Microsaccade Direction Research Articles

Attentional shifts bias microsaccade direction but do not cause new microsaccades

Brain circuitry that controls where we look also contributes to attentional selection of visual contents outside current fixation, or content within the spatial layout of working memory. A behavioural manifestation of this contribution comes from modulations in microsaccade direction that accompany spatial attention shifts. Here, we address whether such modulations come about because attention shifts trigger new microsaccades or whether, instead, spatial attention only biases the direction of ongoing microsaccades that would have been made whether or not attention was also shifted. We utilised an internal-selective-attention task that has recently been shown to yield robust spatial microsaccade modulations and compared microsaccade rates following colour retrocues that were carefully matched for sensory input, but differed in whether they invited an attention shift or not. If attention shifts trigger new microsaccades then we would expect more microsaccades following attention-directing cues than following neutral cues. In contrast, we found no evidence for an increase in overall microsaccade rate, despite robust modulations in microsaccade direction. This implies that shifting spatial attention biases the direction of ongoing microsaccades without changing the probability of microsaccade occurrence. These findings help to explain why microsaccades and visual-spatial shifts of attention are often correlated but not obligatorily linked.

Microsaccades Track Location-Based Object Rehearsal in Visual Working Memory.

Besides controlling eye movements, the brain's oculomotor system has been implicated in the control of covert spatial attention and the rehearsal of spatial information in working memory. We investigated whether the oculomotor system also contributes to rehearsing visual objects in working memory when object location is never asked about. To address this, we tracked the incidental use of locations for mnemonic rehearsal via directional biases in microsaccades while participants maintained two visual objects (colored oriented gratings) in working memory. By varying the stimulus configuration (horizontal, diagonal, and vertical) at encoding, we could quantify whether microsaccades were more aligned with the configurational axis of the memory contents, as opposed to the orthogonal axis. Experiment 1 revealed that microsaccades continued to be biased along the axis of the memory content several seconds into the working memory delay. In Experiment 2, we confirmed that this directional microsaccade bias was specific to memory demands, ruling out lingering effects from passive and attentive encoding of the same visual objects in the same configurations. Thus, by studying microsaccade directions, we uncover oculomotor-driven rehearsal of visual objects in working memory through their associated locations.

Visual perceptual learning modulates microsaccade rate and directionality

Microsaccades, incessant “fixational eye movements” (< 1°), are an important window into cognitive functions. Yet, its role in visual perceptual learning (VPL)–improvements in visual discrimination due to practice–remains practically unexplored. Here we investigated whether and how microsaccades change in VPL. Human observers performed a Landolt acuity task for 5 consecutive days and were assigned to the Neutral or Attention group. On each trial, two peripheral Landolt squares were presented briefly along a diagonal. Observers reported the gap side of the target stimulus. Training improved acuity and modified the microsaccade rate; with training, the rate decreased during the fixation period but increased during the response cue. Furthermore, microsaccade direction during the response cue was biased toward the target location, and training enhanced and sped up this bias. Finally, the microsaccade rate during a task-free fixation period correlated with observers’ initial acuity threshold, indicating that the fewer the microsaccades during fixation the better the individual visual acuity. All these results, which were similar for both the Neutral and Attention groups and at both trained and untrained locations, suggest that microsaccades could serve as a physiological marker reflecting functional dynamics in human perceptual learning.

Microsaccade directions track spatial oculomotor-based rehearsal of non-spatial object features in visual working memory

Microsaccade directions track spatial oculomotor-based rehearsal of non-spatial object features in visual working memory

Human microsaccade cueing modulation in visual- and memory-delay saccade tasks after theta burst transcranial magnetic stimulation over the frontal eye field

Microsaccades that occur during periods of fixation are modulated by various cognitive processes and have an impact on visual processing. A network of brain areas is involved in microsaccade generation, including the superior colliculus and frontal eye field (FEF) which are involved in modulating microsaccade rate and direction after the appearance of a visual cue (referred to as microsaccade cueing modulation). Although the neural mechanisms underlying microsaccade cueing modulations have been demonstrated in monkeys, limited research has investigated a causal role of these areas in humans. By applying continuous theta-burst transcranial magnetic stimulation (cTBS) over the right FEF and vertex, we investigated the role of human FEF in modulating microsaccade responses after the appearance of a visual target in a visual- and memory-delay saccade task. After target appearance, microsaccade rate was initially suppressed but then increased in both cTBS conditions. More importantly, in the visual-delay task, microsaccades after target appearance were directed to the ipsilateral side more often with FEF, compared to vertex stimulation. Moreover, microsaccades were directed towards the target location, then to the opposite location of the target in both tasks, with larger effects in the visual-, compared to, memory-delay task. This microsaccade direction modulation was delayed after FEF stimulation in the memory-delay task. Overall, some microsaccade cueing modulations were moderately disrupted after FEF cTBS, suggesting a causal role for involvement of the human FEF in microsaccade generation after presentation of salient stimuli.

Microsaccades are directed toward the midpoint between targets in a variably cued attention task

Reliable, noninvasive biomarkers that reveal the internal state of a subject are an invaluable tool for neurological diagnoses. Small fixational eye movements, called microsaccades, are a candidate biomarker thought to reflect a subject's focus of attention [Z. M. Hafed, J. J. Clark, VisionRes. 42, 2533-2545 (2002); R. Engbert, R. Kliegl, VisionRes. 43, 1035-1045 (2003)]. The linkage between the direction of microsaccades and attention has mainly been demonstrated using explicit and unambiguous attentional cues. However, the natural world is seldom predictable and rarely provides unambiguous information. Thus, a useful biomarker must be robust to such changes in environmental statistics. To determine how well microsaccades reveal visual-spatial attention across behavioral contexts, we analyzed these fixational eye movements in monkeys performing a conventional change detection task. The task included two stimulus locations and variable cue validities across blocks of trials. Subjects were adept at the task, showing precise and graded modulations of visual attention for subtle target changes and performing better and faster when the cue was more reliable [J. P. Mayo, J. H. R. Maunsell, J. Neurosci.36, 5353 (2016)]. However, over tens of thousands of microsaccades, we found no difference in microsaccade direction between cued locations when cue variability was high nor between hit and miss trials. Instead, microsaccades were made toward the midpoint of the two target locations, not toward individual targets. Our results suggest that the direction of microsaccades should be interpreted with caution and may not be a reliable measure of covert spatial attention in more complex viewing conditions.

Microsaccades and temporal attention at different locations of the visual field.

Temporal attention, the prioritization of information at specific points in time, improves performance in behavioral tasks but cannot ameliorate the perceptual asymmetries that exist across the visual field. That is, even after attentional deployment, performance is better along the horizontal than vertical meridian and worse at the upper than lower vertical meridian. Here we asked whether and how microsaccades-tiny fixational eye-movements-could mirror or alternatively attempt to compensate for these performance asymmetries by assessing temporal profiles and direction of microsaccades as a function of visual field location. Observers were asked to report the orientation of one of two targets presented at different time points, in one of three blocked locations (fovea, right horizontal meridian, upper vertical meridian). We found the following: (1) Microsaccade occurrence did not affect either task performance or the magnitude of the temporal attention effect. (2) Temporal attention modulated the microsaccade temporal profiles, and this modulation varied with polar angle location. At all locations, microsaccade rates were significantly more suppressed in anticipation of the target when temporally cued than in the neutral condition. Moreover, microsaccade rates were more suppressed during target presentation in the fovea than in the right horizontal meridian. (3) Across locations and attention conditions, there was a pronounced bias toward the upper hemifield. Overall, these results reveal that temporal attention benefits performance similarly around the visual field, microsaccade suppression is more pronounced for attention than expectation (neutral trials) across locations, and the directional bias toward the upper hemifield could reflect an attempt to compensate for typical poor performance at the upper vertical meridian.

Microsaccades transiently lateralise EEG alpha activity.

The lateralisation of 8-12Hz alpha activity is a canonical signature of human spatial cognition that is typically studied under strict fixation requirements. Yet, even during attempted fixation, the brain produces small involuntary eye movements known as microsaccades. Here we report how spontaneous microsaccades - made in the absence of incentives to look elsewhere - can themselves drive transient lateralisation of EEG alpha power according to microsaccade direction. This transient lateralisation of posterior alpha power occurs similarly following start and return microsaccades and is, at least for start microsaccades, driven by increased alpha power ipsilateral to microsaccade direction. This reveals new links between spontaneous microsaccades and human electrophysiological brain activity. It highlights how microsaccades are an important factor to consider in studies relating alpha activity - including spontaneous fluctuations in alpha activity - to spatial cognition, such as studies on visual attention, anticipation, and working memory.

Microsaccade directions are not influenced by the orientation of natural scene tilt during fixation

Microsaccade directions are not influenced by the orientation of natural scene tilt during fixation

Measurement of Fixational Eye Movements With the Head-Mounted Perimeter Imo.

PurposeAlthough visual field testing is conducted with the subject gazing at a fixation target, constant minute eye movements, called fixational eye movements, do occur during fixation. We examined dynamic changes in fixational eye movements associated with stimulus presentation during visual field testing.MethodsWe used the head-mounted perimeter imo, which is capable of measurement under binocular conditions, with the frame rate of its fixation monitoring camera improved to 300 Hz, to assess fixational eye movements in 18 healthy individuals. We measured changes in fixational eye movements during testing under monocular and binocular conditions and analyzed these changes based on the bivariate contour ellipse area (BCEA). We also assessed the changes in the horizontal and vertical microsaccade rates separately.ResultsBoth the BCEA and horizontal microsaccade rates were higher at 400 to 600 msec after stimulus presentation than during stimulus presentation (P < 0.01). Additionally, the BCEA and vertical microsaccade rates were significantly lower in the binocular condition than in the monocular condition (P < 0.01 and P < 0.05, respectively). We did not observe a significant correlation between the test locations and microsaccade direction during visual field testing.ConclusionsFixational eye movements, especially vertical microsaccade rates, were lower in the binocular condition than in the monocular condition. Visual field testing under binocular conditions is a useful method for suppressing fixational eye movements and stabilizing the fixation during testing and may improve the reliability of the test results.Translational RelevanceVisual field testing under binocular conditions can make the fixation more stable during the testing compared with monocular conditions.

Role of the frontal eye field in human microsaccade responses: A TMS study

Microsaccade is a type of fixational eye movements that is modulated by various sensory and cognitive processes, and impact our visual perception. Although studies in monkeys have demonstrated a functional role for the superior colliculus and frontal eye field (FEF) in controlling microsaccades, our understanding of the neural mechanisms underlying the generation of microsaccades is still limited. By applying continuous theta-burst stimulation (cTBS) over the right FEF and the vertex, we investigated the role of the FEF in generating human microsaccade responses evoked by salient stimuli or by changes in background luminance. We observed higher microsaccade rates prior to target appearance, and larger rebound in microsaccade occurrence following salient stimuli, when disruptive cTBS was applied over FEF compared to vertex stimulation. Moreover, the microsaccade direction modulation after changes in background luminance was disrupted with FEF stimulation. Together, our results constitute the first evidence of FEF modulation in human microsaccade responses.

Sensory Input Modulates Microsaccades during Heading Perception.

Microsaccades are small eye movements produced during attempted fixation. During locomotion, the eyes scan the environment; the gaze is not always directed to the focus of expansion of the optic flow field. We sought to investigate whether the microsaccadic activity was modulated by eye position during the view of radial optic flow stimuli, and if the presence or lack of a proprioceptive input signal may influence the microsaccade characteristics during self-motion perception. We recorded the oculomotor activity when subjects were either standing or sitting in front of a screen during the view of optic flow stimuli that simulated specific heading directions with different gaze positions. We recorded five trials of each stimulus. Results showed that microsaccade duration, peak velocity, and rate were significantly modulated by optic flow stimuli and trial sequence. We found that the microsaccade rate increased in each condition from trial 1 to trial 5. Microsaccade peak velocity and duration were significantly different across trials. The analysis of the microsaccade directions showed that the different combinations of optic flow and eye position evoked non-uniform directions of microsaccades in standing condition with mean vectors in the upper-left quadrant of the visual field, uncorrelated with optic flow directions and eye positions. In sitting conditions, all stimuli evoked uniform directions of microsaccades. Present results indicate that the proprioceptive signals when the subjects stand up creates a different input that could alter the eye-movement characteristics during heading perceptions.

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.

Sustained spatial attention accounts for the direction bias of human microsaccades

Small ballistic eye movements, so called microsaccades, occur even while foveating an object. Previous studies using covert attention tasks have shown that shortly after a symbolic spatial cue, specifying a behaviorally relevant location, microsaccades tend to be directed toward the cued location. This suggests that microsaccades can serve as an index for the covert orientation of spatial attention. However, this hypothesis faces two major challenges: First, effects associated with visual spatial attention are hard to distinguish from those that associated with the contemplation of foveating a peripheral stimulus. Second, it is less clear whether endogenously sustained attention alone can bias microsaccade directions without a spatial cue on each trial. To address the first issue, we investigated the direction of microsaccades in human subjects while they attended to a behaviorally relevant location and prepared a response eye movement either toward or away from this location. We find that directions of microsaccades are biased toward the attended location rather than towards the saccade target. To tackle the second issue, we verbally indicated the location to attend before the start of each block of trials, to exclude potential visual cue-specific effects on microsaccades. Our results indicate that sustained spatial attention alone reliably produces the microsaccade direction effect. Overall, our findings demonstrate that sustained spatial attention alone, even in the absence of saccade planning or a spatial cue, is sufficient to explain the direction bias observed in microsaccades.

Triggering microsaccades by foveal motor error is sufficient to modulate peripheral visual sensitivity: neural and perceptual evidence

Visual processing is frequently interspersed with saccades, which are associated with strong peri-movement changes in neural and perceptual sensitivity. With fixed gaze, for controlled experiments on processes like covert attention, microsaccades still occur. During the past two decades, it became clear that microsaccades are not random (Hafed and Clark, 2002; Engbert and Kliegl, 2003), but instead exhibit predictable correlations with enhanced or decreased peripheral visual sensitivity (in multiple brain areas) and perception. These time-locked changes appear at eccentricities 1-2 orders of magnitude larger than the eye movement endpoints themselves. However, it remains unclear whether it is microsaccades, perhaps through their motor preparatory activity, that causally influence visual sensitivity, or whether visual sensitivity is itself modulated independently of microsaccades, maybe through oscillatory brain-state fluctuations; in this case, it is such modulations that “leak” into the motor system and trigger microsaccades. Here, motivated by (Hafed and Clark, 2002), in which no attentional effects were present in the absence of microsaccades, we tested the former hypothesis. We used real-time retinal image stabilization to introduce foveal motor errors at fixation (~0.06 deg) and causally drive microsaccades in an experimentally-controlled direction. We then presented peripheral (>5 deg) visual stimuli congruent or incongruent with microsaccade direction and recorded monkey superior colliculus (SC) activity. We found enhanced visual sensitivity and faster reaction times for microsaccade-congruent stimuli as a result of causally-generated microsaccades. In humans, we adapted a known task for pre-saccadic perceptual sensitivity (Rolfs & Carrasco, 2012) for microsaccades: subjects fixated, and we shifted the fixation spot by ~0.18 deg right or left to trigger microsaccades; the actual perceptual task (contrast comparison) was done for stimuli at 7 deg. Peripheral contrast sensitivity was enhanced before experimentally-manipulated microsaccades congruent with stimulus location, consistent with the neurophysiological results. Thus, foveal motor activity is sufficient to influence peripheral visual sensitivity.

Microsaccades: Empirical Research and Methodological Advances - Introduction to Part 1 of the Thematic Special Issue.

Microsaccades: Empirical Research and Methodological Advances - Introduction to Part 1 of the Thematic Special Issue.

Microsaccade generation requires a foveal anchor.

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.

Saliency and priority modulation in a pop-out paradigm: Pupil size and microsaccades

A salient stimulus can trigger a coordinated orienting response consisting of a saccade, pupil, and microsaccadic responses. Saliency models predict that the degree of visual conspicuity of all visual stimuli guides visual orienting. By presenting a multiple-item array that included an oddball colored item (pop-out), randomly mixed colored items (mixed-color), or single-color items (single-color), we examined the effects of saliency and priority (saliency + relevancy) on pupil size and microsaccade responses. Larger pupil responses were produced in the pop-out compared to the mixed-color or single-color conditions after stimulus presentation. However, the saliency modulation on microsaccades was not significant. Furthermore, although goal-relevancy information did not modulate pupil responses and microsaccade rate, microsaccade direction was biased toward the pop-out item when it was the subsequent saccadic target. Together, our results demonstrate saliency modulation on pupil size and priority effects on microsaccade direction during visual pop-out.

Microsaccades reflect the dynamics of misdirected attention in magic.

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

No supplementary evidence of attention to a spatial cue when saccadic facilitation is absent

Attending a location in space facilitates responses to targets at that location when the time between cue and target is short. Certain types of exogenous cues – such as sudden peripheral onsets – have been described as reflexive and automatic. Recent studies however, have been showing many cases where exogenous cues are less automatic than previously believed and do not always result in facilitation. A lack of the behavioral facilitation, however, does not automatically necessitate a lack of underlying attention to that location. We test exogenous cueing in two experiments where facilitation is and is not likely to be observed with saccadic responses. We also test alternate measures linked to the allocation of attention such as saccadic curvature, microsaccades and pupil size. As expected, we find early facilitation as measured by saccadic reaction time when CTOAs are predictable but not when they are randomized within a block. We find no impact of the cue on microsaccade direction for either experiment, and only a slight dip in the frequency of microsaccades after the cue. We do find that change in pupil size to the cue predicts the magnitude of the validity effect, but only in the experiment where facilitation was observed. In both experiments, we observed a tendency for saccadic curvature to deviate away from the cued location and this was stronger for early CTOAs and toward vertical targets. Overall, we find that only change in pupil size is consistent with observed facilitation. Saccadic curvature is influenced by the onset of the cue, buts its direction is indicative of oculomotor inhibition whether we see RT facilitation or not. Microsaccades were not diagnostic in either experiment. Finally, we see little to no evidence of attention at the cued location in any additional measures when facilitation of saccadic responses is absent.