scenes. The fastest components of these miniature eye movements are microsaccades, which can be observed about once per second. Recent studies demonstrated that microsaccades are linked to covert shifts of visual attention. Here, we generalized this finding in two ways. First, we used peripheral cues, rather than the centrally presented cues of earlier studies. Second, we spatially cued attention in vision and audition to visual and auditory targets. An analysis of microsaccade responses revealed an equivalent impact of visual and auditory cues on microsaccade-rate signature (i.e. an initial inhibition followed by an overshoot and a final return to the pre-cue baseline rate). With visual cues or visual targets, microsaccades were briefly aligned with cue direction and then opposite to cue direction during the overshoot epoch, probably as a result of an inhibition of an automatic saccade to the peripheral cue. With left auditory cues and auditory targets microsaccades oriented in cue direction. We argue that microsaccades can be used to study crossmodal integration of sensory information and to ma p the time course of saccade preparation during covert shifts of visual and auditory attention.

Covert shifts of visuospatial attention are traditionally assumed to occur in the absence of oculomotor behavior. In contrast, recent behavioral studies have linked attentional cueing effects to the occurrence of microsaccades, small eye movements executed involuntarily during attempted fixation. Here we used a new type of electrophysiological marker to explore the attention-microsaccade relationship, the visual brain activity evoked by the microsaccade itself. By shifting the retinal image, microsaccades frequently elicit neural responses throughout the visual pathway, scalp-recordable in the human EEG as a microsaccade-related potential (mSRP). Although mSRPs contain similar signal components (P1/N1) as traditional visually-evoked potentials (VEPs), it is unknown whether they are also influenced by cognition. Based on established findings that VEPs are amplified for visual inputs at currently attended locations, we expected a selective gain-modulation also for mSRPs. Eye movements and EEG were coregistered in a classic spatial cueing task with an endogenous cue. Replicating behavioral findings, the direction of early microsaccades 200–400 ms after cue onset was biased towards the cued side. However, for microsaccades throughout the cue-target interval, mSRPs were systematically enhanced at occipital scalp sites contralateral to the cued hemifield. This attention effect resembled that in a control condition with VEPs and did not interact with the direction of the underlying microsaccade, suggesting that mSRPs reflect the focus of sustained visuospatial attention, which remains fixed at the cued location, despite microsaccades. Microsaccades are not merely an artifact source in the EEG; instead, they are followed by cognitively modulated brain potentials that can serve as non-intrusive electrophysiological probes of attention.

Fixation-related potentials (FRPs), neural responses aligned to the end of saccades, are a promising tool for studying the dynamics of attention and cognition under natural viewing conditions. In the past, four methodological problems have complicated the analysis of such combined eye-tracking/electroencephalogram experiments: (1) the synchronization of data streams, (2) the removal of ocular artifacts, (3) the condition-specific temporal overlap between the brain responses evoked by consecutive fixations, and (4) the fact that numerous low-level stimulus and saccade properties also influence the postsaccadic neural responses. Although effective solutions exist for the first two problems, the latter two are only beginning to be addressed. In the current paper, we present and review a unified regression-based framework for FRP analysis that allows us to deconvolve overlapping potentials while also controlling for both linear and nonlinear confounds on the FRP waveform. An open software implementation is provided for all procedures. We then demonstrate the advantages of this proposed (non)linear deconvolution modeling approach for data from three commonly studied paradigms: face perception, scene viewing, and reading. First, for a traditional event-related potential (ERP) face recognition experiment, we show how this technique can separate stimulus ERPs from overlapping muscle and brain potentials produced by small (micro)saccades on the face. Second, in natural scene viewing, we model and isolate multiple nonlinear effects of saccade parameters on the FRP. Finally, for a natural sentence reading experiment using the boundary paradigm, we show how it is possible to study the neural correlates of parafoveal preview after removing spurious overlap effects caused by the associated difference in average fixation time. Our results suggest a principal way of measuring reliable eye movement-related brain activity during natural vision.

Covert shifts of visuospatial attention are traditionally assumed to occur in the absence of oculomotor behavior.
In contrast, recent behavioral studies have linked attentional cueing effects to the occurrence of microsaccades,
small eyemovements executed involuntarily during attempted fixation. Here we used a new type of electrophysiological
marker to explore the attention–microsaccade relationship, the visual brain activity evoked by the
microsaccade itself. By shifting the retinal image, microsaccades frequently elicit neural responses throughout
the visual pathway, scalp-recordable in the human EEG as a microsaccade-related potential (mSRP). Although
mSRPs contain similar signal components (P1/N1) as traditional visually-evoked potentials (VEPs), it is unknown
whether they are also influenced by cognition. Based on established findings that VEPs are amplified for visual
inputs at currently attended locations, we expected a selective gain-modulation also for mSRPs. Eye movements
and EEG were coregistered in a classic spatial cueing task with an endogenous cue. Replicating behavioral findings,
the direction of early microsaccades 200–400 ms after cue onset was biased towards the cued side. However,
for microsaccades throughout the cue-target interval, mSRPs were systematically enhanced at occipital scalp
sites contralateral to the cued hemifield. This attention effect resembled that in a control condition with VEPs and
did not interact with the direction of the underlying microsaccade, suggesting that mSRPs reflect the focus of
sustained visuospatial attention, which remains fixed at the cued location, despite microsaccades. Microsaccades
are not merely an artifact source in the EEG; instead, they are followed by cognitively modulated brain potentials
that can serve as non-intrusive electrophysiological probes of attention.

When the eyes fixate at a point in a visual scene, small saccades rapidly shift the image on the retina. The effect of these microsaccades on the latency of subsequent large-scale saccades may be twofold. First, microsaccades are associated with an enhancement of visual perception. Their occurrence during saccade target perception could, thus, decrease saccade latencies. Second, microsaccades are likely to indicate activity in fixation-related oculomotor neurons. These represent competitors to saccade-related cells in the interplay of gaze holding and shifting. Consequently, an increase in saccade latencies would be expected after microsaccades. Here, we present evidence for both aspects of microsaccadic impact on saccade latency. In a delayed response task, participants made saccades to visible or memorized targets. First, microsaccade occurrence up to 50 ms before target disappearance correlated with 18 ms (or 8%) faster saccades to memorized targets. Second, if microsaccades occurred shortly (i.e., <150 ms) before a saccade was required, mean saccadic reaction time in visual and memory trials was increased by about 40 ms (or 16%). Hence, microsaccades can have opposite consequences for saccade latencies, pointing at a differential role of these fixational eye movements in the preparation of saccade motor programs.

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.

The visual substitution paradigm aims to facilitate the life of blind people. Generally one uses electro-stimulating devices where electrodes are arranged into arrays to stimulate the skin or the tongue mucosa to send signals of visual type to the subjects. When an electro-stimulation signal is applied continuously (e.g. when static visual scenes are displayed for a long period of time), the receptors of the affected region can get saturated and the patient may lose the displayed information. We propose here some mechanisms that ameliorate the quality of perception of the electro-stimulation information. The electrical signal is encoded as 2D scenes projected onto the tongue via a Tongue Display Unit, i.e. an electro-tactile stimulator formed by a 12×12 matrix of electrodes. We propose to apply stochastic saccades on this signal. Our assumption is that this eye-inspired mechanism should make the visual substitution more efficient (by improving the perception) because of the reductio...

Implements a spatial cuing paradigm in 3 experiments investigating the modulation of microsaccades by shifts in covert attention. A total of 80 undergraduate college students participated as subjects. Experiment 1 involved a classical spatial cueing paradigm. In Experiment 2 attention shifts were cued through alteration of the color of fixation stimuli. Experiment 3 studied the effect of display change on microsaccade rate in the absence of attention shifts. Response latencies and microsaccade rate were determined. Taken together the experiments (1) replicated the suppression of microsaccades with a minimum rate of about 150 ms after cue onset, (2) demonstrated microsaccadic enhancement with a maximum rate of about 350 ms after cue presentation, and (3) showed modulation of cue orientation. The findings confirm the influence of visual attention on microsaccades. The utility of microsaccades to map visual attention orientation in psychophysiological experiments is considered.

Following up on an exchange about the relation between microsaccades and spatial attention (Horowitz, Fenc- sik, Fine, Yurgenson, & Wolfe, 2007; Horowitz, Fine, Fencsik, Yurgenson, & Wolfe, 2007; Laubrock, Engbert, Rolfs, & Kliegl, 2007), we examine the effects of selection criteria and response modality. We show that for Posner cuing with saccadic responses, microsaccades go with attention in at least 75% of cases (almost 90% if probability matching is assumed) when they are first (or only) microsaccades in the cue–target interval and when they occur between 200 and 400 msec after the cue. The relation between spatial attention and the direction of microsaccades drops to chance level for unselected microsaccades collected during manual-response conditions. Analyses of data from four cross-modal cuing experiments demonstrate an above-chance, intermediate link for visual cues, but no systematic relation for auditory cues. Thus, the link between spatial attention and direction of microsaccades depends on the experimental condition and time of occurrence, but it can be very strong.

Microsaccade research has recently reached a critical mass of studies that allows, for the first time, a comprehensive review of how microsaccadic dynamics change in neurological and ophthalmic disease. We discuss the various pathological conditions that affect microsaccades, their impact on microsaccadic and other fixational eye movement dynamics, and the incipient studies that point to microsaccadic features as potential indicators of differential and early diagnoses of multiple clinical conditions, from movement disorders to attention-deficit hyperactivity disorder to amblyopia. We propose that the objective assessment of fixational eye movement parameters may help refine differential diagnostics in neurological disease and assist in the evaluation of ongoing therapy regimes. In addition, determining the effects of ophthalmic disease on fixational eye movement features may help evaluate visual impairment in an objective manner, particularly in young patients or those experiencing...

Neuronal activity in area LIP is correlated with the perceived direction of ambiguous apparent motion (Z. M. Williams, J. C. Elfar, E. N. Eskandar, L. J. Toth, & J. A. Assad, 2003). Here we show that a similar correlation exists for small eye movements made during fixation. A moving dot grid with superimposed fixation point was presented through an aperture. In a motion discrimination task, unambiguous motion was compared with ambiguous motion obtained by shifting the grid by half of the dot distance. In three experiments we show that (a) microsaccadic inhibition, i.e., a drop in microsaccade frequency precedes reports of perceptual flips, (b) microsaccadic inhibition does not accompany simple response changes, and (c) the direction of microsaccades occurring before motion onset biases the subsequent perception of ambiguous motion. We conclude that microsaccades provide a signal on which perceptual judgments rely in the absence of objective disambiguating stimulus information.

Following up on an exchange about the relation between microsaccades and spatial attention (Horowitz, Fencsik, Fine, Yurgenson, & Wolfe, 2007; Horowitz, Fine, Fencsik, Yurgenson, & Wolfe, 2007; Laubrock, Engbert, Rolfs, & Kliegl, 2007), we examine the effects of selection criteria and response modality. We show that for Posner cuing with saccadic responses, microsaccades go with attention in at least 75% of cases (almost 90% if probability matching is assumed) when they are first (or only) microsaccades in the cue–target interval and when they occur between 200 and 400 msec after the cue. The relation between spatial attention and the direction of microsaccades drops to chance level for unselected microsaccades collected during manual-response conditions. Analyses of data from four cross-modal cuing experiments demonstrate an above-chance, intermediate link for visual cues, but no systematic relation for auditory cues. Thus, the link between spatial attention and direction of microsaccades depends on the experimental condition and time of occurrence, but it can be very strong.

We compared effects of covert spatial-attention shifts induced with exogenous or endogenous cues on microsaccade rate and direction. Separate and dissociated effects were obtained in rate and direction measures. Display changes caused microsaccade rate inhibition, followed by sustained rate enhancement. Effects on microsaccade direction were differentially tied to cue class (exogenous vs. endogenous) and type (neutral vs. directional). For endogenous cues, direction effects were weak and occurred late. Exogenous cues caused a fast direction bias towards the cue (i.e., early automatic triggering of saccade programs), followed by a shift in the opposite direction (i.e, controlled inhibition of cue-directed saccades, leading to a "leakage" of microsaccades in the opposite direction).

Neuronal activity in area LIP is correlated with the perceived direction of ambiguous apparent motion (Z. M. Williams, J. C. Elfar, E. N. Eskandar, L. J. Toth, & J. A. Assad, 2003). Here we show that a similar correlation exists for small eye movements made during fixation. A moving dot grid with superimposed fixation point was presented through an aperture. In a motion discrimination task, unambiguous motion was compared with ambiguous motion obtained by shifting the grid by half of the dot distance. In three experiments we show that (a) microsaccadic inhibition, i.e., a drop in microsaccade frequency precedes reports of perceptual flips, (b) microsaccadic inhibition does not accompany simple response changes, and (c) the direction of microsaccades occurring before motion onset biases the subsequent perception of ambiguous motion. We conclude that microsaccades provide a signal on which perceptual judgments rely in the absence of objective disambiguating stimulus information.

We examine how the size of saccadic under-/over-shoot and target eccentricity influence the latency, amplitude and orientation of secondary (micro-)saccades. In our experiment, a target appeared at an eccentricity of either 6° or 14° of visual angle. Subjects were instructed to direct their gaze as quickly as possible to the target and hold fixation at the new location until the end of the trial. Typically, increasing saccadic error is associated with faster and larger secondary saccades. We show that secondary saccades at distant in contrast to close targets have in a specific error range a shorter latency, larger amplitude, and follow more often the direction of the primary saccade. Finally, we demonstrate that an undershooting primary saccade is followed almost exclusively by secondary saccades into the same direction while overshooting primary saccades are followed by secondary saccades into both directions. This supports the notion that under- and over-shooting imply different consequences for postsaccadic oculomotor processing. Results are discussed using a model, introduced by Rolfs, Kliegl, and Engbert (2008), to account for the generation of microsaccades. We argue that the dynamic interplay of target eccentricity and the magnitude of the saccadic under-/over-shoot can be explained by a different strength of activation in the two hemispheres of the saccadic motor map in this model.

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.

Microsaccades are very small, involuntary flicks in eye position that occur on average once or twice per second during attempted visual fixation. Microsaccades give rise to EMG eye muscle spikes that can distort the spectrum of the scalp EEG and mimic increases in gamma band power. Here we demonstrate that microsaccades are also accompanied by genuine and sizeable cortical activity, manifested in the EEG. In three experiments, high-resolution eye movements were corecorded with the EEG: during sustained fixation of checkerboard and face stimuli and in a standard visual oddball task that required the counting of target stimuli. Results show that microsaccades as small as 0.15° generate a field potential over occipital cortex and midcentral scalp sites 100–140 ms after movement onset, which resembles the visual lambda response evoked by larger voluntary saccades. This challenges the standard assumption of human brain imaging studies that saccade-related brain activity is precluded by fixation, even when fully complied with. Instead, additional cortical potentials from microsaccades were present in 86% of the oddball task trials and of similar amplitude as the visual response to stimulus onset. Furthermore, microsaccade probability varied systematically according to the proportion of target stimuli in the oddball task, causing modulations of late stimulus-locked event-related potential (ERP) components. Microsaccades present an unrecognized source of visual brain signal that is of interest for vision research and may have influenced the data of many ERP and neuroimaging studies.