Perception-action Dissociations as a Window into Consciousness.

Understanding the neural correlates of unconscious perception stands as a primary goal of experimental research in cognitive psychology and neuroscience. In this Perspectives paper, we explain why experimental protocols probing qualitative dissociations between perception and action provide valuable insights into conscious and unconscious processing, along with their corresponding neural correlates. We present research that utilizes human eye movements as a sensitive indicator of unconscious visual processing. Given the increasing reliance on oculomotor and pupillary responses in consciousness research, these dissociations also provide a cautionary tale about inferring conscious perception solely based on no-report protocols.

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.

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.

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.

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.

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.

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.

Introduction to special issue on "Prediction in Perception and Action".

The wide diversity of articles in this issue reveals an explosion of evidence for the mechanisms of prediction in the visual system. When thought of as visual priors, predictive mechanisms can be seen as tightly interwoven with incoming sensory data. Prediction is thus a fundamental and essential aspect not only of visual perception but of the actions that are guided by perception.

Ocular torsion is related to perceived motion-induced position shifts.

Ocular torsion (i.e., rotations of the eye about the line of sight) can be induced by visual rotational motion. It remains unclear whether and how such visually induced torsion is related to perception. By using the flash-grab effect, an illusory position shift of a briefly flashed stationary target superimposed on a rotating pattern, we examined the relationship between torsion and perception. In two experiments, 25 observers reported the perceived location of a flash while their three-dimensional eye movements were recorded. In Experiment 1, the flash coincided with a direction reversal of a large, centrally displayed, rotating grating. The grating triggered visually induced torsion in the direction of stimulus rotation. The magnitude of torsional eye rotation correlated with the illusory perceptual position shift. To test whether torsion caused the illusion, in Experiment 2, the flash was superimposed on two peripheral gratings rotating in opposite directions. Even though torsion was eliminated, the illusory position shift persisted. Despite the lack of a causal relationship, the torsion-perception correlations indicate a close link between both systems, either through similar visual-input processing or a boost of visual rotational signal strength via oculomotor feedback.

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.

Prediction in goal-directed action.

Prediction allows humans and other animals to prepare for future interactions with their environment. This is important in our dynamically changing world that requires fast and accurate reactions to external events. Knowing when and where an event is likely to occur allows us to plan eye, hand, and body movements that are suitable for the circumstances. Predicting the sensory consequences of such movements helps to differentiate between self-produced and externally generated movements. In this review, we provide a selective overview of experimental studies on predictive mechanisms in human vision for action. We present classic paradigms and novel approaches investigating mechanisms that underlie the prediction of events guiding eye and hand movements.

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.

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.

Efference copy failure during smooth pursuit eye movements in schizophrenia.

Abnormal smooth pursuit eye movements in patients with schizophrenia are often considered a consequence of impaired motion perception. Here we used a novel motion prediction task to assess the effects of abnormal pursuit on perception in human patients. Schizophrenia patients (n = 15) and healthy controls (n = 16) judged whether a briefly presented moving target ("ball") would hit/miss a stationary vertical line segment ("goal"). To relate prediction performance and pursuit directly, we manipulated eye movements: in half of the trials, observers smoothly tracked the ball; in the other half, they fixated on the goal. Strict quality criteria ensured that pursuit was initiated and that fixation was maintained. Controls were significantly better in trajectory prediction during pursuit than during fixation, their performance increased with presentation duration, and their pursuit gain and perceptual judgments were correlated. Such perceptual benefits during pursuit may be due to the use of extraretinal motion information estimated from an efference copy signal. With an overall lower performance in pursuit and perception, patients showed no such pursuit advantage and no correlation between pursuit gain and perception. Although patients' pursuit showed normal improvement with longer duration, their prediction performance failed to benefit from duration increases. This dissociation indicates relatively intact early visual motion processing, but a failure to use efference copy information. Impaired efference function in the sensory system may represent a general deficit in schizophrenia and thus contribute to symptoms and functional outcome impairments associated with the disorder.

Perceptual learning modifies untrained pursuit eye movements.

Perceptual learning improves detection and discrimination of relevant visual information in mature humans, revealing sensory plasticity. Whether visual perceptual learning affects motor responses is unknown. Here we implemented a protocol that enabled us to address this question. We tested a perceptual response (motion direction estimation, in which observers overestimate motion direction away from a reference) and a motor response (voluntary smooth pursuit eye movements). Perceptual training led to greater overestimation and, remarkably, it modified untrained smooth pursuit. In contrast, pursuit training did not affect overestimation in either pursuit or perception, even though observers in both training groups were exposed to the same stimuli for the same time period. A second experiment revealed that estimation training also improved discrimination, indicating that overestimation may optimize perceptual sensitivity. Hence, active perceptual training is necessary to alter perceptual responses, and an acquired change in perception suffices to modify pursuit, a motor response.