Perceptual-Cognitive Integration for Goal-Directed Action in Naturalistic Environments.

Real-world actions require one to simultaneously perceive, think, and act on the surrounding world, requiring the integration of (bottom-up) sensory information and (top-down) cognitive and motor signals. Studying these processes involves the intellectual challenge of cutting across traditional neuroscience silos, and the technical challenge of recording data in uncontrolled natural environments. However, recent advances in techniques, such as neuroimaging, virtual reality, and motion tracking, allow one to address these issues in naturalistic environments for both healthy participants and clinical populations. In this review, we survey six topics in which naturalistic approaches have advanced both our fundamental understanding of brain function and how neurologic deficits influence goal-directed, coordinated action in naturalistic environments. The first part conveys fundamental neuroscience mechanisms related to visuospatial coding for action, adaptive eye-hand coordination, and visuomotor integration for manual interception. The second part discusses applications of such knowledge to neurologic deficits, specifically, steering in the presence of cortical blindness, impact of stroke on visual-proprioceptive integration, and impact of visual search and working memory deficits. This translational approach-extending knowledge from lab to rehab-provides new insights into the complex interplay between perceptual, motor, and cognitive control in naturalistic tasks that are relevant for both basic and clinical research.

Visual search for reach targets in actionable space is influenced by movement costs imposed by obstacles.

Real world search tasks often involve action on a target object once it has been located. However, few studies have examined whether movement-related costs associated with acting on located objects influence visual search. Here, using a task in which participants reached to a target object after locating it, we examined whether people take into account obstacles that increase movement-related costs for some regions of the reachable search space but not others. In each trial, a set of 36 objects (4 targets and 32 distractors) were displayed on a vertical screen and participants moved a cursor to a target after locating it. Participants had to fixate on an object to determine whether it was a target or distractor. A rectangular obstacle, of varying length, location, and orientation, was briefly displayed at the start of the trial. Participants controlled the cursor by moving the handle of a robotic manipulandum in a horizontal plane. The handle applied forces to simulate contact between the cursor and the unseen obstacle. We found that search, measured using eye movements, was biased to regions of the search space that could be reached without moving around the obstacle. This result suggests that when deciding where to search, people can incorporate the physical structure of the environment so as to reduce the movement-related cost of subsequently acting on the located target.

The influence of movement-related costs when searching to act and acting to search.

Real-world search behavior often involves limb movements, either during search or after search. Here we investigated whether movement-related costs influence search behavior in two kinds of search tasks. In our visual search tasks, participants made saccades to find a target object among distractors and then moved a cursor, controlled by the handle of a robotic manipulandum, to the target. In our manual search tasks, participants moved the cursor to perform the search, placing it onto objects to reveal their identity as either a target or a distractor. In all tasks, there were multiple targets. Across experiments, we manipulated either the effort or time costs associated with movement such that these costs varied across the search space. We varied effort by applying different resistive forces to the handle, and we varied time costs by altering the speed of the cursor. Our analysis of cursor and eye movements during manual and visual search, respectively, showed that effort influenced manual search but did not influence visual search. In contrast, time costs influenced both visual and manual search. Our results demonstrate that, in addition to perceptual and cognitive factors, movement-related costs can also influence search behavior.NEW & NOTEWORTHY Numerous studies have investigated the perceptual and cognitive factors that influence decision making about where to look, or move, in search tasks. However, little is known about how search is influenced by movement-related costs associated with acting on an object once it has been visually located or acting during manual search. In this article, we show that movement time costs can bias visual and manual search and that movement effort costs bias manual search.

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.

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.

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.

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.

Zoned in or zoned out? Investigating immersion in slot machine gambling using mobile eye-tracking.

BACKGROUND AND AIMS: Immersion during slot machine gambling has been linked to disordered gambling. Current conceptualizations of immersion (namely dissociation, flow and the machine zone) make contrasting predictions as to whether gamblers are captivated by the game per se ('zoned in') or motivated by the escape that immersion provides ('zoned out'). We examined whether selected eye-movement metrics can distinguish between these predictions. DESIGN AND SETTING: Pre-registered, correlational analysis in a laboratory setting. Participants gambled on a genuine slot machine for 20 minutes while wearing eye-tracking glasses. PARTICIPANTS: Fifty-three adult slot machine gamblers who were not high-risk problem gamblers. MEASUREMENTS: We examined self-reported immersion during the gambling session and eye movements at different areas of the slot machine screen (the reels, the credit window, etc.). We further explored these variables' relationships with saccade count and amplitude. FINDINGS: The ratio of dwell time on the game's credit window relative to the game's reels was positively associated with immersion (t(51)  = 1.68, P = 0.049 one-tailed, R2  = 0.05). Follow-up analyses described event-related changes in these patterns following different spin outcomes. CONCLUSIONS: Immersion while gambling on a slot machine appears to be associated with active scanning of the game and a focus on the game's credit window. These results are more consistent with a 'zoned in' account of immersion aligned with flow theory than a 'zoned out' account based on escape.

Decoding go/no-go decisions from eye movements.

Neural activity in brain areas involved in the planning and execution of eye movements predicts the outcome of an upcoming perceptual decision. Many real-world decisions, such as whether to swing at a baseball pitch, are accompanied by characteristic eye-movement behavior. Here we ask whether human eye-movement kinematics can sensitively predict decision outcomes in a go/no-go task requiring rapid interceptive hand movements. Observers (n = 45) viewed a moving target that passed through or missed a designated strike box. Critically, the target disappeared briefly after launch, and observers had to predict the target's trajectory, withholding a hand movement if it missed (no-go) or intercepting inside the strike box (go). We found that go/no-go decisions were reflected in distinct eye-movement responses on a trial-by-trial basis: Eye-position error and targeting-saccade dynamics predicted decision outcome with 76% accuracy across conditions. Model prediction accuracy was related to observers' decision accuracy across different levels of task difficulty and sensory-signal strength. Our findings suggest that eye movements provide a sensitive and continuous readout of internal neural decision-making processes and reflect decision-task requirements in human observers.

Perception of Looming Motion in Virtual Reality Egocentric Interception Tasks.

Motion in depth is commonly misperceived in Virtual Reality (VR), making it difficult to intercept moving objects, for example, in games. We investigate whether motion cues could be modified to improve these interactions in VR. We developed a time-to-contact estimation task, in which observers ($n=18$n=18) had to indicate by button press when a looming virtual object would collide with their head. We show that users consistently underestimate speed. We construct a user-specific model of motion-in-depth perception, and use this model to propose a novel method to modify monocular depth cues tailored to the specific user, correcting individual response errors in speed estimation. A user study was conducted in a simulated baseball environment and observers were asked to hit a looming baseball back in the direction of the pitcher. The study was conducted with and without intervention and demonstrates the effectiveness of the method in reducing interception errors following cue modifications. The intervention was particularly effective at fast ball speeds where performance is most limited by the user's sensorimotor constraints. The proposed approach is easy to implement and could improve the user experience of interacting with dynamic virtual environments.

Eye movement training is most effective when it involves a task-relevant sensorimotor decision.

Eye and hand movements are closely linked when performing everyday actions. We conducted a perceptual-motor training study to investigate mutually beneficial effects of eye and hand movements, asking whether training in one modality benefits performance in the other. Observers had to predict the future trajectory of a briefly presented moving object, and intercept it at its assumed location as accurately as possible with their finger. Eye and hand movements were recorded simultaneously. Different training protocols either included eye movements or a combination of eye and hand movements with or without external performance feedback. Eye movement training did not transfer across modalities: Irrespective of feedback, finger interception accuracy and precision improved after training that involved the hand, but not after isolated eye movement training. Conversely, eye movements benefited from hand movement training or when external performance feedback was given, thus improving only when an active interceptive task component was involved. These findings indicate only limited transfer across modalities. However, they reveal the importance of creating a training task with an active sensorimotor decision to improve the accuracy and precision of eye and hand movements.

Context effects on smooth pursuit and manual interception of a disappearing target.

In our natural environment, we interact with moving objects that are surrounded by richly textured, dynamic visual contexts. Yet most laboratory studies on vision and movement show visual objects in front of uniform gray backgrounds. Context effects on eye movements have been widely studied, but it is less well known how visual contexts affect hand movements. Here we ask whether eye and hand movements integrate motion signals from target and context similarly or differently, and whether context effects on eye and hand change over time. We developed a track-intercept task requiring participants to track the initial launch of a moving object ("ball") with smooth pursuit eye movements. The ball disappeared after a brief presentation, and participants had to intercept it in a designated "hit zone." In two experiments (n = 18 human observers each), the ball was shown in front of a uniform or a textured background that either was stationary or moved along with the target. Eye and hand movement latencies and speeds were similarly affected by the visual context, but eye and hand interception (eye position at time of interception, and hand interception timing error) did not differ significantly between context conditions. Eye and hand interception timing errors were strongly correlated on a trial-by-trial basis across all context conditions, highlighting the close relation between these responses in manual interception tasks. Our results indicate that visual contexts similarly affect eye and hand movements but that these effects may be short-lasting, affecting movement trajectories more than movement end points.NEW & NOTEWORTHY In a novel track-intercept paradigm, human observers tracked a briefly shown object moving across a textured, dynamic context and intercepted it with their finger after it had disappeared. Context motion significantly affected eye and hand movement latency and speed, but not interception accuracy; eye and hand position at interception were correlated on a trial-by-trial basis. Visual context effects may be short-lasting, affecting movement trajectories more than movement end points.

Distinct eye movement patterns enhance dynamic visual acuity.

Dynamic visual acuity (DVA) is the ability to resolve fine spatial detail in dynamic objects during head fixation, or in static objects during head or body rotation. This ability is important for many activities such as ball sports, and a close relation has been shown between DVA and sports expertise. DVA tasks involve eye movements, yet, it is unclear which aspects of eye movements contribute to successful performance. Here we examined the relation between DVA and the kinematics of smooth pursuit and saccadic eye movements in a cohort of 23 varsity baseball players. In a computerized dynamic-object DVA test, observers reported the location of the gap in a small Landolt-C ring moving at various speeds while eye movements were recorded. Smooth pursuit kinematics-eye latency, acceleration, velocity gain, position error-and the direction and amplitude of saccadic eye movements were linked to perceptual performance. Results reveal that distinct eye movement patterns-minimizing eye position error, tracking smoothly, and inhibiting reverse saccades-were related to dynamic visual acuity. The close link between eye movement quality and DVA performance has important implications for the development of perceptual training programs to improve DVA.

Eye movement accuracy determines natural interception strategies.

Eye movements aid visual perception and guide actions such as reaching or grasping. Most previous work on eye-hand coordination has focused on saccadic eye movements. Here we show that smooth pursuit eye movement accuracy strongly predicts both interception accuracy and the strategy used to intercept a moving object. We developed a naturalistic task in which participants (n = 42 varsity baseball players) intercepted a moving dot (a "2D fly ball") with their index finger in a designated "hit zone." Participants were instructed to track the ball with their eyes, but were only shown its initial launch (100-300 ms). Better smooth pursuit resulted in more accurate interceptions and determined the strategy used for interception, i.e., whether interception was early or late in the hit zone. Even though early and late interceptors showed equally accurate interceptions, they may have relied on distinct tactics: early interceptors used cognitive heuristics, whereas late interceptors' performance was best predicted by pursuit accuracy. Late interception may be beneficial in real-world tasks as it provides more time for decision and adjustment. Supporting this view, baseball players who were more senior were more likely to be late interceptors. Our findings suggest that interception strategies are optimally adapted to the proficiency of the pursuit system.