Changes in visibility as a function of spatial frequency and microsaccade occurrence

Fixational eye movements (FEMs), including microsaccades, drift, and tremor, shift our eye position during ocular fixation, producing retinal motion that is thought to help visibility by counteracting neural adaptation to unchanging stimulation. Yet, how each FEM type influences this process is still debated. Recent studies found little to no relationship between microsaccades and visual perception of spatial frequencies (SF). However, these conclusions were based on coarse analyses that make it hard to appreciate the actual effects of microsaccades on target visibility as a function of SF. Thus, how microsaccades contribute to the visibility of stimuli of different SFs remains unclear. Here, we asked how the visibility of targets of various SFs changed over time, in relationship with concurrent microsaccade production. Participants continuously reported on changes in target visibility, allowing us to time‐lock ongoing changes in microsaccade parameters to perceptual transitions in visibility. Microsaccades restored/increased the visibility of low SF targets more efficiently than that of high SF targets. Yet, microsaccade rates rose before periods of increased visibility, and dropped before periods of diminished visibility, for all the SFs tested, suggesting that microsaccades boosted target visibility across a wide range of SFs. Our data also indicate that visual stimuli fade/become harder to see less often in the presence of microsaccades. In addition, larger microsaccades restored/increased target visibility more effectively than smaller microsaccades. These combined results support the proposal that microsaccades enhance visibility across a broad variety of SFs.     

Microsaccade and drift dynamics reflect mental fatigue

Our eyes are always in motion. Even during periods of relative fixation we produce so‐called ‘fixational eye movements’, which include microsaccades, drift and tremor. Mental fatigue can modulate saccade dynamics, but its effects on microsaccades and drift are unknown. Here we asked human subjects to perform a prolonged and demanding visual search task (a simplified air traffic control task), with two difficulty levels, under both free‐viewing and fixation conditions. Saccadic and microsaccadic velocity decreased with time‐on‐task whereas drift velocity increased, suggesting that ocular instability increases with mental fatigue. Task difficulty did not influence eye movements despite affecting reaction times, performance errors and subjective complexity ratings. We propose that variations in eye movement dynamics with time‐on‐task are consistent with the activation of the brain's sleep centers in correlation with mental fatigue. Covariation of saccadic and microsaccadic parameters moreover supports the hypothesis of a common generator for microsaccades and saccades. We conclude that changes in fixational and saccadic dynamics can indicate mental fatigue due to time‐on‐task, irrespective of task complexity. These findings suggest that fixational eye movement dynamics have the potential to signal the nervous system's activation state.     

Modulation of microsaccades in monkey during a covert visual attention task

The use of awake, fixating monkeys in neuroscience has allowed significant advances in understanding numerous brain functions. However, fixation is an active process, with the occurrence of incessant eye movements, including rapid ones called microsaccades. Even though microsaccades have been shown to be modulated by stimulus and cognitive processes in humans, it is not known to what extent these results are similar in monkeys or why they occur. Here, we analyzed the stimulus-, context-, and attention-related changes in microsaccades while monkeys performed a challenging visual attention task. The distributions of microsaccade times were highly stereotypical across thousands of trials in the task. Moreover, in epochs of the task in which animals anticipated the occurrence of brief stimulus probes, microsaccade frequency decreased to a rate of less than one movement per second even on long multisecond trials. These effects were explained by the observation that microsaccades occurring at the times of the brief probes were sometimes associated with reduced perceptual performance. Microsaccade directions also exhibited temporal modulations related to the attentional demands of the task, like earlier studies in humans, and were more likely to be directed toward an attended location on successfully performed trials than on unsuccessfully completed ones. Our results show that microsaccades in nonhuman primates are correlated with the allocation of stimulus-evoked and sustained covert attention. We hypothesize that involvement of the superior colliculus in microsaccade generation and attentional allocation contributes to these observations. More importantly, our results clarify the potential role of these eye movements in modifying behavior and neural activity.     

Superior colliculus inactivation alters the relationship between covert visual attention and microsaccades

Microsaccades are tiny saccades that occur during gaze fixation. Whereas these movements have traditionally been viewed as random, it was recently discovered that microsaccade directions can be significantly biased by covertly attended visual stimuli. The detailed mechanisms mediating such a bias are neither known nor immediately obvious, especially because the amplitudes of the movements influenced by attentional cueing could be up to two orders of magnitude smaller than the eccentricity of the attended location. Here, we tested whether activity in the peripheral superior colliculus (SC) is necessary for this correlation between attentional cueing and microsaccades. We reversibly and focally inactivated SC neurons representing peripheral regions of visual space while rhesus monkeys performed a demanding covert visual attention task. The normal bias of microsaccade directions observed in each monkey before SC inactivation was eliminated when a cue was placed in the visual region affected by the inactivation; microsaccades were, instead, biased away from the affected visual space. When the cue was placed at another location unaffected by SC inactivation, the baseline cue‐induced bias of microsaccade directions remained mostly intact, because the cue was in unaffected visual space, and any remaining changes were again explained by a repulsion of microsaccades away from the inactivated region. Our results indicate that peripheral SC activity is required for the link between microsaccades and the cueing of covert visual attention, and that it could do so by altering the probability of triggering microsaccades without necessarily affecting the motor generation of these movements.     

Individual neurons in the caudal fastigial oculomotor region convey information on both macro‐ and microsaccades

Recent studies have suggested that microsaccades, the small amplitude saccades made during fixation, are precisely controlled. Two lines of evidence suggest that the cerebellum plays a key role not only in improving the accuracy of macrosaccades but also of microsaccades. First, lesions of the fastigial oculomotor regions (FOR) cause horizontal dysmetria of both micro‐ and macrosaccades. Secondly, our previous work on Purkinje cell simple spikes in the oculomotor vermis (OV) has established qualitatively similar response preferences for these two groups of saccades. In this work, we investigated the control signals for micro‐ and macrosaccades in the FOR, the target of OV Purkinje cell axons. We found that the same FOR neurons discharged for micro‐ and macrosaccades. For both groups of saccades, FOR neurons exhibited very similar dependencies of their discharge strength on direction and amplitude and very similar burst onset time differences for ipsi‐ and contraversive saccades and, in both, response duration reflected saccade duration, at least at the population level. An intriguing characteristic of microsaccade‐related responses is that immediate pre‐saccadic firing rates decreased with distance to the target center, a pattern that strikingly parallels the eye position dependency of both microsaccade metrics and frequency, which may suggest a potential neural mechanism underlying the role of FOR in fixation. Irrespective of this specific consideration, our study supports the view that microsaccades and macrosaccades share the same cerebellar circuitry and, in general, further strengthens the notion of a microsaccade–macrosaccade continuum.     

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.     

Accumulation of non‐numerical evidence during nonsymbolic number processing in the brain: An fMRI study

Behavioral evidence has shown that when performing a nonsymbolic number comparison task (e.g., deciding which of two dot arrays contains more dots), participants' responses are sensitive to affected by both numerical (e.g., number of items) and non‐numerical magnitudes (i.e., area, density, etc.). Thus far it is unclear what brain circuits support this process of accumulating non‐numerical variables during nonsymbolic number processing. To investigate this, 21 adult participants were asked to engage in a dot comparison task. To measure the neural correlates of accumulating numerical and non‐numerical variables, we manipulated the number of the non‐numerical magnitudes that were congruent (correlated with number) or incongruent (anticorrelated with number). In a control task, participants were asked to choose the darker of two gray rectangles (brightness task). The tasks were matched in terms of their difficulty. The results of a whole brain analysis for regions sensitive to the congruity of numerical and non‐numerical magnitudes revealed a region in the right inferior frontal gyrus (rIFG). Activation in this region was found to be correlated with the relative congruency of numerical and non‐numerical magnitudes. In contrast, this region was not modulated by difficulty of the brightness control task. Accordingly in view of these findings, we suggest that the rIFG supports the accumulation of non‐numerical magnitudes that are positively correlated with number. Therefore taken together, this study reveals a brain region whose pattern of activity is influenced by the congruency between numerical and non‐numerical variables during nonsymbolic number judgments. Hum Brain Mapp 38:4908–4921, 2017. © 2017 Wiley Periodicals, Inc.     

Microsaccades and blinks trigger illusory rotation in the "rotating snakes" illusion

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

Fixational eye movements in Tourette syndrome

Studies of saccadic eye movements in subjects with Tourette syndrome (TS) have provided additional evidence that there is a link between TS symptoms and deficits in fronto-striato-thalamic networks. These studies revealed impaired timing and inhibition of saccades. We compared fixational eye movements, such as microsaccades and ocular drifts, in subjects with TS and healthy controls.We measured horizontal and vertical eye positions with video-oculography in 14 subjects with Tourette syndrome. We found reduced microsaccade amplitude but increased time between adjacent microsaccades (intersaccadic interval). Hence, the rate of microsaccades was reduced in subjects with TS compared to controls. Measure of ocular stability during intersaccadic intervals revealed increased drift velocity and increased variance in eye position. We hypothesize that increased activity of the direct fronto-striatal pathway and the resulting reduction in basal ganglia outflow targeting the superior colliculus fixation zone affect the rate and amplitude of microsaccades in subjects with TS. The resulting impairment in frontal eye field fixation leads to increased drifts during intersaccadic interval in subjects with TS. Possible clinical implication for these results is that fixational eye movements can be objective biological markers of TS.     

Attention to number: The convergence of numerical magnitude processing,attention, and mathematics in the inferior frontal gyrus

Research indicates that the neurocognitive system representing nonsymbolic numerical magnitudes is foundational for the development of mathematical competence. However, recent studies found that the most common task used to measure numerical acuity, the nonsymbolic number comparison task, is heavily influenced by non‐numerical visual parameters of stimuli that increase executive function demands. Further, this influence may be a confound invalidating theoretical accounts of the relation between number comparison performance and mathematical competence. Instead of acuity, the relation may depend on one's ability to attend to numerical information in the face of competing, non‐numerical cues. The current study investigated this issue by measuring neural activity associated with numerical magnitude processing acuity, domain‐general attention, and selective attention to number via functional magnetic resonance imaging while children 8–11 years old completed a nonsymbolic number comparison task and a flanker task. Results showed that activation in the right inferior frontal gyrus during incongruent versus congruent trials of the comparison task, our construct for attention to number, predicted mathematics achievement after controlling for verbal IQ, flanker accuracy rate, and the neural congruency effect from the flanker task. In contrast, activity in frontal and parietal regions responding to differences in difficulty of numerical comparisons, our construct for numerical magnitude processing acuity, did not correlate with achievement. Together, these findings suggest a need to reframe existing models of the relation between number processing and math competence to include the interaction between attention and use of numerical information, or in other words “attention to number.”     

Are you ready? I can tell by looking at your microsaccades

The direction of microsaccades has been shown to be biased by the allocation of spatial attention. Here, we investigated whether the cognitive processes involved in preparing to respond to an upcoming target can modulate the microsaccadic response. Specifically, we found that optimal manual response preparation, reflected by faster response times, was associated with a reduction in the absolute frequency of microsaccades. The present results are consistent with previous studies suggesting a relationship between oculomotor activity and different sorts of motor responses. Our findings, however, surprisingly demonstrate that the effect of preparation and stimulus expectation extends to an automatic and unconscious oculomotor activity such as microsaccade execution.     

Coherent illusory contours reduce microsaccade frequency

Synchronized high-frequency gamma band oscillations (30-100 Hz) are thought to mediate the binding of single visual features into whole-object representations. For example, induced gamma band oscillations (iGBRs) have been recorded ∼280 ms after the onset of a coherent Kanizsa triangle, but not after an incoherent equivalent shape. However, several recent studies have provided evidence that the EEG-recorded iGBR may be a by-product of small saccadic eye movements (microsaccades). Considering these two previous findings, one would hypothesis that there should be more microsaccades following the onset of a coherent Kanizsa triangle. However, we found that microsaccade rebound rate was significantly higher after an incoherent triangle was presented. This result suggests that microsaccades are not a reliable indicator of perceptual binding, and, more importantly, implies that iGBR cannot be universally produced by ocular artefacts.     

Individual differences in stop‐related activity are inflated by the adaptive algorithm in the stop signal task

Research using the Stop Signal Task employing an adaptive algorithm to accommodate individual differences often report inferior performance on the task in individuals with ADHD, OCD, and substance use disorders compared to non‐clinical controls. Furthermore, individuals with deficits in inhibitory control tend to show reduced neural activity in key inhibitory regions during successful stopping. However, the adaptive algorithm systematically introduces performance‐related differences in objective task difficulty that may influence the estimation of individual differences in stop‐related neural activity. This report examines the effect that these algorithm‐related differences have on the measurement of neural activity during the stop signal task. We compared two groups of subjects (n = 210) who differed in inhibitory ability using both a standard fMRI analysis and an analysis that resampled trials to remove the objective task difficulty confound. The results show that objective task difficulty influences the magnitude of between‐group differences and that controlling for difficulty attenuates stop‐related activity differences between superior and poor inhibitors. Specifically, group differences in the right inferior frontal gyrus, right middle occipital gyrus, and left inferior frontal gyrus are diminished when differences in objective task difficulty are controlled for. Also, when objective task difficulty effects are exaggerated, group differences in stop related activity emerge in other regions of the stopping network. The implications of these effects for how we interpret individual differences in activity levels are discussed.     

A model-based theory on the signal transformation for microsaccade generation

The eyes are continuously fluctuating even during fixation. The fluctuations are called miniature eye movements and consist of microsaccades, drifts, and tremors. It has been revealed that these miniature eye movements aid our vision; they improve the visibility of high spatial frequency components, and prevent retinal adaptation during fixation. Although the functional roles of the miniature eye movements have gradually been uncovered, their generation mechanism remains a mystery. Here, we focused on microsaccades, and constructed a neuronal network model to explore their generation mechanism. Several lines of evidence ensure that microsaccades and saccades share the same neuronal circuitry because they fall on the same main sequence, a relationship between their amplitudes and peak velocities. In the saccade pathway, saccade commands generated in the superior colliculus are relayed to motoneurons via burst neurons (BNs) and the integrator network. The BNs are inhibited by omnipause neurons (OPNs) except when saccades are generated. We configured a model for microsaccades based on the well-defined saccade neuronal pathway including tonic neurons, BNs, OPNs, the integrator network, and the eye plant. The model successfully reproduced various characteristics of microsaccade: square-wave jerk, single-sided microsaccades, and the main sequence. Moreover, during microsaccades, BNs showed low-rate spikes due to a partial release from the OPN inhibition. These results suggest that microsaccades are generated when BNs are partially, but not completely, released from tonic inhibition by OPNs during fixation, in contrast to the generation of ordinary saccades in which OPNs pause firing and release BNs from their strong inhibition.     

Task difficulty in a simultaneous face matching task modulates activity in face fusiform area

The level of difficulty of a task can alter the neural network that activates for performance of the task. Previous studies have shown increased activation with task difficulty in the frontal lobes while the effects in the extrastriate visual areas have been unclear. We hypothesized that the face fusiform area (FFA), an area specialized for face processing, would increase activation as task difficulty increased in a face matching task. The difficulty level was increased by degrading the quality of the images. The degradation levels were 10%, 20%, 40% and 60%. Based on the correct response rate, the data were divided into a baseline level (composed of non-degraded and 10% degraded images) and a difficult level (composed of the 20%, 40% and 60% degraded images). Brain activation was measured using functional magnetic resonance imaging. The baseline face matching task activated a wide network of regions that included bilaterally the occipital, temporal and parietal lobes and the right frontal lobe. A novel behavioral finding was that task difficulty did not linearly increase with image degradation. The novel brain imaging finding was that the FFA is modulated by task difficulty and performance in the task was linearly correlated to activation in FFA. In addition, we found that activation in the dorsolateral prefrontal cortex (DLPFC) had increased activation as task difficulty increased. When adding the response time as a covariate, the differences in the DLPFC did not remain statistically significant. Increased task difficulty also led to a decrease in activation of visual areas in the extrastriate cortex. Task difficulty increased activation in the FFA to enhance the face processing and suppressed activation in visual extrastriate areas that processed low level properties of the stimuli. Task difficulty led to enhanced response in the FFA and suppressed response in other visual areas.     

Postural responses to a suprapostural visual task among children with and without developmental coordination disorder

We sought to determine the effects of varying the perceptual demands of a suprapostural visual task on the postural activity of children with developmental coordination disorder (DCD), and typically developing children (TDC). Sixty-four (32 per group) children aged between 9 and 10 years participated. In a within-participants design, each child performed a signal detection task at two levels of difficulty, low (LD) and high difficulty (HD). During performance of the signal detection tasks we recorded positional variability of the head and torso using a magnetic tracking system. We found that task difficulty had a greater effect on task performance among the TDC group than among children with DCD. Overall positional variability was greater the DCD group than in the TDC group. In the TDC group, positional variability was reduced during performance of the HD task, relative to sway during performance of the LD task. In the DCD group, positional variability was greater during performance of the HD task than during performance of the LD task. In children, DCD may reduce the strength of functional integration of postural activity with the demands of suprapostural visual tasks.     

Mechanisms for generating and compensating for the smallest possible saccades

Microsaccades are small eye movements that occur during gaze fixation. Although taking place only when we attempt to stabilize gaze position, microsaccades can be understood by relating them to the larger voluntary saccades, which abruptly shift gaze position. Starting from this approach to microsaccade analysis, I show how it can lead to significant insight about the generation and functional role of these eye movements. Like larger saccades, microsaccades are now known to be generated by brainstem structures involved not only in compiling motor commands for eye movements, but also in identifying and selecting salient target locations in the visual environment. In addition, these small eye movements both influence and are influenced by sensory and cognitive processes in various areas of the brain, and in a manner that is similar to the interactions between larger saccades and sensory or cognitive processes. By approaching the study of microsaccades from the perspective of what has been learned about their larger counterparts, we are now in a position to make greater strides in our understanding of the function of the smallest possible saccadic eye movements.     

Microsaccadic efficacy and contribution to foveal and peripheral vision

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

Effects of ageing on cognitive task preparation as reflected by event-related potentials.

OBJECTIVE: The anticipation of complex cognitive tasks involves effortful preparation being reflected in the contingent negative variation (CNV) of the event-related potential. In the literature there are contradictory results concerning the effect of age on this potential. We wanted to investigate effects of age, time-on-task, and task difficulty on the CNV. METHOD: Young and middle-aged participants performed a visual search and a non-search task during an early and a late phase of a 6-h session. RESULTS: Performance data revealed increased response times and error rates for middle-aged vs. young participants. Most importantly, an increased frontal CNV amplitude was found for the older participants, especially pronounced in the search task. A late positivity which was elicited to the offset of the preceding stimulus was increased for the middle-aged vs. young group in the visual search task only. There was no effect of time-on-task on performance, but the CNV became larger with time-on-task in the search task while it became smaller in the non-search task. CONCLUSIONS: The results suggest an enhancement of effortful task preparation for middle-aged participants especially when the task is difficult. SIGNIFICANCE: This underlines the role of the CNV as a neurophysiological indicator for effortful cognitive preparation.     

Functional magnetic resonance imaging movers and shakers: Does subject‐movement cause sampling bias?

Head movement during functional magnetic resonance imaging (fMRI) degrades data quality. The effects of small movements can be ameliorated during data postprocessing, but data associated with severe movement is frequently discarded. In discarding these data, it is often assumed that head‐movement is a source of random error, and that data can be discarded from subjects with severe movement without biasing the sample. We tested this assumption by examining whether head movement was related to task difficulty and cognitive status among persons with multiple sclerosis (MS). Thirty‐four persons with MS were scanned while performing a working memory task with three levels of difficulty (the N‐back task). Maximum movement (angle, shift) was estimated for each difficulty level. Cognitive status was assessed by combining performance on a working memory and processing speed task. An interaction was found between task difficulty and cognitive status (high vs. low cognitive ability): there was a linear increase in movement as task difficulty increased that was larger among subjects with lower cognitive ability. Analyses of the signal‐to‐noise ratio (SNR) confirmed that increases in movement degraded data quality. Similar, though far smaller, effects were found in a cohort of healthy control (HC) subjects. Therefore, discarding data with severe movement artifact may bias MS samples such that only those with less‐severe cognitive impairment are included in the analyses. However, even if such data are not discarded outright, subjects who move more (MS and HC) will contribute less to the group‐level results because of degraded SNR. Hum Brain Mapp 35:1–13, 2014. © 2012 Wiley Periodicals, Inc.