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

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

Smooth pursuit deficits impact dynamic visual acuity in macular degeneration.

SIGNIFICANCE: Prior studies with large, highly visible targets report low smooth pursuit gains in individuals with macular degeneration (MD). We show that lower gains persist even when observers are pursuing a target that requires discrimination at the acuity limit. This low gain causes retinal slip, potentially leading to motion blur and target disappearance in the scotoma, which further compromise the visibility of moving object. PURPOSE: In this study, we examine whether the characteristics of smooth pursuit (pursuit gain and placement of the fixational locus relative to the target) change when the task requires dynamic visual acuity. METHODS: Using the scanning laser ophthalmoscope, we recorded smooth pursuit eye movements in 10 eyes of 6 MD participants and 7 eyes of 4 age-matched controls in response to leftward- or rightward-moving annular targets (O) that briefly (300 milliseconds) changed to a Landolt C at one of several time points during the pursuit trial. Participants were asked to pursue the target and indicate the direction of the C opening. RESULTS: Individuals with MD had lower pursuit gains and fewer saccades during the C presentation than during the O, compared with their age-matched peers. Further, pursuit gain, but not the distance of the retinal pursuit locus from the target, predicted task performance in the MD group. CONCLUSIONS: Our findings suggest that compromised pursuit gain in MD participants likely further compromises their dynamic visual acuity and thus ability to view moving targets.

An Exploratory Analysis of Physical Examination Subtypes in Pediatric Athletes With Concussion.

OBJECTIVE: Pediatric athletes with concussion present with a variety of impairments on clinical assessment and require individualized treatment. The Buffalo Concussion Physical Examination is a brief, pertinent clinical assessment for individuals with concussion. The purpose of this study was to identify physical examination subtypes in pediatric athletes with concussion within 2 weeks of injury that are relevant to diagnosis and treatment. DESIGN: Secondary analysis of a published cohort study and clinician consensus. SETTING: Three university-affiliated sports medicine centers. PARTICIPANTS: Two hundred seventy children (14.9 ± 1.9 years). INDEPENDENT VARIABLES: Orthostatic intolerance, horizontal and vertical saccades, smooth pursuits, vestibulo-ocular reflex, near-point convergence, complex tandem gait, neck range of motion, neck tenderness, and neck spasm. MAIN OUTCOME MEASURES: Correlations between independent variables were calculated, and network graphs were made. k -means and hierarchical clustering were used to identify clusters of impairments. Optimal number of clusters was assessed. Results were reviewed by experienced clinicians and consensus was reached on proposed subtypes. RESULTS: Physical examination clusters overlapped with each other, and no optimal number of clusters was identified. Clinician consensus suggested 3 possible subtypes: (1) visio-vestibular (horizontal and vertical saccades, smooth pursuits, and vestibulo-ocular reflex), (2) cervicogenic (neck range of motion and spasm), and (3) autonomic/balance (orthostatic intolerance and complex tandem gait). CONCLUSIONS: Although we identified 3 physical examination subtypes, it seemed that physical examination findings alone are not enough to define subtypes that are both statistically supported and clinically relevant, likely because they do not include symptoms, assessment of mood or cognitive problems, or graded exertion testing.

EEG Activity during Pursuit and Saccade Visual Strategies to Predict the Arrival Position of a Target.

BACKGROUND: In this study, we used electroencephalogram (EEG) to investigate the activity pattern of the cerebral cortex related to visual pursuit and saccade strategies to predict the arrival position of a visual target. In addition, we clarified the differences in the EEG of those who could predict the arrival position well using the saccade strategy compared to those who were not proficient. METHODS: Sixteen participants performed two tasks: the "Pursuit Strategy Task (PST)" and the "Saccade Strategy Task (SST)" while undergoing EEG. For the PST, the participants were instructed to follow the target with their eyes throughout its trajectory and indicate when it reached the final point. For the SST, the participants were instructed to shift their gaze to the end point of arrival once they had predicted it. RESULTS: Low beta EEG activity at the Oz, Cz, and CP2 electrodes was significantly higher during the SST than during the PST. In addition, low beta EEG activity at P7 electrode was significantly higher in the group showing a small position error (PE) than in the group showing a large PE at response. CONCLUSIONS: EEG activity at the Oz, Cz, and CP2 electrodes during the SST may reflect visuospatial attention to the moving target, the tracking of moving targets, and the focus on the final destination position. In addition, EEG activity at P7 electrode may more accurately detect the speed and direction of the moving target by the small PE group at response.

(The limits of) eye-tracking with iPads.

Applications for eye-tracking-particularly in the clinic-are limited by a reliance on dedicated hardware. Here we compare eye-tracking implemented on an Apple iPad Pro 11" (third generation)-using the device's infrared head-tracking and front-facing camera-with a Tobii 4c infrared eye-tracker. We estimated gaze location using both systems while 28 observers performed a variety of tasks. For estimating fixation, gaze position estimates from the iPad were less accurate and precise than the Tobii (mean absolute error of 3.2° ± 2.0° compared with 0.75° ± 0.43°), but fixation stability estimates were correlated across devices (r = 0.44, p < 0.05). For tasks eliciting saccades >1.5°, estimated saccade counts (r = 0.4-0.73, all p < 0.05) were moderately correlated across devices. For tasks eliciting saccades >8° we observed moderate correlations in estimated saccade speed and amplitude (r = 0.4-0.53, all p < 0.05). We did, however, note considerable variation in the vertical component of estimated smooth pursuit speed from the iPad and a catastrophic failure of tracking on the iPad in 5% to 20% of observers (depending on the test). Our findings sound a note of caution to researchers seeking to use iPads for eye-tracking and emphasize the need to properly examine their eye-tracking data to remove artifacts and outliers.

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.

Confidence in predicted position error explains saccadic decisions during pursuit.

A fundamental problem in motor control is the coordination of complementary movement types to achieve a common goal. As a common example, humans view moving objects through coordinated pursuit and saccadic eye movements. Pursuit is initiated and continuously controlled by retinal image velocity. During pursuit, eye position may lag behind the target. This can be compensated by the discrete execution of a catch-up saccade. The decision to trigger a saccade is influenced by both position and velocity errors, and the timing of saccades can be highly variable. The observed distributions of saccade frequency and trigger time remain poorly understood, and this decision process remains imprecisely quantified. Here, we propose a predictive, probabilistic model explaining the decision to trigger saccades during pursuit to foveate moving targets. In this model, expected position error and its associated uncertainty are predicted through Bayesian inference across noisy, delayed sensory observations (Kalman filtering). This probabilistic prediction is used to estimate the confidence that a saccade is needed (quantified through log-probability ratio), triggering a saccade upon accumulating to a fixed threshold. The model qualitatively explains behavioral observations on the frequency and trigger time distributions of saccades during pursuit over a range of target motion trajectories. Furthermore, this model makes novel predictions that saccade decisions are highly sensitive to uncertainty for small predicted position errors, but this influence diminishes as the magnitude of predicted position error increases. We suggest that this predictive, confidence-based decision-making strategy represents a fundamental principle for the probabilistic neural control of coordinated movements.NEW & NOTEWORTHY This is the first stochastic dynamical systems model of pursuit-saccade coordination accounting for noise and delays in the sensorimotor system. The model uses Bayesian inference to predictively estimate visual motion, triggering saccades when confidence in predicted position error accumulates to a threshold. This model explains saccade frequency and trigger time distributions across target trajectories and makes novel predictions about the influence of sensory uncertainty in saccade decisions during pursuit.

Micro-pursuit: A class of fixational eye movements correlating with smooth, predictable, small-scale target trajectories.

Humans generate ocular pursuit movements when a moving target is tracked throughout the visual field. In this article, we show that pursuit can be generated and measured at small amplitudes, at the scale of fixational eye movements, and tag these eye movements as micro-pursuits. During micro-pursuits, gaze direction correlates with a target's smooth, predictable target trajectory. We measure similarity between gaze and target trajectories using a so-called maximally projected correlation and provide results in three experimental data sets. A first observation of micro-pursuit is provided in an implicit pursuit task, where observers were tasked to maintain their gaze fixed on a static cross at the center of screen, while reporting changes in perception of an ambiguous, moving (Necker) cube. We then provide two experimental paradigms and their corresponding data sets: a first replicating micro-pursuits in an explicit pursuit task, where observers had to follow a moving fixation cross (Cross), and a second with an unambiguous square (Square). Individual and group analyses provide evidence that micro-pursuits exist in both the Necker and Cross experiments but not in the Square experiment. The interexperiment analysis results suggest that the manipulation of stimulus target motion, task, and/or the nature of the stimulus may play a role in the generation of micro-pursuits.

The role of frontal pursuit area in interaction between smooth pursuit eye movements and attention: A TMS study.

Close coupling between attention and smooth pursuit eye movements has been widely established and frontal eye field (FEF) is a "hub" region for attention and eye movements. Frontal pursuit area (FPA), a subregion of the FEF, is part of neural circuit for the pursuit, here, we directly checked the role of the FPA in the interaction between the pursuit and attention. To do it, we applied a dual-task paradigm where an attention demanding task was integrated into the pursuit target and interrupted the FPA using transcranial magnetic stimulation (TMS). In the study, participants were required to pursue a moving circle with a letter inside, which changed to another one every 100 ms and report whether "H" (low attentional load) or one of "H," "S," or "L" (high attentional load) appeared during the trial. As expected, increasing the attentional load decreased accuracy of the letter detection. Importantly, the FPA TMS had no effect on both the pursuit and letter detection tasks in the low load condition, whereas it reduced 200 to 320 ms gain, but tended to increase the letter detection accuracy in the high load condition. Moreover, individual's FPA TMS effect on pursuit gain was significantly correlated with that on letter detection accuracy. Presumably, the pursuit gain control by the FPA was compensated by attention in low load condition, and the FPA may flexibly allocate attentional resources between the pursuit and letter detection task in high load condition. Altogether, it seems that the FPA has a control over attentional allocation between tasks.

Oculomotor inhibition during smooth pursuit and its dependence on contrast sensitivity.

Our eyes are never still, but tend to "freeze" in response to stimulus onset. This effect is termed "oculomotor inhibition" (OMI); its magnitude and time course depend on the stimulus parameters, attention, and expectation. We previously showed that the time course and duration of microsaccade and spontaneous eye-blink inhibition provide an involuntary measure of low-level visual properties such as contrast sensitivity during fixation. We investigated whether this stimulus-dependent inhibition also occurs during smooth pursuit, for both the catch-up saccades and the pursuit itself. Observers followed a target with continuous back-and-forth horizontal motion while a Gabor patch was briefly flashed centrally with varied spatial frequency and contrast. Catch-up saccades of the size of microsaccades had a similar pattern of inhibition as microsaccades during fixation, with stronger inhibition onset and faster inhibition release for more salient stimuli. Moreover, a similar stimulus dependency of inhibition was shown for pursuit latencies and peak velocity. Additionally, microsaccade latencies at inhibition release, peak pursuit velocities, and latencies at minimum pursuit velocity were correlated with contrast sensitivity. We demonstrated the generality of OMI to smooth pursuit for both microsaccades and the pursuit itself and its close relation to the low-level processes that define saliency, such as contrast sensitivity.

Eye Position Error Influence over "Open-Loop" Smooth Pursuit Initiation.

The oculomotor system integrates a variety of visual signals into appropriate motor plans, but such integration can have widely varying time scales. For example, smooth pursuit eye movements to follow a moving target are slower and longer lasting than saccadic eye movements and it has been suggested that initiating a smooth pursuit eye movement involves an obligatory "open-loop" interval in which new visual motion signals presumably cannot influence the ensuing motor plan for up to 100 ms after movement initiation. However, this view is contrary to the idea that the oculomotor periphery has privileged access to short-latency visual signals. Here, we show that smooth pursuit initiation is sensitive to visual inputs, even in open-loop intervals. We instructed male rhesus macaque monkeys to initiate saccade-free smooth pursuit eye movements and injected a transient, instantaneous eye position error signal at different times relative to movement initiation. We found robust short-latency modulations in eye velocity and acceleration, starting only ∼50 ms after transient signal occurrence and even during open-loop pursuit initiation. Critically, the spatial direction of the injected position error signal had predictable effects on smooth pursuit initiation, with forward errors increasing eye acceleration and backward errors reducing it. Catch-up saccade frequencies and amplitudes were also similarly altered ∼50 ms after transient signals, much like the well known effects on microsaccades during fixation. Our results demonstrate that smooth pursuit initiation is highly sensitive to visual signals and that catch-up saccade generation is reset after a visual transient.SIGNIFICANCE STATEMENT Smooth pursuit eye movements allow us to track moving objects. The first ∼100 ms of smooth pursuit initiation are characterized by smooth eye acceleration and are overwhelmingly described as being "open-loop"; that is, unmodifiable by new visual motion signals. We found that all phases of smooth pursuit, including the so-called open-loop intervals, are reliably modifiable by visual signals. We injected transient flashes resulting in very brief, spatially specific position error signals to smooth pursuit and observed very short-latency changes in smooth eye movements to minimize such errors. Our results highlight the flexibility of the oculomotor system in reacting to environmental events and suggest a functional role for the pervasiveness of visual sensitivity in oculomotor control brain regions.

Retinal Stabilization Reveals Limited Influence of Extraretinal Signals on Heading Tuning in the Medial Superior Temporal Area.

Heading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable, even though smooth-pursuit eye movements often distort optic flow. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing. Our results from 3 female monkeys demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions.SIGNIFICANCE STATEMENT Sensory systems discount stimulation caused by an animal's own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. The latter can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that extraretinal signals have little influence on activity in visual cortex, whereas visually based corrections for ongoing eye movements have stronger effects and are likely most important under real-world conditions.

Following Forrest Gump: Smooth pursuit related brain activation during free movie viewing.

Most fMRI studies investigating smooth pursuit (SP) related brain activity have used simple synthetic stimuli such as a sinusoidally moving dot. However, real-life situations are much more complex and SP does not occur in isolation but within sequences of saccades and fixations. This raises the question whether the same brain networks for SP that have been identified under laboratory conditions are activated when following moving objects in a movie. Here, we used the publicly available studyforrest data set that provides eye movement recordings along with 3 â€‹T fMRI recordings from 15 subjects while watching the Hollywood movie "Forrest Gump". All three major eye movement events, namely fixations, saccades, and smooth pursuit, were detected with a state-of-the-art algorithm. In our analysis, smooth pursuit (SP) was the eye movement of interest, while saccades were acting as the steady state of viewing behaviour due to their lower variability. For the fMRI analysis we used an event-related design modelling saccades and SP as regressors initially. Because of the interdependency of SP and content motion, we then added a new low-level content motion regressor to separate brain activations from these two sources. We identified higher BOLD-responses during SP than saccades bilaterally in MT+/V5, in middle cingulate extending to precuneus, and in the right temporoparietal junction. When the motion regressor was added, SP showed higher BOLD-response relative to saccades bilaterally in the cortex lining the superior temporal sulcus, precuneus, and supplementary eye field, presumably due to a confounding effect of background motion. Only parts of V2 showed higher activation during saccades in comparison to SP. Taken together, our approach should be regarded as proof of principle for deciphering brain activity related to SP, which is one of the most prominent eye movements besides saccades, in complex dynamic naturalistic situations.

Eye, head, and gaze contributions to smooth pursuit in macular degeneration.

Macular degeneration (MD) often leads to the loss of the fovea and surrounding central visual field. This type of visual loss is very common and can present particular challenges for oculomotor tasks that may rely on the fovea. For certain tasks, individuals develop a new, eccentric fixational locus. Our previous work has shown that smooth pursuit is impaired in MD. However, extent of retinal lesion size and eccentricity of fixation do not directly contribute to changes in smooth pursuit gain. Oculomotor limitations due to eccentric eye position in the orbit may be another culprit. Here we test the hypothesis that deficits in smooth pursuit in MD would be reduced under head-unrestrained conditions. To that end, we examined eye, head, and gaze movements in eight individuals with MD and seven age-matched controls in response to a step-ramp pursuit stimulus. We found that despite variability across participants, both groups had similar smooth pursuit head movements (P = 0.76), while both had significantly higher pursuit gains in the head-restrained condition (P < 0.0001), suggesting that in older populations, head movements may lead to a decrease in pursuit gain. Furthermore, we did not find a correlation between eccentricity of fixation and amount of head displacement during the trial (P = 0.25), suggesting that eccentric eye position does not lead to higher reliance on head movements in smooth pursuit. Our finding that individuals with MD have lower pursuit gains, despite similar head movements as controls, suggests a difference in how MD affects mechanisms underlying eye versus head movements in smooth pursuit.NEW & NOTEWORTHY This article is the first to look at eye and head movements in observers with macular degeneration. It is the first to show that in older individuals, regardless of central field defect, freedom of head movement may reduce pursuit gain. Despite oculomotor limitations due to eccentric fixation, individuals with macular degeneration do not rely on head movements more than age-matched controls, with both groups having a similarly heterogenous eye and head movement strategy for pursuit.

Different mechanisms for modulation of the initiation and steady-state of smooth pursuit eye movements.

Smooth pursuit eye movements are used by primates to track moving objects. They are initiated by sensory estimates of target speed represented in the middle temporal (MT) area of extrastriate visual cortex and then supported by motor feedback to maintain steady-state eye speed at target speed. Here, we show that reducing the coherence in a patch of dots for a tracking target degrades the eye speed both at the initiation of pursuit and during steady-state tracking, when eye speed reaches an asymptote well below target speed. The deficits are quantitatively different between the motor-supported steady-state of pursuit and the sensory-driven initiation of pursuit, suggesting separate mechanisms. The deficit in visually guided pursuit initiation could not explain the deficit in steady-state tracking. Pulses of target speed during steady-state tracking revealed lower sensitivities to image motion across the retina for lower values of dot coherence. However, sensitivity was not zero, implying that visual motion should still be driving eye velocity toward target velocity. When we changed dot coherence from 100% to lower values during accurate steady-state pursuit, we observed larger eye decelerations for lower coherences, as expected if motor feedback was reduced in gain. A simple pursuit model accounts for our data based on separate modulation of the strength of visual-motor transmission and motor feedback. We suggest that reduced dot coherence allows us to observe evidence for separate modulations of the gain of visual-motor transmission during pursuit initiation and of the motor corollary discharges that comprise eye velocity memory and support steady-state tracking.NEW & NOTEWORTHY We exploit low-coherence patches of dots to control the initiation and steady state of smooth pursuit eye movements and show that these two phases of movement are modulated separately by the reliability of visual motion signals. We conclude that the neural circuit for pursuit includes separate modulation of the strength of visual-motor transmission for movement initiation and of eye velocity positive feedback to support steady-state tracking.

Suppressive control of optokinetic and vestibular nystagmus by the primate frontal eye field.

When the eyes are fixated on a spot, fixation neurons in the frontal eye field (FEF) show an increase in activity. Our previous study suggested that fixation neurons in the FEF contribute to the suppression of saccades and smooth pursuit eye movements to maintain active fixation. The present study examined the role of the FEF in the suppressive control of reflexive eye movements, optokinetic and vestibular nystagmus, in trained monkeys. Electrical stimulation in the FEF suppressed the quick and slow phases of optokinetic and vestibular nystagmus at an intensity lower than the threshold for eliciting electrically evoked saccades. Relatively weak suppression influenced the slow phase of vestibular nystagmus. During optokinetic or vestibular nystagmus, presentation of a stationary small spot to the eyes followed by fixation is known to suppress both the quick and slow phases of eye movements. We recorded the activity of fixation neurons in the FEF and found that fixation neurons usually showed a decrease in activity during optokinetic and vestibular nystagmus and an increase in activity during the suppression of nystagmus by visual fixation. The present results show that the activity of fixation neurons in the FEF is related to the suppressive control of optokinetic and vestibular nystagmus for maintaining active fixation. We discuss the role of a generalized visual fixation system that can maintain visual attention on an interesting object.NEW & NOTEWORTHY In this study, electrical stimulation in the frontal eye field (FEF) suppressed the quick and slow phases of optokinetic and vestibular nystagmus at an intensity subthreshold for eliciting saccades. Furthermore, the activity of fixation neurons in the FEF was related to the suppression of optokinetic and vestibular nystagmus by visual fixation. This suggests that a common neuronal assembly in the FEF may contribute to the suppressive control of different functional classes of eye movements.

Perceptual decisions about object shape bias visuomotor coordination during rapid interception movements.

Visual processing in parietal areas of the dorsal stream facilitates sensorimotor transformations for rapid movement. This action-related visual processing is hypothesized to play a distinct functional role from perception-related processing in the ventral stream. However, it is unclear how the two streams interact when perceptual identification is a prerequisite to executing an accurate movement. In the current study, we investigated how perceptual decision-making involving the ventral stream influences arm and eye movement strategies. Participants (n = 26) moved a robotic manipulandum using right whole arm movements to rapidly reach a stationary object or intercept a moving object on an augmented-reality display. On some blocks of trials, participants needed to identify the shape of the object (circle or ellipse) as a cue to either hit the object (circle) or move to a predefined location away from the object (ellipse). We found that during perceptual decision-making, there was an increased urgency to act during interception movements relative to reaching, which was associated with more decision errors. Faster hand reaction times were associated with a strategy to adjust the movement postinitiation, and this strategy was more prominent during interception. Saccadic reaction times were faster and initial saccadic peak velocity, initial gaze lags, and gains greater during decisions, suggesting that eye movements adapt to perceptual decision-making requirements. Together, our findings suggest that the integration of ventral stream information with visuomotor planning depends on imposed (or perceived) task demands.NEW & NOTEWORTHY Visual processing for perception and for action is thought to be mediated by two specialized neural pathways. Using a visuomotor decision-making task, we show that participants differentially utilized online perceptual decision-making in reaching and interception and that eye movements necessary for perception influenced motor decision strategies. These results provide evidence that task complexity modulates how pathways processing perception versus action information interact during the visual control of movement.

Encoding of eye movements explains reward-related activity in cerebellar simple spikes.

The cerebellum exhibits both motor and reward-related signals. However, it remains unclear whether reward is processed independently from the motor command or might reflect the motor consequences of the reward drive. To test how reward-related signals interact with sensorimotor processing in the cerebellum, we recorded Purkinje cell simple spike activity in the cerebellar floccular complex while monkeys were engaged in smooth pursuit eye movement tasks. The color of the target signaled the size of the reward the monkeys would receive at the end of the target motion. When the tracking task presented a single target, both pursuit and neural activity were only slightly modulated by the reward size. The reward modulations in single cells were rarely large enough to be detected. These modulations were only significant in the population analysis when we averaged across many neurons. In two-target tasks where the monkey learned to select based on the size of the reward outcome, both behavior and neural activity adapted rapidly. In both the single- and two-target tasks, the size of the reward-related modulation matched the size of the effect of reward on behavior. Thus, unlike cortical activity in eye movement structures, the reward-related signals could not be dissociated from the motor command. These results suggest that reward information is integrated with the eye movement command upstream of the Purkinje cells in the floccular complex. Thus reward-related modulations of the simple spikes are akin to modulations found in motor behavior and not to the central processing of the reward value.NEW & NOTEWORTHY Disentangling sensorimotor and reward signals is only possible if these signals do not completely overlap. We recorded activity in the floccular complex of the cerebellum while monkeys performed tasks designed to separate representations of reward from those of movement. Activity modulation by reward could be accounted for by the coding of eye movement parameters, suggesting that reward information is already integrated into motor commands upstream of the floccular complex.

Functional connectivity during smooth pursuit eye movements.

Smooth pursuit eye movements (SPEM) hold the image of a slowly moving stimulus on the fovea. The neural system underlying SPEM primarily includes visual, parietal, and frontal areas. In the present study, we investigated how these areas are functionally coupled and how these couplings are influenced by target motion frequency. To this end, healthy participants (n = 57) were instructed to follow a sinusoidal target stimulus moving horizontally at two different frequencies (0.2 Hz, 0.4 Hz). Eye movements and blood oxygen level-dependent (BOLD) activity were recorded simultaneously. Functional connectivity of the key areas of the SPEM network was investigated with a psychophysiological interaction (PPI) approach. How activity in five eye movement-related seed regions (lateral geniculate nucleus, V1, V5, posterior parietal cortex, frontal eye fields) relates to activity in other parts of the brain during SPEM was analyzed. The behavioral results showed clear deterioration of SPEM performance at higher target frequency. BOLD activity during SPEM versus fixation occurred in a geniculo-occipito-parieto-frontal network, replicating previous findings. PPI analysis yielded widespread, partially overlapping networks. In particular, frontal eye fields and posterior parietal cortex showed task-dependent connectivity to large parts of the entire cortex, whereas other seed regions demonstrated more regionally focused connectivity. Higher target frequency was associated with stronger activations in visual areas but had no effect on functional connectivity. In summary, the results confirm and extend previous knowledge regarding the neural mechanisms underlying SPEM and provide a valuable basis for further investigations such as in patients with SPEM impairments and known alterations in brain connectivity.NEW & NOTEWORTHY This study provides a comprehensive investigation of blood oxygen level-dependent (BOLD) functional connectivity during smooth pursuit eye movements. Results from a large sample of healthy participants suggest that key oculomotor regions interact closely with each other but also with regions not primarily associated with eye movements. Understanding functional connectivity during smooth pursuit is important, given its potential role as an endophenotype of psychoses.

Smooth pursuit eye movement deficits as a biomarker for psychotic features in bipolar disorder-Findings from the PARDIP study.

OBJECTIVES: Smooth pursuit eye movement deficits are an established psychosis biomarker across schizophrenia, schizoaffective and psychotic bipolar disorder (BPwP). Whether smooth pursuit deficits are also seen in bipolar disorder without psychosis (BPwoP) is unclear. Here we present data from the Psychosis and Affective Research Domains and Intermediate Phenotypes (PARDIP) study comparing bipolar patients with and without psychotic features. METHODS: Probands with BPwP (N = 49) and BPwoP (N = 36), and healthy controls (HC, N = 71) performed eye tracking tasks designed to evaluate specific sensorimotor components relevant for pursuit initiation and pursuit maintenance. RESULTS: While BPwoP did not differ from either BPwP or HC on initial eye acceleration, they performed significantly better than BPwP on early (P < .01) and predictive (P = .02) pursuit maintenance measures, both without differing from HC. BPwP were impaired compared to HC on initial eye acceleration, and on early and predictive pursuit maintenance (all P < .01). In contrast to the three pursuit measures, BPwP and BPwoP were both impaired on general neurocognitive assessments in relation to HC (both P < .001), without a significant difference between the two bipolar patient groups. CONCLUSIONS: Our findings support the model that impairments of sensorimotor and cognitive processing as required for early and later predictive smooth pursuit maintenance are relatively specific to those bipolar patients with a history of psychosis. This suggests that the neural circuitry for developing feed-forward predictive models for accurate pursuit maintenance is associated with the occurrence of psychotic features in bipolar patients. In contrast, generalized neuropsychological impairments did not differentiate the two bipolar patient groups.