The dynamics of microsaccade amplitude reflect shifting of covert attention.

Attention flexibly shifts between spatial locations to accommodate task demands. The present study examined if the dynamics of attentional shifting are seen in microsaccades whose direction has been shown to accompany the shifts of covert attention. In a spatial cueing task, the cue predicted the target location on 100%, 75%, or 50% of the trials. The results revealed that microsaccade rate and amplitude were both reduced following cue onset and then rebounded. Both microsaccade rate and amplitude were biased towards the opposite direction of the cue and then returned to the cued direction. Importantly, the cue validity modulated the temporal profile of microsaccade amplitude but had little impact on the temporal profile of microsaccade rate. In line with this, the cueing effect measured with target response accuracy was correlated with the microsaccade amplitude only. These results indicate that the temporal dynamics of microsaccade amplitude reflect shifting of covert attention.

Can Microsaccades Be Used for Biometrics?

Human eyes are in constant motion. Even when we fix our gaze on a certain point, our eyes continue to move. When looking at a point, scientists have distinguished three different fixational eye movements (FEM)-microsaccades, drift and tremor. The main goal of this paper is to investigate one of these FEMs-microsaccades-as a source of information for biometric analysis. The paper argues why microsaccades are preferred for biometric analysis over the other two fixational eye movements. The process of microsaccades' extraction is described. Thirteen parameters are defined for microsaccade analysis, and their derivation is given. A gradient algorithm was used to solve the biometric problem. An assessment of the weights of the different pairs of parameters in solving the biometric task was made.

Visual Strategies Underpinning the Spatiotemporal Demands During Visuomotor Tasks in Predicting Ball Direction.

We investigated gaze behavior of expert goalkeepers during the prediction of penalty kicks in different spatiotemporal constraints: penalties taken from 11 and 6 m. From 11 m, goalkeepers were more successful in predicting ball direction, with longer movement time initiation and a visual strategy with more fixations and greater saccade rates than penalties from 6 m, where they exhibited fewer fixations with higher microsaccade rates. As long as the opponent's distance is large and time pressure low, gaze can be frequently shifted between the kicker's body and the ball, due to the low cost of saccades. Conversely, when the objects are close, there is increased reliance on foveal and parafoveal information. In conclusion, when the spatiotemporal constraint is less severe, goalkeepers adopt a visual strategy with more fixations and small saccades. When the spatiotemporal constraint is more severe, they rely on peripheral vision to monitor kickers' movements through the use of microsaccades.

Small eye movements cannot be reliably measured by video-based P-CR eye-trackers.

For evaluating whether an eye-tracker is suitable for measuring microsaccades, Poletti & Rucci (2016) propose that a measure called 'resolution' could be better than the more established root-mean-square of the sample-to-sample distances (RMS-S2S). Many open questions exist around the resolution measure, however. Resolution needs to be calculated using data from an artificial eye that can be turned in very small steps. Furthermore, resolution has an unclear and uninvestigated relationship to the RMS-S2S and STD (standard deviation) measures of precision (Holmqvist & Andersson, 2017, p. 159-190), and there is another metric by the same name (Clarke, Ditterich, Drüen, Schönfeld, and Steineke 2002), which instead quantifies the errors of amplitude measurements. In this paper, we present a mechanism, the Stepperbox, for rotating artificial eyes in arbitrary angles from 1' (arcmin) and upward. We then use the Stepperbox to find the minimum reliably detectable rotations in 11 video-based eye-trackers (VOGs) and the Dual Purkinje Imaging (DPI) tracker. We find that resolution correlates significantly with RMS-S2S and, to a lesser extent, with STD. In addition, we find that although most eye-trackers can detect some small rotations of an artificial eye, the rotations of amplitudes up to 2∘ are frequently erroneously measured by video-based eye-trackers. We show evidence that the corneal reflection (CR) feature of these eye-trackers is a major cause of erroneous measurements of small rotations of artificial eyes. Our data strengthen the existing body of evidence that video-based eye-trackers produce errors that may require that we reconsider some results from research on reading, microsaccades, and vergence, where the amplitude of small eye movements have been measured with past or current video-based eye-trackers. In contrast, the DPI reports correct rotation amplitudes down to 1'.

Human-level saccade detection performance using deep neural networks.

Saccades are ballistic eye movements that rapidly shift gaze from one location of visual space to another. Detecting saccades in eye movement recordings is important not only for studying the neural mechanisms underlying sensory, motor, and cognitive processes, but also as a clinical and diagnostic tool. However, automatically detecting saccades can be difficult, particularly when such saccades are generated in coordination with other tracking eye movements, like smooth pursuits, or when the saccade amplitude is close to eye tracker noise levels, like with microsaccades. In such cases, labeling by human experts is required, but this is a tedious task prone to variability and error. We developed a convolutional neural network to automatically detect saccades at human-level accuracy and with minimal training examples. Our algorithm surpasses state of the art according to common performance metrics and could facilitate studies of neurophysiological processes underlying saccade generation and visual processing. NEW & NOTEWORTHY Detecting saccades in eye movement recordings can be a difficult task, but it is a necessary first step in many applications. We present a convolutional neural network that can automatically identify saccades with human-level accuracy and with minimal training examples. We show that our algorithm performs better than other available algorithms, by comparing performance on a wide range of data sets. We offer an open-source implementation of the algorithm as well as a web service.

Microsaccadic behavior when developing a complex dynamical activity.

Microsaccade are sensitive to changes of perceptual inputs as well as modulations of cognitive states. There are just a few works analyzing microsaccade while subjects are processing complex information and fewer when doing predictions about upcoming events. To evaluate whether contextual predictability would change microsaccadic behavior, we evaluated microsaccade of twenty one persons when reading 40 regular sentences and 40 proverbs. Analysis of microsaccade during reading proverbs and regular sentences revealed that microsaccade rate on words before maxjump, during maxjump and words after maxjump varied depending on the kind of sentence and on the word predictability. Maxjump was defined as the word with the largest difference between the cloze predictability of two consecutive words. Low and high predictable words demanded less or more microsaccade on words previous, during and on maxjump depending of the semantic context and of the readers' predictions of upcoming words.In summary, the present study shows that microsaccade' rate evidenced significant differences when reading proverbs and regular sentences. Hence, evaluation of microsaccade during reading sentences with different contextual predictability might provide information about specific effect of cue attention on complex task.

Microsaccadic responses indicate fast categorization of sounds: a novel approach to study auditory cognition.

The mental chronometry of the human brain's processing of sounds to be categorized as targets has intensively been studied in cognitive neuroscience. According to current theories, a series of successive stages consisting of the registration, identification, and categorization of the sound has to be completed before participants are able to report the sound as a target by button press after ∼300-500 ms. Here we use miniature eye movements as a tool to study the categorization of a sound as a target or nontarget, indicating that an initial categorization is present already after 80-100 ms. During visual fixation, the rate of microsaccades, the fastest components of miniature eye movements, is transiently modulated after auditory stimulation. In two experiments, we measured microsaccade rates in human participants in an auditory three-tone oddball paradigm (including rare nontarget sounds) and observed a difference in the microsaccade rates between targets and nontargets as early as 142 ms after sound onset. This finding was replicated in a third experiment with directed saccades measured in a paradigm in which tones had to be matched to score-like visual symbols. Considering the delays introduced by (motor) signal transmission and data analysis constraints, the brain must have differentiated target from nontarget sounds as fast as 80-100 ms after sound onset in both paradigms. We suggest that predictive information processing for expected input makes higher cognitive attributes, such as a sound's identity and category, available already during early sensory processing. The measurement of eye movements is thus a promising approach to investigate hearing.

The visual input to the retina during natural head-free fixation.

Head and eye movements incessantly modulate the luminance signals impinging onto the retina during natural intersaccadic fixation. Yet, little is known about how these fixational movements influence the statistics of retinal stimulation. Here, we provide the first detailed characterization of the visual input to the human retina during normal head-free fixation. We used high-resolution recordings of head and eye movements in a natural viewing task to examine how they jointly transform spatial information into temporal modulations. In agreement with previous studies, we report that both the head and the eyes move considerably during fixation. However, we show that fixational head and eye movements mostly compensate for each other, yielding a spatiotemporal redistribution of the input power to the retina similar to that previously observed under head immobilization. The resulting retinal image motion counterbalances the spectral distribution of natural scenes, giving temporal modulations that are equalized in power over a broad range of spatial frequencies. These findings support the proposal that "ocular drift," the smooth fixational motion of the eye, is under motor control, and indicate that the spatiotemporal reformatting caused by fixational behavior is an important computational element in the encoding of visual information.

Unsupervised clustering method to detect microsaccades.

Microsaccades, small involuntary eye movements that occur once or twice per second during attempted visual fixation, are relevant to perception, cognition, and oculomotor control and present distinctive characteristics in visual and oculomotor pathologies. Thus, the development of robust and accurate microsaccade-detection techniques is important for basic and clinical neuroscience research. Due to the diminutive size of microsaccades, however, automatic and reliable detection can be difficult. Current challenges in microsaccade detection include reliance on set, arbitrary thresholds and lack of objective validation. Here we describe a novel microsaccade-detecting method, based on unsupervised clustering techniques, that does not require an arbitrary threshold and provides a detection reliability index. We validated the new clustering method using real and simulated eye-movement data. The clustering method reduced detection errors by 62% for binocular data and 78% for monocular data, when compared to standard contemporary microsaccade-detection techniques. Further, the clustering method's reliability index was correlated with the microsaccade-detection error rate, suggesting that the reliability index may be used to determine the comparative precision of eye-tracking devices.

Temporal Changes in Fixational Eye Movements After Concussion in Adolescents and Adults: Preliminary Findings.

Concussions often involve ocular impairment and symptoms such as convergence insufficiency, accommodative insufficiency, blurred vision, diplopia, eye strain, and pain. Current clinical assessments of ocular function and symptoms rely on subjective symptom reporting and/or involve lengthy administration time. More objective, brief assessments of ocular function following concussion are warranted. The purpose of this study was to evaluate changes in fixational eye movements (FEMs) and their association with clinical outcomes including recovery time, symptoms, cognitive and vestibular/ocular motor impairment. Thirty-three athletes (13-27 years of age; 54.5% female) within 21 days of a diagnosed concussion participated in the study. A tracking scanning laser ophthalmoscope (TSLO) evaluated FEMs metrics during fixation on a center and corner target. Participants completed symptom (Post-Concussion Symptom Scale [PCSS]), cognitive (Immediate Post-concussion Assessment and Cognitive Testing [ImPACT], and Vestibular/Ocular Motor Screening (VOMS) evaluations. All measures were administered at the initial visit and following medical clearance, which was defined as clinical recovery. Changes in FEMs were calculated using paired-samples t tests. Linear regression (LR) models were used to evaluate the association of FEMs with clinical recovery. Pearson product-moment correlations were used to evaluate the associations among FEMs and clinical outcomes. On the center task, changes across time were supported for average microsaccade amplitude (p = 0.005; Cohen's d = 0.53), peak velocity of microsaccades (p = 0.01; d = 0.48), peak acceleration of microsaccades (p = 0.02; d = 0.48), duration of microsaccade (p < 0.001; d = 0.72), and drift vertical (p = 0.017; d = -0.154). The LR model for clinical recovery was significant (R2 = 0.37; p = 0.023) and retained average instantaneous drift amplitude (ß = 0.547) and peak acceleration of microsaccade (ß = 0.414). On the corner task, changes across time were supported for drift proportion (p = 0.03; d = 0.43). The LR model to predict clinical recovery was significant (R2 = 0.85; p = 0.004) and retained average amplitude of microsaccades (ß = 2.66), peak velocity of microsaccades (ß = -15.11), peak acceleration of microsaccades (ß = 12.56), drift horizontal (ß = 7.95), drift vertical (ß = 1.29), drift amplitude (ß = -8.34), drift proportion (ß = 0.584), instantaneous drift direction (ß = -0.26), and instantaneous drift amplitude (ß = 0.819). FEMs metrics were also associated with reports of nausea and performance within the domain of visual memory. The FEMs metric were also associated with PCSS, ImPACT, and VOMS clinical concussion outcomes, with the highest magnitude correlations between average saccade amplitude and VOMS symptoms of nausea and average instantaneous drift speed and ImPACT visual memory, respectively. FEMs metrics changed across time following concussion, were useful in predicting clinical recovery, and were correlated with clinical outcomes. FEMs measurements may provide objective data to augment clinical assessments and inform prognosis following this injury.

Jointly looking to the past and the future in visual working memory.

Working memory enables us to bridge past sensory information to upcoming future behaviour. Accordingly, by its very nature, working memory is concerned with two components: the past and the future. Yet, in conventional laboratory tasks, these two components are often conflated, such as when sensory information in working memory is encoded and tested at the same location. We developed a task in which we dissociated the past (encoded location) and future (to-be-tested location) attributes of visual contents in working memory. This enabled us to independently track the utilisation of past and future memory attributes through gaze, as observed during mnemonic selection. Our results reveal the joint consideration of past and future locations. This was prevalent even at the single-trial level of individual saccades that were jointly biased to the past and future. This uncovers the rich nature of working memory representations, whereby both past and future memory attributes are retained and can be accessed together when memory contents become relevant for behaviour.

Oculomotor Dysfunction in Idiopathic and LRRK2-Parkinson's Disease and At-Risk Individuals.

Background: Video-oculography constitutes a highly-sensitive method of characterizing ocular movements, which could detect subtle premotor changes and contribute to the early diagnosis of Parkinson's disease (PD). Objective: To investigate potential oculomotor differences between idiopathic PD (iPD) and PD associated with the G2019S variant of LRRK2 (L2PD), as well as to evaluate oculomotor function in asymptomatic carriers of the G2019S variant of LRRK2. Methods: The study enrolled 129 subjects: 30 PD (16 iPD, 14 L2PD), 23 asymptomatic carriers, 13 non-carrier relatives of L2PD patients, and 63 unrelated HCs. The video-oculographic evaluation included fixation, prosaccade, antisaccade, and memory saccade tests. Results: We did not find significant differences between iPD and L2PD. Compared to controls, PD patients displayed widespread oculomotor deficits including larger microsaccades, hypometric vertical prosaccades, increased latencies in all tests, and lower percentages of successful antisaccades and memory saccades. Non-carrier relatives showed oculomotor changes with parkinsonian features, such as fixation instability and hypometric vertical saccades. Asymptomatic carriers shared multiple similarities with PD, including signs of unstable fixation and hypometric vertical prosaccades; however, they were able to reach percentages of successful antisaccade and memory saccades similar to controls, although at the expense of longer latencies. Classification accuracy of significant oculomotor parameters to differentiate asymptomatic carriers from HCs ranged from 0.68 to 0.74, with BCEA, a marker of global fixation instability, being the parameter with the greatest classification accuracy. Conclusions: iPD and LRRK2-G2019S PD patients do not seem to display a differential oculomotor profile. Several oculomotor changes in asymptomatic carriers of LRRK2 mutations could be considered premotor biomarkers.

Microsaccades reflect attention shifts: a mini review of 20 years of microsaccade research.

Microsaccades are small, involuntary eye movements that occur during fixation. Since the 1950s, researchers have conducted extensive research on the role of microsaccades in visual information processing, and found that they also play an important role in human advanced visual cognitive activities. Research over the past 20 years further suggested that there is a close relationship between microsaccades and visual attention, yet lacking a timely review. The current article aims to provide a state-of-the-art review and bring microsaccades studies into the sight of attention research. We firstly introduce basic characteristics about microsaccades, then summarized the empirical evidence supporting the view that microsaccades can reflect both external (perception) and internal (working memory) attention shifts. We finally conclude and highlight three promising avenues for future research.

Consequences of eye movements for spatial selectivity.

What determines spatial tuning in the visual system? Standard views rely on the assumption that spatial information is directly inherited from the relative position of photoreceptors and shaped by neuronal connectivity.1,2 However, human eyes are always in motion during fixation,3,4,5,6 so retinal neurons receive temporal modulations that depend on the interaction of the spatial structure of the stimulus with eye movements. It has long been hypothesized that these modulations might contribute to spatial encoding,7,8,9,10,11,12 a proposal supported by several recent observations.13,14,15,16 A fundamental, yet untested, consequence of this encoding strategy is that spatial tuning is not hard-wired in the visual system but critically depends on how the fixational motion of the eye shapes the temporal structure of the signals impinging onto the retina. Here we used high-resolution techniques for eye-tracking17 and gaze-contingent display control18 to quantitatively test this distinctive prediction. We examined how contrast sensitivity, a hallmark of spatial vision, is influenced by fixational motion, both during normal active fixation and when the spatiotemporal stimulus on the retina is altered to mimic changes in fixational control. We showed that visual sensitivity closely follows the strength of the luminance modulations delivered within a narrow temporal bandwidth, so changes in fixational motion have opposite visual effects at low and high spatial frequencies. By identifying a key role for oculomotor activity in spatial selectivity, these findings have important implications for the perceptual consequences of abnormal eye movements, the sources of perceptual variability, and the function of oculomotor control.

Fixational saccades reflect volitional action preparation.

Human volitional actions are preceded by preparatory processes, a critical mental process of cognitive control for future behavior. Volitional action preparation is regulated by large-scale neural circuits including the cerebral cortex and the basal ganglia. Because volitional action preparation is a covert process, the network dynamics of such neural circuits have been examined by neuroimaging and recording event-related potentials. Here, we examined whether such covert processes can be measured by the overt responses of fixational saccades (including microsaccades), the largest miniature eye movements that occur during eye fixation. We analyzed fixational saccades while adult humans maintained fixation on a central visual stimulus as they prepared to generate a volitional saccade in response to peripheral stimulus appearance. We used the antisaccade paradigm, in which subjects generate a saccade toward the opposite direction of a peripheral stimulus. Appropriate antisaccade performance requires the following two aspects of volitional control: 1) facilitation of saccades away from the stimulus and 2) suppression of inappropriate saccades toward the stimulus. We found that fixational saccades that occurred before stimulus appearance reflected the dual preparatory states of saccade facilitation and suppression and correlated with behavioral outcome (i.e., whether subjects succeeded or failed to cancel inappropriate saccades toward the stimulus). Moreover, fixational saccades explained a large proportion of individual differences in behavioral performance (poor/excellent) across subjects. These results suggest that fixational saccades predict the outcome of future volitional actions and may be used as a potential biomarker to detect people with difficulties in volitional action preparation.

Microsaccades transiently lateralise EEG alpha activity.

The lateralisation of 8-12 Hz 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.

Building a decoder of perceptual decisions from microsaccades and pupil size.

Many studies have reported neural correlates of visual awareness across several brain regions, including the sensory, parietal, and frontal areas. In most of these studies, participants were instructed to explicitly report their perceptual experience through a button press or verbal report. It is conceivable, however, that explicit reporting itself may trigger specific neural responses that can confound the direct examination of the neural correlates of visual awareness. This suggests the need to assess visual awareness without explicit reporting. One way to achieve this is to develop a technique to predict the visual awareness of participants based on their peripheral responses. Here, we used eye movements and pupil sizes to decode trial-by-trial changes in the awareness of a stimulus whose visibility was deteriorated due to adaptation-induced blindness (AIB). In the experiment, participants judged whether they perceived a target stimulus and rated the confidence they had in their perceptual judgment, while their eye movements and pupil sizes were recorded. We found that not only perceptual decision but also perceptual confidence can be separately decoded from the eye movement and pupil size. We discuss the potential of this technique with regard to assessing visual awareness in future neuroimaging experiments.

EEG Signals Index a Global Signature of Arousal Embedded in Neuronal Population Recordings.

Electroencephalography (EEG) has long been used to index brain states, from early studies describing activity in the presence and absence of visual stimulation to modern work employing complex perceptual tasks. These studies have shed light on brain-wide signals but often lack explanatory power at the single neuron level. Similarly, single neuron recordings can suffer from an inability to measure brain-wide signals accessible using EEG. Here, we combined these techniques while monkeys performed a change detection task and discovered a novel link between spontaneous EEG activity and a neural signal embedded in the spiking responses of neuronal populations. This "slow drift" was associated with fluctuations in the subjects' arousal levels over time: decreases in prestimulus α power were accompanied by increases in pupil size and decreases in microsaccade rate. These results show that brain-wide EEG signals can be used to index modes of activity present in single neuron recordings, that in turn reflect global changes in brain state that influence perception and behavior.

Stochastic Physiological Gaze-Evoked Nystagmus With Slow Centripetal Drift During Fixational Eye Movements at Small Gaze Eccentricities.

Involuntary eye movement during gaze (GZ) fixation, referred to as fixational eye movement (FEM), consists of two types of components: a Brownian motion like component called drifts-tremor (DRT) and a ballistic component called microsaccade (MS) with a mean saccadic amplitude of about 0.3° and a mean inter-MS interval of about 0.5 s. During GZ fixation in healthy people in an eccentric position, typically with an eccentricity more than 30°, eyes exhibit oscillatory movements alternating between centripetal drift and centrifugal saccade with a mean saccadic amplitude of about 1° and a period in the range of 0.5-1.0 s, which has been known as the physiological gaze-evoked nystagmus (GEN). Here, we designed a simple experimental paradigm of GZ fixation on a target shifted horizontally from the front-facing position with fewer eccentricities. We found a clear tendency of centripetal DRT and centrifugal MS as in GEN, but with more stochasticity and with slower drift velocity compared to GEN, even during FEM at GZ positions with small eccentricities. Our results showed that the target shift-dependent balance between DRT and MS achieves the GZ bounded around each of the given targets. In other words, GZ relaxes slowly with the centripetal DRT toward the front-facing position during inter-MS intervals, as if there always exists a quasi-stable equilibrium posture in the front-facing position, and MS actions pull GZ intermittently back to the target position in the opposite direction to DRT.

The Role of Blinks, Microsaccades and their Retinal Consequences in Bistable Motion Perception.

Eye-related movements such as blinks and microsaccades are modulated during bistable perceptual tasks. However, if they play an active role during internal perceptual switches is not known. We conducted two experiments involving an ambiguous plaid stimulus, wherein participants were asked to continuously report their percept, which could consist of either unidirectional coherent or bidirectional component movement. Our main results show that blinks and microsaccades did not facilitate perceptual switches. On the contrary, a reduction in eye movements preceded the perceptual switch. Blanks, on the other hand, thought to mimic the retinal consequences of a blink, consistently led to a switch. Through the timing of the blank-introduced perceptual change, we were able to estimate the delay between the internal switch and the response. This delay further allowed us to evaluate that the reduction in blink probability co-occurred with the internal perceptual switch. Additionally, our results indicate that distinct internal processes underlie the switch to coherent vs. component percept. Blanks exclusively facilitated a switch to the coherent percept, and only the switch to coherent percept was followed by an increase in blink rate. In a second study, we largely replicated the findings and included a microsaccade analysis. Microsaccades only showed a weak relation with perceptual switches, but their direction was correlated with the perceived motion direction. Nevertheless, our data suggests an interaction between microsaccades and blinks by showing that microsaccades were differently modulated around blinks compared with blanks. This study shows that a reduction in eye movements precedes internal perceptual switches indicating that the rate of blinks can set the stage for a reinterpretation of sensory input. While a perceptual switch based on changed sensory input usually leads to an increase in blink rate, such an increase was only present after the perceptual switch to coherent motion but absent after the switch to component percept. This provides evidence of different underlying mechanism or internal consequence of the two perceptual switches and suggests that blinks can uncover differences in internal percept-related processes that are not evident from the percept itself.