Modeling kinematic variability reveals displacement and velocity based dual control of saccadic eye movements.

Noise is a ubiquitous component of motor systems that leads to behavioral variability of all types of movements. Nonetheless, systems-based models investigating human movements are generally deterministic and explain only the central tendencies like mean trajectories. In this paper, a novel approach to modeling kinematic variability of movements is presented and tested on the oculomotor system. This approach reconciles the two prominent philosophies of saccade control: displacement-based control versus velocity-based control. This was achieved by quantifying the variability in saccadic eye movements and developing a stochastic model of its control. The proposed stochastic dual model generated significantly better fits of inter-trial variances of the saccade trajectories compared to existing models. These results suggest that the saccadic system can flexibly use the information of both desired displacement and velocity for its control. This study presents a potential framework for investigating computational principles of motor control in the presence of noise utilizing stochastic modeling of kinematic variability.

Navigating Visual Challenges: How Parkinson's Disease Alters Cognitive Priorities in Visual Search.

OBJECTIVE: Parkinson's disease (PD) hampers visual search tasks such as reading, driving, and navigation. We examined expectations from past experiences, guiding cognition and contextual priors, on visual search in PD. METHODS: We compared eye movements as PD and healthy participants searched for a hidden object (target) in cluttered real-world scenes. RESULTS: PD participants prolonged fixation on high-probability (high-prior) locations for the target, consistent across expected and unexpected scenario. Such emphasis on contextual visual priors, evidenced by high fixation duration on high-probability areas, was beneficial when the target was at the expected location but presented challenges when the target was situated in an unlikely place. CONCLUSION: This study contributes to understanding how PD impacts visual search behavior and cognitive processing. The findings indicate that PD alters attention allocation and visual processing by affecting the utilization of contextual visual priors. It provides insights for potential interventions targeting visuo-cognitive deficits in PD patients. Published 2024. This article is a U.S. Government work and is in the public domain in the USA.

Idiosyncratic fixation patterns generalize across dynamic and static facial expression recognition.

Facial expression recognition (FER) is crucial for understanding the emotional state of others during human social interactions. It has been assumed that humans share universal visual sampling strategies to achieve this task. However, recent studies in face identification have revealed striking idiosyncratic fixation patterns, questioning the universality of face processing. More importantly, very little is known about whether such idiosyncrasies extend to the biological relevant recognition of static and dynamic facial expressions of emotion (FEEs). To clarify this issue, we tracked observers' eye movements categorizing static and ecologically valid dynamic faces displaying the six basic FEEs, all normalized for time presentation (1 s), contrast and global luminance across exposure time. We then used robust data-driven analyses combining statistical fixation maps with hidden Markov Models to explore eye-movements across FEEs and stimulus modalities. Our data revealed three spatially and temporally distinct equally occurring face scanning strategies during FER. Crucially, such visual sampling strategies were mostly comparably effective in FER and highly consistent across FEEs and modalities. Our findings show that spatiotemporal idiosyncratic gaze strategies also occur for the biologically relevant recognition of FEEs, further questioning the universality of FER and, more generally, face processing.

An early effect of the parafoveal preview on post-saccadic processing of English words.

A key aspect of efficient visual processing is to use current and previous information to make predictions about what we will see next. In natural viewing, and when looking at words, there is typically an indication of forthcoming visual information from extrafoveal areas of the visual field before we make an eye movement to an object or word of interest. This "preview effect" has been studied for many years in the word reading literature and, more recently, in object perception. Here, we integrated methods from word recognition and object perception to investigate the timing of the preview on neural measures of word recognition. Through a combined use of EEG and eye-tracking, a group of multilingual participants took part in a gaze-contingent, single-shot saccade experiment in which words appeared in their parafoveal visual field. In valid preview trials, the same word was presented during the preview and after the saccade, while in the invalid condition, the saccade target was a number string that turned into a word during the saccade. As hypothesized, the valid preview greatly reduced the fixation-related evoked response. Interestingly, multivariate decoding analyses revealed much earlier preview effects than previously reported for words, and individual decoding performance correlated with participant reading scores. These results demonstrate that a parafoveal preview can influence relatively early aspects of post-saccadic word processing and help to resolve some discrepancies between the word and object literatures.

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.

Clinical reading-related oculomotor assessment in visual snow syndrome / Evaluación oculomotora clínica relacionada con la lectura en el síndrome de nieve visual

Purpose: Visual snow syndrome (VSS) is a complex neurological condition presenting with an array of sensory, motor, and perceptual dysfunctions and related visual and non-visual symptoms. Recent laboratory studies have found subtle, basic, saccadic-based abnormalities in this population. The objective of the present investigation was to determine if saccadic-related problems could be confirmed and extended using three common clinical reading-related eye movement tests having well-developed protocols and normative databases. Methods: This was a retrospective analysis of 32 patients (ages 16–56 years) diagnosed with VSS in the first author's optometric practice. There was a battery of three reading-related tests: the Visagraph Reading Eye Movement Test, the Developmental Eye Movement (DEM) Test, and the RightEye Dynamic Vision Assessment Test, all performed using their standard documented protocols and large normative databases. Results: A high frequency of oculomotor deficits was found with all three tests. The greatest percentage was revealed with the Visagraph (56%) and the least with the RightEye (23%). A total of 77% of patients failed at least one of the three tests. Conclusion: The present findings confirm and extend earlier investigations revealing a high frequency of saccadic-based oculomotor problems in the VSS population, now including reading-related tasks. This is consistent with the more general oculomotor/motor problems found in these individuals.(AU)

Spatial updating of gaze position in younger and older adults - A path integration-like process in eye movements.

Path integration (PI) is a navigation process that allows an organism to update its current location in reference to a starting point. PI can involve updating self-position continuously with respect to the starting point (continuous updating) or creating a map representation of the route which is then used to compute the homing vector (configural updating). One of the brain areas involved in PI, the entorhinal cortex, is modulated similarly by whole-body and eye movements, suggesting that if PI updates self-position, an analogous process may be used to update gaze position, and may undergo age-related changes. Here, we created an eyetracking version of a PI task in which younger and older participants followed routes with their eyes as guided by visual onsets; at the end of each route, participants were cued to return to the starting point or another enroute location. When only memory for the starting location was required for successful task performance, younger and older adults were generally not influenced by the number of locations, indicative of continuous updating. However, when participants could be cued to any enroute location, thereby requiring memory for the entire route, processing times increased, accuracy decreased, and overt revisits to enroute locations increased with the number of locations in a route, indicative of configural updating. Older participants showed evidence for similar updating strategies as younger participants, but they were less accurate and made more overt revisits to mid-route locations. These findings suggest that spatial updating mechanisms are generalizable across effector systems.

Factors Affecting the Situational Awareness of Armored Vehicle Occupants.

In the field of armored vehicles, up to 70% of accidents are associated with low levels of situational awareness among the occupants, highlighting the importance of situational awareness in improving task performance. In this study, we explored the mechanisms influencing situational awareness by simulating an armored vehicle driving platform with 14 levels of experimentation in terms of five factors: experience, expectations, attention, the cueing channel, and automation. The experimental data included SART and SAGAT questionnaire scores, eye movement indicators, and electrocardiographic and electrodermal signals. Data processing and analysis revealed the following conclusions: (1) Experienced operators have higher levels of situational awareness. (2) Operators with certain expectations have lower levels of situational awareness. (3) Situational awareness levels are negatively correlated with information importance affiliations and the frequency of anomalous information in non-primary tasks. (4) Dual-channel cues lead to higher levels of situational awareness than single-channel cues. (5) Operators' situational awareness is lower at high automation levels.

Shared Mechanisms Drive Ocular Following and Motion Perception.

How features of complex visual patterns are combined to drive perception and eye movements is not well understood. Here we simultaneously assessed human observers' perceptual direction estimates and ocular following responses (OFR) evoked by moving plaids made from two summed gratings with varying contrast ratios. When the gratings were of equal contrast, observers' eye movements and perceptual reports followed the motion of the plaid pattern. However, when the contrasts were unequal, eye movements and reports during early phases of the OFR were biased toward the direction of the high-contrast grating component; during later phases, both responses followed the plaid pattern direction. The shift from component- to pattern-driven behavior resembles the shift in tuning seen under similar conditions in neuronal responses recorded from monkey MT. Moreover, for some conditions, pattern tracking and perceptual reports were correlated on a trial-by-trial basis. The OFR may therefore provide a precise behavioral readout of the dynamics of neural motion integration for complex visual patterns.

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.

Sleep disturbances and incident risk of major depressive disorder in a population-based cohort.

Sleep disturbances are well-known symptoms of major depressive disorder (MDD). However, the prospective risk of MDD in the presence of sleep disturbances in a general population-based cohort is not well known. This study investigated associations between both polysomnography (PSG)-based or subjective sleep features and incident MDD. Participants representative of the general population who had never had MDD completed sleep questionnaires (n = 2000) and/or underwent PSG (n = 717). Over 8 years' follow-up, participants completed psychiatric interviews enabling the diagnosis of MDD. Survival Cox models were used to analyze associations between sleep features and MDD incidence. A higher Epworth Sleepiness Scale and presence of insomnia symptoms were significantly associated with a higher incidence of MDD (hazard ratio [HR] [95 % confidence interval (CI)]: 1.062 [1.022-1.103], p = 0.002 and 1.437 [1.064-1.940], p = 0.018, respectively). Higher density of rapid eye movements in rapid eye movement (REM) sleep was associated with a higher incidence of MDD in men (HR 1.270 [95 % CI 1.064-1.516], p = 0.008). In women, higher delta power spectral density was associated with a lower MDD incidence (HR 0.674 [95 % CI 0.463-0.981], p = 0.039). This study confirmed the associations between subjective and objective sleep features and the incidence of MDD in a large community dwelling cohort.

Perceptual task drives later fixations and long latency saccades, while early fixations and short latency saccades are more automatic.

We used a simple stimulus, dissociating perceptually relevant information in space, to differentiate between bottom-up and task-driven fixations. Six participants viewed a dynamic scene showing the reaction of an elastic object fixed to the ceiling being hit. In one condition they had to judge the object's stiffness and in the other condition its lightness. The results show that initial fixations tend to land in the centre of an object, independent of the task. After the initial fixation, participants tended to look at task diagnostic regions. This fixation behaviour correlates with high perceptual performance. Similarly, low-latency saccades lead to fixations that do not depend on the task, whereas higher latency does.

Audiovisual presentation of variable message signs improves message processing in distracted drivers during partially automated driving.

INTRODUCTION: Highly automated driving is expected to reduce the accident risk occurrence by human errors, but it can also increase driver distraction. Previous evidence shows that auditory signals can help drivers take over in critical situations. However, it is still uncertain whether the potential benefit of verbal auditory signals could be generalized to driving situations where drivers are visually and auditorily distracted. METHOD: Our first objective was to compare the effectiveness of complementary audio messages (audio + visual condition) and visual only (visual condition) variable message signs (VMS) messages. The second objective was to explore the potential use of oral messages with traffic information to help highly-automated vehicle drivers identify critical situations. Eye-tracking data were also registered. Twenty-four volunteers participated in a driving simulator study, completing two tasks: (a) a TV series task, where they had to pay attention to an episode of a TV series while traveling along the route; and (b) a VMS task, where they had to recover the manual control of the car if the VMS message was a 'critical message.' RESULTS: General results showed that, when the audio was available, the participants: (a) had a higher ability to discriminate the VMS messages, (b) were less conservative, (c) responded earlier, and (d) their pattern of fixations was more efficient. A complementary analysis showed that the counterbalance order was a moderating factor for the discrimination ability and the response distance measures. This evidence suggests a potential learning effect, not cancelled by counterbalancing the order of the conditions. CONCLUSION: The processing of traffic messages may improve when provided as oral and visual messages. PRACTICAL APPLICATIONS: These results would be of special interest for engineers designing highly automated cars, considering that the design of automated systems must ensure that the driver's attention is sufficient to take over control.

Ocular working memory signals are flexible to behavioral priority and subjective imagery strength.

The pupillary light response was long considered a brainstem reflex, outside of cognitive influence. However, newer findings indicate that pupil dilation (and eye movements) can reflect content held "in mind" with working memory (WM). These findings may reshape understanding of ocular and WM mechanisms, but it is unclear whether the signals are artifactual or functional to WM. Here, we ask whether peripheral and oculomotor WM signals are sensitive to the task-relevance or "attentional state" of WM content. During eye-tracking, human participants saw both dark and bright WM stimuli, then were retroactively cued to the item that would most likely be tested. Critically, we manipulated the attentional priority among items by varying the cue reliability across blocks. We confirmed previous findings that remembering darker items is associated with larger pupils (vs. brighter), and that gaze is biased toward cued item locations. Moreover, we discovered that pupil and eye movement responses were influenced differently by WM item relevance. Feature-specific pupillary effects emerged only for highly prioritized WM items but were eliminated when cues were less reliable, and pupil effects also increased with self-reported visual imagery strength. Conversely, gaze position consistently veered toward the cued item location, regardless of cue reliability. However, biased microsaccades occurred at a higher frequency when cues were more reliable, though only during a limited post-cue time window. Therefore, peripheral sensorimotor processing is sensitive to the task-relevance or functional state of internal WM content, but pupillary and eye movement WM signals show distinct profiles. These results highlight a potential role for early visual processing in maintaining multiple WM content dimensions.NEW & NOTEWORTHY Here, we found that working memory (WM)-driven ocular inflections-feature-specific pupillary and saccadic biases-were muted for memory items that were less behaviorally relevant. This work illustrates that functionally informative goal signals may extend as early as the sensorimotor periphery, that pupil size may be under more fine-grained control than originally thought, and that ocular signals carry multiple dimensions of cognitively relevant information.

Effect of methylphenidate on oculomotor function in individuals with multiple sclerosis: a pilot randomized placebo-controlled trial.

Introduction: Individuals with multiple sclerosis (MS) frequently experience visual and oculomotor symptoms that may impact and confound neuropsychological assessments of information processing speed (IPS). In this study, we examined the effect of the psychostimulant methylphenidate on oculomotor function and the association between change in oculomotor speed and change in information processing speed. Methods: We used a repeated measures crossover design in which a sample of 11 participants with MS were randomly assigned to one of two treatment arms: one that received methylphenidate for 4 weeks and another that received a placebo for 4 weeks. After a 7-day washout period, the treatments were crossed over. The King Devick test, the Symbol Digit Modalities Test, and the Paced Auditory Serial Addition Test were administered at baseline and after each of the two study arms. Results: We found a significant improvement in oculomotor speed in the methylphenidate condition as compared to placebo. This improvement was significantly correlated with improvement on a visuomotor assessment of IPS (Symbol Digit Modalities Test), but no such association was found for an auditory-verbal assessment of IPS (Paced Auditory Serial Addition Test). Discussion: These findings suggest that individuals with MS experience improved oculomotor speed while taking methylphenidate, which may, in turn, improve performance on assessments of IPS with visuomotor demands.

Dorsal pulvinar inactivation leads to spatial selection bias without perceptual deficit.

The dorsal pulvinar has been implicated in visuospatial attentional and perceptual confidence processing. Pulvinar lesions in humans and monkeys lead to spatial neglect symptoms, including an overt spatial saccade bias during free choices. However, it remains unclear whether disrupting the dorsal pulvinar during target selection that relies on a perceptual decision leads to a perceptual impairment or a more general spatial orienting and choice deficit. To address this question, we reversibly inactivated the unilateral dorsal pulvinar by injecting GABA-A agonist THIP while two macaque monkeys performed a color discrimination saccade task with varying perceptual difficulty. We used Signal Detection Theory and simulations to dissociate perceptual sensitivity (d-prime) and spatial selection bias (response criterion) effects. We expected a decrease in d-prime if dorsal pulvinar affects perceptual discrimination and a shift in response criterion if dorsal pulvinar is mainly involved in spatial orienting. After the inactivation, we observed response criterion shifts away from contralesional stimuli, especially when two competing stimuli in opposite hemifields were present. Notably, the d-prime and overall accuracy remained largely unaffected. Our results underline the critical contribution of the dorsal pulvinar to spatial orienting and action selection while showing it to be less important for visual perceptual discrimination.

Sense of agency at a gaze-contingent display with jittery temporal delay.

Introduction: Inconsistent jittery temporal delays between action and subsequent feedback, prevalent in network-based human-computer interaction (HCI), have been insufficiently explored, particularly regarding their impact on the sense of agency (SoA). This study investigates the SoA in the context of eye-gaze HCI under jittery delay conditions. Methods: Participants performed a visual search for Chinese characters using a biresolutional gaze-contingent display, which displayed a high-resolution image in the central vision and a low-resolution in the periphery. We manipulated the delay between eye movements and display updates using a truncated normal distribution (µ to µ + 2 σ) with µ ranging from 0 to 400 ms and σ fixed at 50 ms. Playback of recorded gaze data provided a non-controllable condition. Results: The study revealed that both reported authorship and controllability scores, as well as the fixation count per second, decreased as µ increased, aligning with trends observed under constant delay conditions. The subjective authorship weakened significantly at a µ of 94 ms. Notably, the comparison between jittery and constant delays indicated the minimum value (µ) of the distribution as a critical parameter influencing both authorship perception and visual search time efficiency. Discussion: This finding underscores the importance of the shortest delay in modulating SoA. Further examining the relative distribution for fixation duration and saccade amplitude suggests an adaptation in action planning and attention distribution in response to delay. By providing a systematic examination of the statistical attributes of jittery delays that most significantly affect SoA, this research offers valuable implications for the design of efficient, delay-tolerant eye-gaze HCI, expanding our understanding of SoA in technologically mediated interactions. Moreover, our findings highlight the significance of considering both constant and variable delay impacts in HCI usability design, marking a novel contribution to the field.

Attentional suppression of dynamic versus static salient distractors.

Attention must be carefully controlled to avoid distraction by salient stimuli. The signal suppression hypothesis proposes that salient stimuli can be proactively suppressed to prevent distraction. Although this hypothesis has garnered much support, most previous studies have used one class of salient distractors: color singletons. It therefore remains unclear whether other kinds of salient distractors can also be suppressed. The current study directly compared suppression of a variety of salient stimuli using an attentional capture task that was adapted for eye tracking. The working hypothesis was that static salient stimuli (e.g., color singletons) would be easier to suppress than dynamic salient stimuli (e.g., motion singletons). The results showed that participants could ignore a wide variety of salient distractors. Importantly, suppression was weaker and slower to develop for dynamic salient stimuli than static salient stimuli. A final experiment revealed that adding a static salient feature to a dynamic motion distractor greatly improved suppression. Altogether, the results suggest that an underlying inhibitory process is applied to all kinds of salient distractors, but that suppression is more readily applied to static features than dynamic features.

Artificial Intelligence in Eye Movements Analysis for Alzheimer's Disease Early Diagnosis.

As the world's population ages, Alzheimer's disease is currently the seventh most common cause of death globally; the burden is anticipated to increase, especially among middle-class and elderly persons. Artificial intelligence-based algorithms that work well in hospital environments can be used to identify Alzheimer's disease. A number of databases were searched for English-language articles published up until March 1, 2024, that examined the relationships between artificial intelligence techniques, eye movements, and Alzheimer's disease. A novel non-invasive method called eye movement analysis may be able to reflect cognitive processes and identify anomalies in Alzheimer's disease. Artificial intelligence, particularly deep learning, and machine learning, is required to enhance Alzheimer's disease detection using eye movement data. One sort of deep learning technique that shows promise is convolutional neural networks, which need further data for precise classification. Nonetheless, machine learning models showed a high degree of accuracy in this context. Artificial intelligence-driven eye movement analysis holds promise for enhancing clinical evaluations, enabling tailored treatment, and fostering the development of early and precise Alzheimer's disease diagnosis. A combination of artificial intelligence-based systems and eye movement analysis can provide a window for early and non-invasive diagnosis of Alzheimer's disease. Despite ongoing difficulties with early Alzheimer's disease detection, this presents a novel strategy that may have consequences for clinical evaluations and customized medication to improve early and accurate diagnosis.