Predictive posture stabilization before contact with moving objects: equivalence of smooth pursuit tracking and peripheral vision.

Postural stabilization is essential to effectively interact with our environment. Humans preemptively adjust their posture to counteract impending disturbances, such as those encountered during interactions with moving objects, a phenomenon known as anticipatory postural adjustments (APAs). APAs are thought to be influenced by predictive models that incorporate object motion via retinal motion and extraretinal signals. Building on our previous work that examined APAs in relation to the perceived momentum of moving objects, here we explored the impact of object motion within different visual field sectors on the human capacity to anticipate motion and prepare APAs for contact between virtual moving objects and the limb. Participants interacted with objects moving toward them under different gaze conditions. In one condition, participants fixated on either a central point (central fixation) or left-right of the moving object (peripheral fixation), whereas in another, they followed the moving object with smooth pursuit eye movements (SPEMs). We found that APAs had the smallest magnitude in the central fixation condition and that no notable differences in APAs were apparent between the SPEM and peripheral fixation conditions. This suggests that the visual system can accurately perceive motion of objects in peripheral vision for posture stabilization. Using Bayesian model averaging, we also evaluated the contribution of different gaze variables, such as eye velocity and gain (ratio of eye and object velocity) and showed that both eye velocity and gain signals were significant predictors of APAs. Taken together, our study underscores the roles of oculomotor signals in the modulation of APAs.NEW & NOTEWORTHY We show that the human visuomotor system can detect motion in peripheral vision and make anticipatory adjustments to posture before contact with moving objects, just as effectively as when the eye movement system tracks those objects with smooth pursuit eye movements. These findings pave the way for research into how age-induced changes in spatial vision, eye movements, and motion perception could affect the control of limb movements and postural stability during motion-mediated interactions with objects.

Oculomotor atypicalities in motor neurone disease: a systematic review.

Introduction: Cognitive dysfunction is commonplace in Motor Neurone Disease (MND). However, due to the prominent motor symptoms in MND, assessing patients' cognitive function through traditional cognitive assessments, which oftentimes require motoric responses, may become increasingly challenging as the disease progresses. Oculomotor pathways are apparently resistant to pathological degeneration in MND. As such, abnormalities in oculomotor functions, largely driven by cognitive processes such as saccades and smooth pursuit eye movement, may be reflective of frontotemporal cognitive deficits in MND. Thus, saccadic and smooth pursuit eye movements may prove to be ideal mechanistic markers of cognitive function in MND. Methods: To ascertain the utility of saccadic and smooth pursuit eye movements as markers of cognitive function in MND, this review summarizes the literature concerning saccadic and smooth pursuit eye movement task performance in people with MND. Results and discussion: Of the 22 studies identified, noticeable patterns suggest that people with MND can be differentiated from controls based on antisaccade and smooth pursuit task performance, and thus the antisaccade task and smooth pursuit task may be potential candidates for markers of cognition in MND. However, further studies which ascertain the concordance between eye tracking measures and traditional measures of cognition are required before this assumption is extrapolated, and clinical recommendations are made. Systematic review registration: https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=376620, identifier CRD42023376620.

Evidence from comprehensive independent validation studies for smooth pursuit dysfunction as a sensorimotor biomarker for psychosis.

Smooth pursuit eye movements are considered a well-established and quantifiable biomarker of sensorimotor function in psychosis research. Identifying psychotic syndromes on an individual level based on neurobiological markers is limited by heterogeneity and requires comprehensive external validation to avoid overestimation of prediction models. Here, we studied quantifiable sensorimotor measures derived from smooth pursuit eye movements in a large sample of psychosis probands (N = 674) and healthy controls (N = 305) using multivariate pattern analysis. Balanced accuracies of 64% for the prediction of psychosis status are in line with recent results from other large heterogenous psychiatric samples. They are confirmed by external validation in independent large samples including probands with (1) psychosis (N = 727) versus healthy controls (N = 292), (2) psychotic (N = 49) and non-psychotic bipolar disorder (N = 36), and (3) non-psychotic affective disorders (N = 119) and psychosis (N = 51) yielding accuracies of 65%, 66% and 58%, respectively, albeit slightly different psychosis syndromes. Our findings make a significant contribution to the identification of biologically defined profiles of heterogeneous psychosis syndromes on an individual level underlining the impact of sensorimotor dysfunction in psychosis.

Video-Oculography Assessment in Neurodegenerative Ataxias and Niemann Pick Type C.

Introduction: Deceleration of vertical saccades, an early and characteristic finding of Niemann-Pick Type C (NP-C), may help diagnosis. Our aim in this study was to demonstrate the role of video-oculography (VOG), in the differential diagnosis of ataxia syndromes, particularly of NP-C, using this technique in the evaluation of saccadic velocity and smooth pursuit gain of ataxia patients. Methods: We recruited consecutive 50 ataxia patients and 50 healthy control subjects who were age and sex-matched with the patient group. Saccadic eye movements and smooth pursuit eye movements for different angles and different directions from patients and healthy subjects were recorded by using VOG. Results: Saccadic eye movement velocity and smooth pursuit gain values of the patients were significantly lower in all directions and at all angles as compared to healthy subjects. In the patient group, 3 cases out of 50 were selected as suspected NP-C, based on the dissociation between their markedly impaired vertical saccadic velocity and near normal to slightly impaired horizontal one and relatively intact smooth pursuit eye movements; the diagnoses in all 3 cases were confirmed with positive genetic testing, and thereupon Miglustat treatment was started. Conclusion: Our findings support that cerebellar pathology in degenerative ataxia patients is associated with both impaired saccadic velocity and smooth pursuit gain, whereas in NP-C, only the impaired vertical saccades as opposed to relatively preserved other eye movements are seemingly a diagnostic marker for the entity. We conclude that recording of eye movements could be useful for differential diagnosis and monitorization of the treatment of ataxia syndromes as an easy and objective method.

Interactions between Saccades and Smooth Pursuit Eye Movements in Marmosets.

Animals use a combination of eye movements to track moving objects. These different eye movements need to be coordinated for successful tracking, requiring interactions between the systems involved. Here, we study the interaction between the saccadic and smooth pursuit eye movement systems in marmosets. Using a single-target pursuit task, we show that saccades cause an enhancement in pursuit following a saccade. Using a two-target pursuit task, we show that this enhancement in pursuit is selective toward the motion of the target selected by the saccade, irrespective of any biases in pursuit prior to the saccade. These experiments highlight the similarities in the functioning of saccadic and smooth pursuit eye movement systems across primates.

Brain representations of motion and position in the double-drift illusion.

In the 'double-drift' illusion, local motion within a window moving in the periphery of the visual field alters the window's perceived path. The illusion is strong even when the eyes track a target whose motion matches the window so that the stimulus remains stable on the retina. This implies that the illusion involves the integration of retinal signals with non-retinal eye-movement signals. To identify where in the brain this integration occurs, we measured BOLD fMRI responses in visual cortex while subjects experienced the double-drift illusion. We then used a combination of univariate and multivariate decoding analyses to identify (1) which brain areas were sensitive to the illusion and (2) whether these brain areas contained information about the illusory stimulus trajectory. We identified a number of cortical areas that responded more strongly during the illusion than a control condition that was matched for low-level stimulus properties. Only in area hMT+ was it possible to decode the illusory trajectory. We additionally performed a number of important controls that rule out possible low-level confounds. Concurrent eye tracking confirmed that subjects accurately tracked the moving target; we were unable to decode the illusion trajectory using eye position measurements recorded during fMRI scanning, ruling out explanations based on differences in oculomotor behavior. Our results provide evidence for a perceptual representation in human visual cortex that incorporates extraretinal information.

SARS-CoV-2 Infection Impairs Oculomotor Functions: A Longitudinal Eye-tracking Study.

Although Severe Acute Respiratory Syndrome Coronavirus 2 infection (SARS-CoV-2) is primarily recognized as a respiratory disease, mounting evidence suggests that it may lead to neurological and cognitive impairments. The current study used three eye-tracking tasks (free-viewing, fixation, and smooth pursuit) to assess the oculomotor functions of mild infected cases over six months with symptomatic SARS-CoV-2 infected volunteers. Fifty symptomatic SARS-CoV-2 infected, and 24 self-reported healthy controls completed the eye-tracking tasks in an initial assessment. Then, 45, and 40 symptomatic SARS-CoV-2 infected completed the tasks at 2- and 6-months post-infection, respectively. In the initial assessment, symptomatic SARS-CoV-2 infected exhibited impairments in diverse eye movement metrics. Over the six months following infection, the infected reported overall improvement in health condition, except for self-perceived mental health. The eye movement patterns in the free-viewing task shifted toward a more focal processing mode and there was no significant improvement in fixation stability among the infected. A linear discriminant analysis shows that eye movement metrics could differentiate the infected from healthy controls with an accuracy of approximately 62%, even 6 months post-infection. These findings suggest that symptomatic SARSCoV- 2 infection may result in persistent impairments in oculomotor functions, and the employment of eye-tracking technology can offer valuable insights into both the immediate and long-term effects of SARS-CoV-2 infections. Future studies should employ a more balanced research design and leverage advanced machine-learning methods to comprehensively investigate the impact of SARSCoV- 2 infection on oculomotor functions.

Schizophrenia and Orthoptic Conditions: A Literature Review.

Purpose: A narrative review of the literature reporting ocular abnormalities in patients with schizophrenia was undertaken to determine the types and prevalence of orthoptic conditions in this patient cohort. Methods: A systematic search of multiple databases yielded 1,974 studies published between January 1992 and January 2022. All were screened for relevance based on their title and abstract. Results: Seventeen studies were included in the final review. Ocular abnormalities reported in schizophrenia included a high incidence of strabismus, reduced visual acuity and reduced stereopsis compared to controls. Additionally, eye movement abnormalities (including reduced smooth pursuit gain and increased prosaccade latency) were frequently reported. Reduced visual acuity was associated with negative symptoms and reduced quality of life in schizophrenia. Conclusions: Orthoptists and eye care professionals should be aware that a higher incidence of strabismus, reduced visual acuity, reduced stereoacuity, and eye movement abnormalities are reported in patients with schizophrenia. Further research is required to determine whether, or to what extent, ocular abnormalities and visual disturbances influence or exacerbate the symptoms of schizophrenia, and whether there is an effect of schizophrenia medication on these orthoptic conditions.

Eye-hand coordination all the way: from discrete to continuous hand movements.

The differentiation between continuous and discrete actions is key for behavioral neuroscience. Although many studies have characterized eye-hand coordination during discrete (e.g., reaching) and continuous (e.g., pursuit tracking) actions, all these studies were conducted separately, using different setups and participants. In addition, how eye-hand coordination might operate at the frontier between discrete and continuous movements remains unexplored. Here we filled these gaps by means of a task that could elicit different movement dynamics. Twenty-eight participants were asked to simultaneously track with their eyes and a joystick a visual target that followed an unpredictable trajectory and whose position was updated at different rates (from 1.5 to 240 Hz). This procedure allowed us to examine actions ranging from discrete point-to-point movements (low refresh rate) to continuous pursuit (high refresh rate). For comparison, we also tested a manual tracking condition with the eyes fixed and a pure eye tracking condition (hand fixed). The results showed an abrupt transition between discrete and continuous hand movements around 3 Hz contrasting with a smooth trade-off between fixations and smooth pursuit. Nevertheless, hand and eye tracking accuracy remained strongly correlated, with each of these depending on whether the other effector was recruited. Moreover, gaze-cursor distance and lag were smaller when eye and hand performed the task conjointly than separately. Altogether, despite some dissimilarities in eye and hand dynamics when transitioning between discrete and continuous movements, our results emphasize that eye-hand coordination continues to smoothly operate and support the notion of synergies across eye movement types.NEW & NOTEWORTHY The differentiation between continuous and discrete actions is key for behavioral neuroscience. By using a visuomotor task in which we manipulate the target refresh rate to trigger different movement dynamics, we explored eye-hand coordination all the way from discrete to continuous actions. Despite abrupt changes in hand dynamics, eye-hand coordination continues to operate via a gradual trade-off between fixations and smooth pursuit, an observation confirming the notion of synergies across eye movement types.

Smooth Pursuit and Reflexive Saccade in Discriminating Multiple-System Atrophy With Predominant Parkinsonism From Parkinson's Disease.

BACKGROUND AND PURPOSE: Performing the differential diagnosis of Parkinson's disease (PD) and multiple-system atrophy of parkinsonian type (MSA-P) is challenging. The oculomotor performances of patients with PD and MSA-P were investigated to explore their potential role as a biomarker for this differentiation. METHODS: Reflexive saccades and smooth pursuit were examined in 56 patients with PD and 34 with MSA-P in the off-medication state. RESULTS: Patients with PD and MSA-P had similar oculomotor abnormalities of prolonged and hypometric reflexive saccades. The incidence rates of decreased reflexive saccadic velocity and saccadic smooth pursuit were significantly higher in MSA-P than in PD (p<0.05 for both). Multiple logistic regression analysis indicated that slowed reflexive saccades (odds ratio [OR]=8.14, 95% confidence interval [CI]=1.45-45.5) and saccadic smooth pursuit (OR=5.27, 95% CI=1.24-22.43) were significantly related to MSA-P. CONCLUSIONS: The distinctive oculomotor abnormalities of saccadic smooth pursuit and slowed reflexive saccades in MSA-P may serve as useful biomarkers for discriminating MSA-P from PD.

Abnormal Ocular Movement in the Early Stage of Multiple-System Atrophy With Predominant Parkinsonism Distinct From Parkinson's Disease.

BACKGROUND AND PURPOSE: The eye-movement examination can be applied as a noninvasive method to identify multiple-system atrophy (MSA). Few studies have investigated eye movements during the early stage of MSA with predominant parkinsonism (MSA-P). We aimed to determine the characteristic oculomotor changes in the early stage of MSA-P. METHODS: We retrospectively selected 17 patients with MSA-P and 40 with Parkinson's disease (PD) with disease durations of less than 2 years, and 40 age-matched healthy controls (HCs). Oculomotor performance in the horizontal direction was measured in detail using videonystagmography. RESULTS: We found that the proportions of patients with MSA-P and PD exhibiting abnormal eye movements were 82.4% and 77.5%, respectively, which were significantly higher than that in the HCs (47.5%, p<0.05). Compared with HCs, patients with MSA-P presented significantly higher abnormal proportions of fixation and gaze-holding (17.6% vs. 0%), without-fixation (47.1% vs. 0%), prolonged latency in reflexive saccades (29.4% vs. 5.0%), memory-guided saccades (93.3% vs. 10.0%), and catch-up saccades in smooth-pursuit movement (SPM, 41.2% vs. 0) (all p<0.05). Compared with those with PD, patients with MSA-P presented a significantly higher proportion of catch-up saccades in SPM (41.2% vs. 2.5%, p<0.001). CONCLUSIONS: MSA-P presented the characteristic of catch-up saccades in SPM in the early stage, which may provide some value in differentiating MSA-P from PD.

Eye movements in Parkinson's disease: from neurophysiological mechanisms to diagnostic tools.

Movement disorders such as Parkinson's disease (PD) impact oculomotor function - the ability to move the eyes accurately and purposefully to serve a multitude of sensory, cognitive, and secondary motor tasks. Decades of neurophysiological research in monkeys and behavioral studies in humans have characterized the neural basis of healthy oculomotor control. This review links eye movement abnormalities in persons living with PD to the underlying neurophysiological mechanisms and pathways. Building on this foundation, we highlight recent progress in using eye movements to gauge symptom severity, assess treatment effects, and serve as potential precision biomarkers. We conclude that whereas eye movements provide insights into PD mechanisms, based on current evidence they appear to lack sufficient sensitivity and specificity to serve as a standalone diagnostic tool. Their full potential may be realized when combined with other disease indicators in big datasets.

Bayesian approaches to smooth pursuit of random dot kinematograms: effects of varying RDK noise and the predictability of RDK direction.

Smooth pursuit eye movements respond on the basis of both immediate and anticipated target motion, where anticipations may be derived from either memory or perceptual cues. To study the combined influence of both immediate sensory motion and anticipation, subjects pursued clear or noisy random dot kinematograms (RDKs) whose mean directions were chosen from Gaussian distributions with SDs = 10° (narrow prior) or 45° (wide prior). Pursuit directions were consistent with Bayesian theory in that transitions over time from dependence on the prior to near total dependence on immediate sensory motion (likelihood) took longer with the noisier RDKs and with the narrower, more reliable, prior. Results were fit to Bayesian models in which parameters representing the variability of the likelihood either were or were not constrained to be the same for both priors. The unconstrained model provided a statistically better fit, with the influence of the prior in the constrained model smaller than predicted from strict reliability-based weighting of prior and likelihood. Factors that may have contributed to this outcome include prior variability different from nominal values, low-level sensorimotor learning with the narrow prior, or departures of pursuit from strict adherence to reliability-based weighting. Although modifications of, or alternatives to, the normative Bayesian model will be required, these results, along with previous studies, suggest that Bayesian approaches are a promising framework to understand how pursuit combines immediate sensory motion, past history, and informative perceptual cues to accurately track the target motion that is most likely to occur in the immediate future.NEW & NOTEWORTHY Smooth pursuit eye movements respond on the basis of anticipated, as well as immediate, target motions. Bayesian models using reliability-based weighting of previous (prior) and immediate target motions (likelihood) accounted for many, but not all, aspects of pursuit of clear and noisy random dot kinematograms with different levels of predictability. Bayesian approaches may solve the long-standing problem of how pursuit combines immediate sensory motion and anticipation of future motion to configure an effective response.

Investigation of Camera-Free Eye-Tracking Glasses Compared to a Video-Based System.

Technological advances in eye-tracking have resulted in lightweight, portable solutions that are capable of capturing eye movements beyond laboratory settings. Eye-tracking devices have typically relied on heavier, video-based systems to detect pupil and corneal reflections. Advances in mobile eye-tracking technology could facilitate research and its application in ecological settings; more traditional laboratory research methods are able to be modified and transferred to real-world scenarios. One recent technology, the AdHawk MindLink, introduced a novel camera-free system embedded in typical eyeglass frames. This paper evaluates the AdHawk MindLink by comparing the eye-tracking recordings with a research "gold standard", the EyeLink II. By concurrently capturing data from both eyes, we compare the capability of each eye tracker to quantify metrics from fixation, saccade, and smooth pursuit tasks-typical elements in eye movement research-across a sample of 13 adults. The MindLink system was capable of capturing fixation stability within a radius of less than 0.5∘, estimating horizontal saccade amplitudes with an accuracy of 0.04∘± 2.3∘, vertical saccade amplitudes with an accuracy of 0.32∘± 2.3∘, and smooth pursuit speeds with an accuracy of 0.5 to 3∘s, depending on the pursuit speed. While the performance of the MindLink system in measuring fixation stability, saccade amplitude, and smooth pursuit eye movements were slightly inferior to the video-based system, MindLink provides sufficient gaze-tracking capabilities for dynamic settings and experiments.

Assessment of oculomotor function after prolonged computer use.

To analyze the specific effects of prolonged computer use on oculomotor function, we propose an oculomotor function evaluation system to analyze changes in oculomotor movement function by using an eye tracker to record eye movement data when performing gaze, smooth pursuit, and saccade under normal condition, after one hour and one and a half hours of continuous working at a computer. The captured eye movement data is pre-processed, and then data features are calculated and analyzed to understand the specific effects of continuously using the computer on the oculomotor function. The results show that the oculomotor function decreases as we gaze at the computer screen for longer periods, as evidenced by a decrease in the stability of the gaze function, a reduction in the gaze focus, a reduction in the speed of eye saccades, and a decrease in the smooth pursuit function. In short, the oculomotor function worsens after prolonged working at a computer. This paper presents the effects of continuously using the computer quantificationally for the first time. The proposed oculomotor function evaluation system could also be used to assess patients who have a disability in oculomotor function and specific individuals, e.g. pilots.

Tracking gaze position from EEG: Exploring the possibility of an EEG-based virtual eye-tracker.

INTRODUCTION: Ocular artifact has long been viewed as an impediment to the interpretation of electroencephalogram (EEG) signals in basic and applied research. Today, the use of blind source separation (BSS) methods, including independent component analysis (ICA) and second-order blind identification (SOBI), is considered an essential step in improving the quality of neural signals. Recently, we introduced a method consisting of SOBI and a discriminant and similarity (DANS)-based identification method, capable of identifying and extracting eye movement-related components. These recovered components can be localized within ocular structures with a high goodness of fit (>95%). This raised the possibility that such EEG-derived SOBI components may be used to build predictive models for tracking gaze position. METHODS: As proof of this new concept, we designed an EEG-based virtual eye-tracker (EEG-VET) for tracking eye movement from EEG alone. The EEG-VET is composed of a SOBI algorithm for separating EEG signals into different components, a DANS algorithm for automatically identifying ocular components, and a linear model to transfer ocular components into gaze positions. RESULTS: The prototype of EEG-VET achieved an accuracy of 0.920° and precision of 1.510° of a visual angle in the best participant, whereas an average accuracy of 1.008° ± 0.357° and a precision of 2.348° ± 0.580° of a visual angle across all participants (N = 18). CONCLUSION: This work offers a novel approach that readily co-registers eye movement and neural signals from a single-EEG recording, thus increasing the ease of studying neural mechanisms underlying natural cognition in the context of free eye movement.

Deep learning models for webcam eye tracking in online experiments.

Eye tracking is prevalent in scientific and commercial applications. Recent computer vision and deep learning methods enable eye tracking with off-the-shelf webcams and reduce dependence on expensive, restrictive hardware. However, such deep learning methods have not yet been applied and evaluated for remote, online psychological experiments. In this study, we tackle critical challenges faced in remote eye tracking setups and systematically evaluate appearance-based deep learning methods of gaze tracking and blink detection. From their own homes and laptops, 65 participants performed a battery of eye tracking tasks including (i) fixation, (ii) zone classification, (iii) free viewing, (iv) smooth pursuit, and (v) blink detection. Webcam recordings of the participants performing these tasks were processed offline through appearance-based models of gaze and blink detection. The task battery required different eye movements that characterized gaze and blink prediction accuracy over a comprehensive list of measures. We find the best gaze accuracy to be 2.4° and precision of 0.47°, which outperforms previous online eye tracking studies and reduces the gap between laboratory-based and online eye tracking performance. We release the experiment template, recorded data, and analysis code with the motivation to escalate affordable, accessible, and scalable eye tracking that has the potential to accelerate research in the fields of psychological science, cognitive neuroscience, user experience design, and human-computer interfaces.

Rate versus synchrony codes for cerebellar control of motor behavior.

Information transmission between neural populations could occur through either coordinated changes in firing rates or the precise transmission of spike timing. We investigate the code for information transmission from a part of the cerebellar cortex that is crucial for the accurate execution of a quantifiable motor behavior. Simultaneous recordings from Purkinje cell pairs in the cerebellum of rhesus macaques reveal how these cells coordinate their activity to drive smooth pursuit eye movements. Purkinje cells show millisecond-scale coordination of spikes (synchrony), but the level of synchrony is small and insufficient to impact the firing of downstream vestibular nucleus neurons. Analysis of previous metrics that purported to reveal Purkinje cell synchrony demonstrates that these metrics conflate changes in firing rate and neuron-neuron covariance. We conclude that the output of the cerebellar cortex uses primarily a rate rather than a synchrony code to drive the activity of downstream neurons and thus control motor behavior.

Visual attentional guidance during smooth pursuit eye movements: Distractor interference is independent of distractor-target similarity.

In the current study, we used abrupt-onset distractors similar and dissimilar in luminance to the target of a smooth pursuit eye-movement to test if abrupt-onset distractors capture attention in a top-down or bottom-up fashion while the eyes track a moving object. Abrupt onset distractors were presented at different positions relative to the current position of a pursuit target during the closed-loop phase of smooth pursuit. Across experiments, we varied the duration of the distractors, their motion direction, and task-relevance. We found that abrupt-onset distractors decreased the gain of horizontally directed smooth-pursuit eye-movements. This effect, however, was independent of the similarity in luminance between distractor and target. In addition, distracting effects on horizontal gain were the same, regardless of the exact duration and position of the distractors, suggesting that capture was relatively unspecific and short-lived (Experiments 1 and 2). This was different with distractors moving in a vertical direction, perpendicular to the horizontally moving target. In line with past findings, these distractors caused suppression of vertical gain (Experiment 3). Finally, making distractors task-relevant by asking observers to report distractor positions increased the pursuit gain effect of the distractors. This effect was also independent of target-distractor similarity (Experiment 4). In conclusion, the results suggest that a strong location signal exerted by the pursuit targets led to very brief and largely location-unspecific interference through the abrupt onsets and that this interference was bottom-up, implying that the control of smooth pursuit was independent of other target features besides its motion signal.