Smooth pursuit inhibition reveals audiovisual enhancement of fast movement control.

The sudden onset of a visual object or event elicits an inhibition of eye movements at latencies approaching the minimum delay of visuomotor conductance in the brain. Typically, information presented via multiple sensory modalities, such as sound and vision, evokes stronger and more robust responses than unisensory information. Whether and how multisensory information affects ultra-short latency oculomotor inhibition is unknown. In two experiments, we investigate smooth pursuit and saccadic inhibition in response to multisensory distractors. Observers tracked a horizontally moving dot and were interrupted by an unpredictable visual, auditory, or audiovisual distractor. Distractors elicited a transient inhibition of pursuit eye velocity and catch-up saccade rate within ∼100 ms of their onset. Audiovisual distractors evoked stronger oculomotor inhibition than visual- or auditory-only distractors, indicating multisensory response enhancement. Multisensory response enhancement magnitudes were equal to the linear sum of responses to component stimuli. These results demonstrate that multisensory information affects eye movements even at ultra-short latencies, establishing a lower time boundary for multisensory-guided behavior. We conclude that oculomotor circuits must have privileged access to sensory information from multiple modalities, presumably via a fast, subcortical pathway.

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.

Shared mechanisms drive ocular following and motion perception.

How features of complex visual patterns combine to drive perception and eye movements is not well understood. 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 more closely 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 behavioural read-out of the dynamics of neural motion integration for complex visual patterns.

Rapid Audiovisual Integration Guides Predictive Actions.

Natural movements, such as catching a ball or capturing prey, typically involve multiple senses. Yet, laboratory studies on human movements commonly focus solely on vision and ignore sound. Here, we ask how visual and auditory signals are integrated to guide interceptive movements. Human observers tracked the brief launch of a simulated baseball, randomly paired with batting sounds of varying intensities, and made a quick pointing movement at the ball. Movement end points revealed systematic overestimation of target speed when the ball launch was paired with a loud versus a quiet sound, although sound was never informative. This effect was modulated by the availability of visual information; sounds biased interception when the visual presentation duration of the ball was short. Amplitude of the first catch-up saccade, occurring ∼125 ms after target launch, revealed early integration of audiovisual information for trajectory estimation. This sound-induced bias was reversed during later predictive saccades when more visual information was available. Our findings suggest that auditory and visual signals are integrated to guide interception and that this integration process must occur early at a neural site that receives auditory and visual signals within an ultrashort time span.

Eye movements during optic flow perception.

Optic flow is an important visual cue for human perception and locomotion and naturally triggers eye movements. Here we investigate whether the perception of optic flow direction is limited or enhanced by eye movements. In Exp. 1, 23 human observers localized the focus of expansion (FOE) of an optic flow pattern; in Exp. 2, 18 observers had to detect brief visual changes at the FOE. Both tasks were completed during free viewing and fixation conditions while eye movements were recorded. Task difficulty was varied by manipulating the coherence of radial motion from the FOE (4 %-90 %). During free viewing, observers tracked the optic flow pattern with a combination of saccades and smooth eye movements. During fixation, observers nevertheless made small-scale eye movements. Despite differences in spatial scale, eye movements during free viewing and fixation were similarly directed toward the FOE (saccades) and away from the FOE (smooth tracking). Whereas FOE localization sensitivity was not affected by eye movement instructions (Exp. 1), observers' sensitivity to detect brief changes at the FOE was 27 % higher (p <.001) during free-viewing compared to fixation (Exp. 2). This performance benefit was linked to reduced saccade endpoint errors, indicating the direct beneficial impact of foveating eye movements on performance in a fine-grain perceptual task, but not during coarse perceptual localization.

Tracking and perceiving diverse motion signals: Directional biases in human smooth pursuit and perception.

Human smooth pursuit eye movements and motion perception behave similarly when observers track and judge the motion of simple objects, such as dots. But moving objects in our natural environment are complex and contain internal motion. We ask how pursuit and perception integrate the motion of objects with motion that is internal to the object. Observers (n = 20) tracked a moving random-dot kinematogram with their eyes and reported the object's perceived direction. Objects moved horizontally with vertical shifts of 0, ±3, ±6, or ±9° and contained internal dots that were static or moved ±90° up/down. Results show that whereas pursuit direction was consistently biased in the direction of the internal dot motion, perceptual biases differed between observers. Interestingly, the perceptual bias was related to the magnitude of the pursuit bias (r = 0.75): perceptual and pursuit biases were directionally aligned in observers that showed a large pursuit bias, but went in opposite directions in observers with a smaller pursuit bias. Dissociations between perception and pursuit might reflect different functional demands of the two systems. Pursuit integrates all available motion signals in order to maximize the ability to monitor and collect information from the whole scene. Perception needs to recognize and classify visual information, thus segregating the target from its context. Ambiguity in whether internal motion is part of the scene or contributes to object motion might have resulted in individual differences in perception. The perception-pursuit correlation suggests shared early-stage motion processing or perception-pursuit interactions.

Do pupillary responses during authentic slot machine use reflect arousal or screen luminance fluctuations? A proof-of-concept study.

Modern slot machines are among the more harmful forms of gambling. Psychophysiological measures may provide a window into mental processes that underpin these harms. Here we investigated pupil dilation derived from eye tracking as a means of capturing changes in sympathetic nervous system arousal following outcomes on a real slot machine. We hypothesized that positively reinforcing slot machine outcomes would be associated with increases in arousal, reflected in larger pupil diameter. We further examined the contribution of game luminance fluctuations on pupil diameter. In Experiment 1A, experienced slot machine gamblers (N = 53) played a commercially-available slot machine in a laboratory for 20 minutes while wearing mobile eye tracking glasses. Analyses differentiated loss outcomes, wins, losses-disguised-as-wins, and (free-spin) bonus features. Bonus features were associated with rapid increases in pupil diameter following the onset of outcome-related audiovisual feedback, relative to losses. In Experiment 1B, luminance data were extracted from captured screen videos (derived from Experiment 1A) to characterize on-screen luminance changes that could modulate pupil diameter. Bonus features and wins were associated with pronounced and complex fluctuations in screen luminance (≈50 L and ≈25L, respectively). However, the pupil dilation that was observed to bonus features in Experiment 1A coincided temporally with only negligible changes in screen luminance, providing partial evidence that the pupil dilation to bonus features may be due to arousal. In Experiment 2, 12 participants viewed pairs of stimuli (scrambled slot machine images) at luminance difference thresholds of ≈25L, ≈50L, and ≈100L. Scrambled images presented at luminance differences of ≈25L and greater were sufficient to cause pupillary responses. Overall, pupillometry may detect event-related changes in sympathetic nervous system arousal following gambling outcomes, but researchers must pay careful attention to substantial in-game luminance changes that may confound arousal-based interpretations.

Eye Movements as a Window into Decision-Making.

For over 100 years, eye movements have been studied and used as indicators of human sensory and cognitive functions. This review evaluates how eye movements contribute to our understanding of the processes that underlie decision-making. Eye movement metrics signify the visual and task contexts in which information is accumulated and weighed. They indicate the efficiency with which we evaluate the instructions for decision tasks, the timing and duration of decision formation, the expected reward associated with a decision, the accuracy of the decision outcome, and our ability to predict and feel confident about a decision. Because of their continuous nature, eye movements provide an exciting opportunity to probe decision processes noninvasively in real time.

Eye-hand coordination during online reach corrections is task dependent.

To produce accurate movements, the human motor system needs to deal with errors that can occur due to inherent noise, changes in the body, or disturbances in the environment. Here, we investigated the temporal coupling of rapid corrections of the eye and hand in response to a change in visual target location during the movement. In addition to a "classic" double-step task in which the target stepped to a new position, participants performed a set of modified double-step tasks in which the change in movement goal was indicated by the appearance of an additional target, or by a spatial or symbolic cue. We found that both the absolute correction latencies of the eye and hand and the relative eye-hand correction latencies were dependent on the visual characteristics of the target change, with increasingly longer latencies in tasks that required more visual and cognitive processing. Typically, the hand started correcting slightly earlier than the eye, especially when the target change was indicated by a symbolic cue, and in conditions where visual feedback of the hand position was provided during the reach. Our results indicate that the oculomotor and limb-motor system can be differentially influenced by processing requirements of the task and emphasize that temporal eye-hand coupling is flexible rather than rigid.NEW & NOTEWORTHY Eye movements support hand movements in many situations. Here, we used variations of a double-step task to investigate temporal coupling of corrective hand and eye movements in response to target displacements. Correction latency coupling depended on the visual and cognitive processing demands of the task. The hand started correcting before the eye, especially when the task required decoding a symbolic cue. These findings highlight the flexibility and task dependency of eye-hand coordination.

Preservation of Eye Movements in Parkinson's Disease Is Stimulus- and Task-Specific.

Parkinson's disease (PD) is a neurodegenerative disease that includes motor impairments, such as tremor, bradykinesia, and postural instability. Although eye movement deficits are commonly found in saccade and pursuit tasks, preservation of oculomotor function has also been reported. Here we investigate specific task and stimulus conditions under which oculomotor function in PD is preserved. Sixteen PD patients and 18 healthy, age-matched controls completed a battery of movement tasks that included stationary or moving targets eliciting reactive or deliberate eye movements: pro-saccades, anti-saccades, visually guided pursuit, and rapid go/no-go manual interception. Compared with controls, patients demonstrated systematic impairments in tasks with stationary targets: pro-saccades were hypometric and anti-saccades were incorrectly initiated toward the cued target in ∼35% of trials compared with 14% errors in controls. In patients, task errors were linked to short latency saccades, indicating abnormalities in inhibitory control. However, patients' eye movements in response to dynamic targets were relatively preserved. PD patients were able to track and predict a disappearing moving target and make quick go/no-go decisions as accurately as controls. Patients' interceptive hand movements were slower on average but initiated earlier, indicating adaptive processes to compensate for motor slowing. We conclude that PD patients demonstrate stimulus and task dependency of oculomotor impairments, and we propose that preservation of eye and hand movement function in PD is linked to a separate functional pathway through the superior colliculus-brainstem loop that bypasses the fronto-basal ganglia network. Our results demonstrate that studying oculomotor and hand movement function in PD can support disease diagnosis and further our understanding of disease progression and dynamics.SIGNIFICANCE STATEMENT Eye movements are a promising clinical tool to aid in the diagnosis of movement disorders and to monitor disease progression. Although Parkinson's disease (PD) patients show some oculomotor abnormalities, it is not clear whether previously described eye movement impairments are task-specific. We assessed eye movements in PD under different visual (stationary vs moving targets) and movement (reactive vs deliberate) conditions. We demonstrate that PD patients are able to accurately track moving objects but make inaccurate eye movements toward stationary targets. The preservation of eye movements toward dynamic stimuli might enable patients to accurately act on the predicted motion path of the moving target. These results can inform the development of tools for the rehabilitation or maintenance of functional performance.

Humans Can Track But Fail to Predict Accelerating Objects.

Objects in our visual environment often move unpredictably and can suddenly speed up or slow down. The ability to account for acceleration when interacting with moving objects can be critical for survival. Here, we investigate how human observers track an accelerating target with their eyes and predict its time of reappearance after a temporal occlusion by making an interceptive hand movement. Before occlusion, observers smoothly tracked the accelerating target with their eyes. At the time of occlusion, observers made a predictive saccade to the location where they subsequently intercepted the target with a quick pointing movement. We tested how observers integrated target motion information by comparing three alternative models that describe time-to-contact (TTC) based on the (1) final target velocity sample before occlusion, (2) average target velocity before occlusion, or (3) final target velocity and the rate of target acceleration. We show that observers were able to accurately track the accelerating target with visually-guided smooth pursuit eye movements. However, the timing of the predictive saccade and manual interception revealed inability to act on target acceleration when predicting TTC. Instead, interception timing was best described by the final velocity model that relies on extrapolating the last available target velocity sample before occlusion. Moreover, predictive saccades and manual interception showed similar insensitivity to target acceleration and were correlated on a trial-by-trial basis. These findings provide compelling evidence for the failure of integrating target acceleration into predictive models of target motion that drive both interceptive eye and hand movements.

Topical Review: Perceptual-cognitive Skills, Methods, and Skill-based Comparisons in Interceptive Sports.

SIGNIFICANCE: We give a comprehensive picture of perceptual-cognitive (PC) skills that could contribute to performance in interceptive sports. Both visual skills that are low level and unlikely influenced by experience and higher-level cognitive-attentional skills are considered, informing practitioners for identification and training and alerting researchers to gaps in the literature.Perceptual-cognitive skills and abilities are keys to success in interceptive sports. The interest in identifying which skills and abilities underpin success and hence should be selected and developed is likely going to grow as technologies for skill testing and training continue to advance. Many different methods and measures have been applied to the study of PC skills in the research laboratory and in the field, and research findings across studies have often been inconsistent. In this article, we provide definitional clarity regarding whether a skill is primarily visual attentional (ranging from fundamental/low-level skills to high-level skills) or cognitive. We review those skills that have been studied using sport-specific stimuli or tests, such as postural cue anticipation in baseball, as well as those that are mostly devoid of sport context, considered general skills, such as dynamic visual acuity. In addition to detailing the PC skills and associated methods, we provide an accompanying table of published research since 1995, highlighting studies (for various skills and sports) that have and have not differentiated across skill groups.

Look where you go: Characterizing eye movements toward optic flow.

When we move through our environment, objects in the visual scene create optic flow patterns on the retina. Even though optic flow is ubiquitous in everyday life, it is not well understood how our eyes naturally respond to it. In small groups of human and non-human primates, optic flow triggers intuitive, uninstructed eye movements to the focus of expansion of the pattern (Knöll, Pillow, & Huk, 2018). Here, we investigate whether such intuitive oculomotor responses to optic flow are generalizable to a larger group of human observers and how eye movements are affected by motion signal strength and task instructions. Observers (N = 43) viewed expanding or contracting optic flow constructed by a cloud of moving dots radiating from or converging toward a focus of expansion that could randomly shift. Results show that 84% of observers tracked the focus of expansion with their eyes without being explicitly instructed to track. Intuitive tracking was tuned to motion signal strength: Saccades landed closer to the focus of expansion, and smooth tracking was more accurate when dot contrast, motion coherence, and translational speed were high. Under explicit tracking instruction, the eyes aligned with the focus of expansion more closely than without instruction. Our results highlight the sensitivity of intuitive eye movements as indicators of visual motion processing in dynamic contexts.

The role of eye movements in manual interception: A mini-review.

When we catch a moving object in mid-flight, our eyes and hands are directed toward the object. Yet, the functional role of eye movements in guiding interceptive hand movements is not yet well understood. This review synthesizes emergent views on the importance of eye movements during manual interception with an emphasis on laboratory studies published since 2015. We discuss the role of eye movements in forming visual predictions about a moving object, and for enhancing the accuracy of interceptive hand movements through feedforward (extraretinal) and feedback (retinal) signals. We conclude by proposing a framework that defines the role of human eye movements for manual interception accuracy as a function of visual certainty and object motion predictability.

Expectations about motion direction affect perception and anticipatory smooth pursuit differently.

Smooth pursuit eye movements and visual motion perception rely on the integration of current sensory signals with past experience. Experience shapes our expectation of current visual events and can drive eye movement responses made in anticipation of a target, such as anticipatory pursuit. Previous research revealed consistent effects of expectation on anticipatory pursuit-eye movements follow the expected target direction or speed-and contrasting effects on motion perception, but most studies considered either eye movement or perceptual responses. The current study directly compared effects of direction expectation on perception and anticipatory pursuit within the same direction discrimination task to investigate whether both types of responses are affected similarly or differently. Observers (n = 10) viewed high-coherence random-dot kinematograms (RDKs) moving rightward and leftward with a probability of 50%, 70%, or 90% in a given block of trials to build up an expectation of motion direction. They were asked to judge motion direction of interleaved low-coherence RDKs (0%-15%). Perceptual judgements were compared with changes in anticipatory pursuit eye movements as a function of probability. Results show that anticipatory pursuit velocity scaled with probability and followed direction expectation (attraction bias), whereas perceptual judgments were biased opposite to direction expectation (repulsion bias). Control experiments suggest that the repulsion bias in perception was not caused by retinal slip induced by anticipatory pursuit, or by motion adaptation. We conclude that direction expectation can be processed differently for perception and anticipatory pursuit.NEW & NOTEWORTHY We show that expectations about motion direction that are based on long-term trial history affect perception and anticipatory pursuit differently. Whereas anticipatory pursuit direction was coherent with the expected motion direction (attraction bias), perception was biased opposite to the expected direction (repulsion bias). These opposite biases potentially reveal different ways in which perception and action utilize prior information and support the idea of different information processing for perception and pursuit.

Functional Use of Eye Movements for an Acting System.

Movements of the eyes assist vision and support hand and body movements in a cooperative way. Despite their strong functional coupling, different types of movements are usually studied independently. We integrate knowledge from behavioral, neurophysiological, and clinical studies on how eye movements are coordinated with goal-directed hand movements and how they facilitate motor learning. Understanding the coordinated control of eye and hand movements can provide important insights into brain functions that are essential for performing or learning daily tasks in health and disease. This knowledge can also inform applications such as robotic manipulation and clinical rehabilitation.

Do eye movements enhance visual memory retrieval?

When remembering an object at a given location, participants tend to return their gaze to that location even after the object has disappeared, known as Looking-at-Nothing (LAN). However, it is unclear whether LAN is associated with better memory performance. Previous studies reporting beneficial effects of LAN have often not systematically manipulated or assessed eye movements. We asked 20 participants to remember the location and identity of eight objects arranged in a circle, shown for 5 s. Participants were prompted to judge whether a location statement (e.g., "Star Right") was correct or incorrect, or referred to a previously unseen object. During memory retrieval, participants either fixated in the screen center or were free to move their eyes. Results reveal no difference in memory accuracy and response time between free-viewing and fixation while a LAN effect was found for saccades during free viewing, but not for microsaccades during fixation. Memory performance was better in those free-viewing trials in which participants made a saccade to the critical location, and scaled with saccade accuracy. These results indicate that saccade kinematics might be related to both memory performance and memory retrieval processes, but the strength of their link would differ between individuals and task demands.

Eye movements as a readout of sensorimotor decision processes.

Real-world tasks, such as avoiding obstacles, require a sequence of interdependent choices to reach accurate motor actions. Yet, most studies on primate decision making involve simple one-step choices. Here we analyze motor actions to investigate how sensorimotor decisions develop over time. In a go/no-go interception task human observers (n = 42) judged whether a briefly presented moving target would pass (interceptive hand movement required) or miss (no hand movement required) a strike box while their eye and hand movements were recorded. Go/no-go decision formation had to occur within the first few hundred milliseconds to allow time-critical interception. We found that the earliest time point at which eye movements started to differentiate actions (go versus no-go) preceded hand movement onset. Moreover, eye movements were related to different stages of decision making. Whereas higher eye velocity during smooth pursuit initiation was related to more accurate interception decisions (whether or not to act), faster pursuit maintenance was associated with more accurate timing decisions (when to act). These results indicate that pursuit initiation and maintenance are continuously linked to ongoing sensorimotor decision formation.NEW & NOTEWORTHY Here we show that eye movements are a continuous indicator of decision processes underlying go/no-go actions. We link different stages of decision formation to distinct oculomotor events during open- and closed-loop smooth pursuit. Critically, the earliest time point at which eye movements differentiate actions preceded hand movement onset, suggesting shared sensorimotor processing for eye and hand movements. These results emphasize the potential of studying eye movements as a readout of cognitive processes.

On the relation between anticipatory ocular torsion and anticipatory smooth pursuit.

Humans and other animals move their eyes in anticipation to compensate for sensorimotor delays. Such anticipatory eye movements can be driven by the expectation of a future visual object or event. Here we investigate whether such anticipatory responses extend to ocular torsion, the eyes' rotation about the line of sight. We recorded three-dimensional eye position in head-fixed healthy human adults who tracked a rotating dot pattern moving horizontally across a computer screen. This kind of stimulus triggers smooth pursuit with a horizontal and torsional component. In three experiments, we elicited expectation of stimulus rotation by repeatedly showing the same rotation (Experiment 1), or by using different types of higher-level symbolic cues indicating the rotation of the upcoming target (Experiments 2 and 3). Across all experiments, results reveal reliable anticipatory horizontal smooth pursuit. However, anticipatory torsion was only elicited by stimulus repetition, but not by symbolic cues. In summary, torsion can be made in anticipation of an upcoming visual event only when low-level motion signals are accumulated by repetition. Higher-level cognitive mechanisms related to a symbolic cue reliably evoke anticipatory pursuit but did not modulate torsion. These findings indicate that anticipatory torsion and anticipatory pursuit are at least partly decoupled and might be controlled separately.