Neural mechanisms underlying the temporal control of sequential saccade planning in the frontal eye field.

Sequences of saccadic eye movements are instrumental in navigating our visual environment. While neural activity has been shown to ramp up to a threshold before single saccades, the neural underpinnings of multiple saccades is unknown. To understand the neural control of saccade sequences, we recorded from the frontal eye field (FEF) of macaque monkeys while they performed a sequential saccade task. We show that the concurrent planning of two saccade plans brings forth processing bottlenecks, specifically by decreasing the growth rate and increasing the threshold of saccade-related ramping activity. The rate disruption affected both saccade plans, and a computational model, wherein activity related to the two saccade plans mutually and asymmetrically inhibited each other, predicted the behavioral and neural results observed experimentally. Borrowing from models in psychology, our results demonstrate a capacity-sharing mechanism of processing bottlenecks, wherein multiple saccade plans in a sequence compete for the processing capacity by the perturbation of the saccade-related ramping activity. Finally, we show that, in contrast to movement-related neurons, visual activity in FEF neurons is not affected by the presence of multiple saccade targets, indicating that, for perceptually simple tasks, inhibition within movement-related neurons mainly instantiates capacity sharing. Taken together, we show how psychology-inspired models of capacity sharing can be mapped onto neural responses to understand the control of rapid saccade sequences.

TURead: An eye movement dataset of Turkish reading.

In this study, we present TURead, an eye movement dataset of silent and oral sentence reading in Turkish, an agglutinative language with a shallow orthography understudied in reading research. TURead provides empirical data to investigate the relationship between morphology and oculomotor control. We employ a target-word approach in which target words are manipulated by word length and by the addition of two commonly used suffixes in Turkish. The dataset contains well-established eye movement variables; prelexical characteristics such as vowel harmony and bigram-trigram frequencies and word features, such as word length, predictability, frequency, eye voice span measures, Cloze test scores of the root word and suffix predictabilities, as well as the scores obtained from two working memory tests. Our findings on fixation parameters and word characteristics are in line with the patterns reported in the relevant literature.

More (corrective) consecutive saccades after a lesion to the posterior parietal cortex.

To reach a target, primary saccades (S1s) are often followed by (corrective) consecutive saccades (S2, and potentially S3, S4, S5), which are based on retinal and extraretinal feedback. Processing these extraretinal signals was found to be significantly impaired by lesions to the posterior parietal cortex (PPC). Recent studies, however, added a more nuanced view to the role of the PPC, where patients with PPC lesions still used extraretinal signals for S2s and perceptual judgements (Fabius et al., 2020; Rath-Wilson & Guitton, 2015). Hence, it seems that a PPC lesion is not disrupting extraretinal processing per se. Yet, a lesion might still result in less reliable processing of extraretinal signals. Here, we investigated whether this lower reliability manifests as decreased or delayed S2 initiation. Patients with PPC lesions (n = 7) and controls (n = 26) performed a prosaccade task where the target either remained visible or was removed after S1 onset. When S1 is removed, accurate S2s (corrections of S1 error) rely solely on extraretinal signals. We analysed S2 quantity and timing using linear mixed-effects modelling and additive hazards analyses. Patients demonstrated slower S1 execution and lower S1 amplitudes than controls, but their S2s still compensated the S1 undershoot, also when they only relied on extraretinal information. Surprisingly, patients showed an increased amount of S2s. This deviation from control behaviour can be seen as suboptimal, but given the decreased accuracy of the primary saccade, it could be optimal for patients to employ more (corrective) consecutive saccades to overcome this inaccuracy.

The anatomical myofascial continuum between the neck and eyes.

The posterior myofascial chain (PMC) or superficial back line encompasses a series of muscles interlinked by the deep fascia, extending from the foot to the fascial sheath of the eyeball. The deep cervical fascia of the neck, the epicranial aponeurosis of the head, and the fascial sheath of eyeball, form the proximal PMC. Although the literature has reported an anatomical myofascial continuum between the neck, head, and eyes, the anatomical descriptions vary substantially. Moreover, there is still no plausible functional interrelationship between the proximal structural myofascial links. Chronic neck pain is usually associated with a plethora of symptoms including craniofacial pain and oculomotor disorders. Understanding the anatomy of the proximal myofascial chain could help clinicians improvise treatment strategies for managing such painful head and neck disorders.

Great-tailed grackles can independently direct their eyes toward different targets.

Many species use eye movements to direct their overt attention toward specific targets within their environments. Some species can move each eye independently but we have a limited understanding of whether they can simultaneously monitor different targets with each eye. This study, therefore, tested whether a songbird can independently move its eyes towards two different targets. Captive great-tailed grackles (Quiscalus mexicanus) were simultaneously presented with one target in their left visual field and another target in their right visual field; the targets were both in the upper visual fields, both in the lower visual fields, or one target was in the upper visual field of one eye, while the other target was in the lower visual field of the other eye. The grackles correctly directed their left and right eyes toward the targets regardless of where the targets appeared at levels greater than chance. These results demonstrate that an avian species can perform simultaneous eye movements towards two different targets.

Undersweep fixations during reading in adults and children.

Return sweeps take a reader's fixation from the end of one line to the start of the next. Return sweeps frequently undershoot their target and are followed by a corrective saccade toward the left margin. The pauses prior to corrective saccades are typically considered to be uninvolved in linguistic processing. However, recent findings indicate that these undersweep fixations influence skilled adult readers' subsequent reading pass across the line and provide preview of line-initial words. The current research examined these effects in children. First, a children's reading corpus analysis revealed that words receiving an undersweep fixation were more likely skipped and received shorter gaze durations during a subsequent pass. Second, a novel eye movement experiment that directly compared adults' and children's eye movements indicated that, during an undersweep fixation, readers very briefly allocate their attention to the fixated word-as indicated by inhibition of return effects during a subsequent pass-prior to deploying attention toward the line-initial word. We argue that prior to the redeployment of attention, readers extract information at the point of fixation that facilitates later encoding and saccade targeting. Given similar patterns of results for adults and children, we conclude that the mechanisms controlling for oculomotor coordination and attention necessary for reading across line boundaries are established from a very early point in reading development.

Oculomotor deficits in children adopted from Eastern Europe.

AIM: We aim to assess oculomotor behaviour in children adopted from Eastern Europe, who are at high risk of maternal alcohol consumption. METHODS: This cross-sectional study included 29 adoptees and 29 age-matched controls. All of them underwent a complete ophthalmological examination. Oculomotor control, including fixation and saccadic performance, was assessed using a DIVE device, with eye tracking technology. Anthropometric and facial measurements were obtained from all the adopted children, to identify features of foetal alcohol spectrum disorders (FASD). Fixational and saccadic outcomes were compared between groups, and the effect of adoption and FASD features quantified. RESULTS: Oculomotor performance was poorer in adopted children. They presented shorter (0.53 vs 1.43 milliseconds in the long task and 0.43 vs 0.82 in the short task) and more unstable fixations (with a bivariate contour ellipse area of 27.9 vs 11.6 degree2 during the long task and 6.9 vs 1.3 degree2 during the short task) and slower saccadic reactions (278 vs 197 milliseconds). Children with sentinel finding for FASD showed the worst oculomotor outcomes. CONCLUSION: Children adopted from Eastern Europe present oculomotor deficits, affecting both fixation and saccadic skills. We highlight prenatal exposure to alcohol as the main cause for these deficits.

Differential Contribution of Low- and High-level Image Content to Eye Movements in Monkeys and Humans.

Oculomotor selection exerts a fundamental impact on our experience of the environment. To better understand the underlying principles, researchers typically rely on behavioral data from humans, and electrophysiological recordings in macaque monkeys. This approach rests on the assumption that the same selection processes are at play in both species. To test this assumption, we compared the viewing behavior of 106 humans and 11 macaques in an unconstrained free-viewing task. Our data-driven clustering analyses revealed distinct human and macaque clusters, indicating species-specific selection strategies. Yet, cross-species predictions were found to be above chance, indicating some level of shared behavior. Analyses relying on computational models of visual saliency indicate that such cross-species commonalities in free viewing are largely due to similar low-level selection mechanisms, with only a small contribution by shared higher level selection mechanisms and with consistent viewing behavior of monkeys being a subset of the consistent viewing behavior of humans.

The role of dentate nuclei in human oculomotor control: insights from cerebrotendinous xanthomatosis.

KEY POINTS: A cerebellar dentate nuclei (DN) contribution to volitional oculomotor control has recently been hypothesized but not fully understood. Cerebrotendinous xanthomatosis (CTX) is a rare neurometabolic disease typically characterized by DN damage. In this study, we compared the ocular movement characteristics of two sets of CTX patients, with and without brain MRI evidence of DN involvement, with a set of healthy subjects. Our results suggest that DN participate in voluntary behaviour, such as the execution of antisaccades, and moreover are involved in controlling the precision of the ocular movement. The saccadic abnormalities related to DN involvement were independent of global and regional brain atrophy. Our study confirms the relevant role of DN in voluntary aspects of oculomotion and delineates specific saccadic abnormalities that could be used to detect the involvement of DN in other cerebellar disorders. ABSTRACT: It is well known that the medial cerebellum controls saccadic speed and accuracy. In contrast, the role of the lateral cerebellum (cerebellar hemispheres and dentate nuclei, DN) is less well understood. Cerebrotendinous xanthomatosis (CTX) is a lipid storage disorder due to mutations in CYP27A1, typically characterized by DN damage. CTX thus provides a unique opportunity to study DN in human oculomotor control. We analysed horizontal and vertical visually guided saccades and horizontal antisaccades of 19 CTX patients. Results were related to the presence/absence of DN involvement and compared with those of healthy subjects. To evaluate the contribution of other areas, abnormal saccadic parameters were compared with global and regional brain volumes. CTX patients executed normally accurate saccades with normal main sequence relationships, indicating that the brainstem and medial cerebellar structures were functionally spared. Patients with CTX executed more frequent multistep saccades and directional errors during the antisaccade task than controls. CTX patients with DN damage showed less precise saccades with longer latencies, and more frequent directional errors, usually not followed by corrections, than either controls or patients without DN involvement. These saccadic abnormalities related to DN involvement but were independent of global and regional brain atrophy. We hypothesize that two different cerebellar networks contribute to the metrics of a movement: the medial cerebellar structures determine accuracy, whereas the lateral cerebellar structures control precision. The lateral cerebellum (hemispheres and DN) also participates in modulating goal directed gaze behaviour, by prioritizing volitional over reflexive movements.

A temporal dependency account of attentional inhibition in oculomotor control.

We used concurrent electroencephalogram (EEG) and eye tracking to investigate the role of covert attentional mechanisms in the control of oculomotor behavior. Human participants made speeded saccades to targets that were presented alongside salient distractors. By subsequently sorting trials based on whether the distractor was strongly represented or suppressed by the visual system - as evident in the accuracy (Exp. 1) or quality of the saccade (Exp. 2) - we could characterize and contrast pre-saccadic neural activity as a function of whether oculomotor control was established. Results show that saccadic behavior is strongly linked to the operation of attentional mechanisms in visual cortex. In Experiment 1, accurate saccades were preceded by attentional selection of the target - indexed by a target-elicited N2pc component - and by attentional suppression of the distractor - indexed by early and late distractor-elicited distractor positivity (Pd) components. In Experiment 2, the strength of distractor suppression predicted the degree to which the path of slower saccades would deviate away from the distractor en route to the target. However, results also demonstrated clear dissociations of covert and overt selective control, with saccadic latency in particular showing no relationship to the latency of covert selective mechanisms. Eye movements could thus be initiated prior to the onset of attentional ERP components, resulting in stimulus-driven behaviour. Taken together, the results indicate that attentional mechanisms play a role in determining saccadic behavior, but that saccade timing is not contingent on the deployment of attention. This creates a temporal dependency, whereby attention fosters oculomotor control only when attentional mechanisms are given sufficient opportunity to impact stimuli representations before an eye movement is executed.

Head Movements During Visual Orienting Toward Moving Prey in the Lizard Takydromus tachydromoides.

It is important to investigate visual orienting in reptiles to better understand the basic organization of the oculomotor system in vertebrates. However, quantitative analyses of visual orienting behavior in reptiles have rarely been conducted, except in chameleons. In the present study, we videorecorded the head and body movements of the lizard Takydromus tachydromoides during visual tracking of moving prey and analyzed them frame-by-frame. Before approaching prey, visual tracking mainly consisted of brief intermittent turns of the head (saccade). After the head saccades, the angular position of the prey relative to the lizard head was kept at 10-70° (laterally) in most cases, rather than at 0° (in front). In addition, the ratio of the amplitude of the head saccades to prey position was 0.2-0.3, which is much smaller than 1, suggesting that the head did not orient exactly toward the prey after most saccades. These results were observed under both white (homogeneous) and grating (structured) backgrounds. Possible functions of head saccades in the lizard are discussed.

The impending demise of the item in visual search.

The way the cognitive system scans the visual environment for relevant information - visual search in short - has been a long-standing central topic in vision science. From its inception as a research topic, and despite a number of promising alternative perspectives, the study of visual search has been governed by the assumption that a search proceeds on the basis of individual items (whether processed in parallel or not). This has led to the additional assumptions that shallow search slopes (at most a few tens of milliseconds per item for target-present trials) are most informative about the underlying process, and that eye movements are an epiphenomenon that can be safely ignored. We argue that the evidence now overwhelmingly favours an approach that takes fixations, not individual items, as its central unit. Within fixations, items are processed in parallel, and the functional field of view determines how many fixations are needed. In this type of theoretical framework, there is a direct connection between target discrimination difficulty, fixations, and reaction time (RT) measures. It therefore promises a more fundamental understanding of visual search by offering a unified account of both eye movement and manual response behaviour across the entire range of observed search efficiency, and provides new directions for research. A high-level conceptual simulation with just one free and four fixed parameters shows the viability of this approach.

Adaptation of Saccades and Perceived Size after Trans-Saccadic Changes of Object Size.

When saccadic eye movements consistently fail to land on the intended target, saccade accuracy is maintained by gradually adapting the amplitude of successive saccades to the same target. Such saccadic adaptation is usually induced by systematically displacing a small visual target during the execution of the saccade. However, saccades are normally performed to extended objects. Here we report changes in saccade amplitude when the size of a target object is systematically changed during a saccade. Moreover, we find that this manipulation also affected the visual perception of the size of that object. Human subjects were tested in shortening and lengthening adaptation where they had to make saccades to targets of different sizes, which were each shortened or lengthened during saccade execution, respectively. In both experiments, a preadaptation and postadaptation phase required manually indicating the horizontal size of each target by grip aperture and, in a further experiment, a verbal size report. We evaluated the effect of change in visual perception on saccade and on the two modalities of judgment. We observed that (1) saccadic adaptation can be induced by modifying target object size and (2) this gradual change in saccade amplitude in the direction of the object size change evokes a concomitant change in perceived object size. These findings suggest that size is a relevant signal for saccadic system and its trans-saccadic manipulation entails considerable changes at multiple levels of sensorimotor performance.

Dynamic causal modelling of eye movements during pursuit: Confirming precision-encoding in V1 using MEG.

This paper shows that it is possible to estimate the subjective precision (inverse variance) of Bayesian beliefs during oculomotor pursuit. Subjects viewed a sinusoidal target, with or without random fluctuations in its motion. Eye trajectories and magnetoencephalographic (MEG) data were recorded concurrently. The target was periodically occluded, such that its reappearance caused a visual evoked response field (ERF). Dynamic causal modelling (DCM) was used to fit models of eye trajectories and the ERFs. The DCM for pursuit was based on predictive coding and active inference, and predicts subjects' eye movements based on their (subjective) Bayesian beliefs about target (and eye) motion. The precisions of these hierarchical beliefs can be inferred from behavioural (pursuit) data. The DCM for MEG data used an established biophysical model of neuronal activity that includes parameters for the gain of superficial pyramidal cells, which is thought to encode precision at the neuronal level. Previous studies (using DCM of pursuit data) suggest that noisy target motion increases subjective precision at the sensory level: i.e., subjects attend more to the target's sensory attributes. We compared (noisy motion-induced) changes in the synaptic gain based on the modelling of MEG data to changes in subjective precision estimated using the pursuit data. We demonstrate that imprecise target motion increases the gain of superficial pyramidal cells in V1 (across subjects). Furthermore, increases in sensory precision - inferred by our behavioural DCM - correlate with the increase in gain in V1, across subjects. This is a step towards a fully integrated model of brain computations, cortical responses and behaviour that may provide a useful clinical tool in conditions like schizophrenia.

Effects of reward on oculomotor control.

The present study examines the extent to which distractors that signal the availability of monetary reward on a given trial affect eye movements. We used a novel eye movement task in which observers had to follow a target around the screen while ignoring distractors presented at varying locations. We examined the effects of reward magnitude and distractor location on a host of oculomotor properties, including saccade latency, amplitude, landing position, curvature, and erroneous saccades toward the distractor. We found consistent effects of reward magnitude on classic oculomotor phenomena such as the remote distractor effect, the global effect, and oculomotor capture by the distractor. We also show that a distractor in the visual hemifield opposite to the target had a larger effect on oculomotor control than an equidistant distractor in the same hemifield as the target. Bayesian hierarchical drift diffusion modeling revealed large differences in drift rate depending on the reward value, location, and visual hemifield of the distractor stimulus. Our findings suggest that high reward distractors not only capture the eyes but also affect a multitude of oculomotor properties associated with oculomotor inhibition and control.

Eye-Movement Control in RAN and Reading.

The present study examined the visual scanning hypothesis, which suggests that fluent oculomotor control is an important component underlying the predictive relationship between Rapid Automatized Naming (RAN) tasks and reading ability. Our approach was to isolate components of saccadic planning, articulation, and lexical retrieval in three modified RAN tasks. We analyzed two samples of undergraduate readers (age 17-27), we evaluated the incremental contributions of these components and found that saccadic planning to non-linguistic stimuli alone explained roughly one-third of the variance that conventional RAN tasks explained in eye-movements registered during text reading for comprehension. We conclude that the well-established predictive role of RAN for reading performance is in part due to the individual ability to coordinate rapid sequential eye-movements to visual non-linguistic stimuli.

Eye movements in chameleons are not truly independent - evidence from simultaneous monocular tracking of two targets.

Chameleons perform large-amplitude eye movements that are frequently referred to as independent, or disconjugate. When prey (an insect) is detected, the chameleon's eyes converge to view it binocularly and 'lock' in their sockets so that subsequent visual tracking is by head movements. However, the extent of the eyes' independence is unclear. For example, can a chameleon visually track two small targets simultaneously and monocularly, i.e. one with each eye? This is of special interest because eye movements in ectotherms and birds are frequently independent, with optic nerves that are fully decussated and intertectal connections that are not as developed as in mammals. Here, we demonstrate that chameleons presented with two small targets moving in opposite directions can perform simultaneous, smooth, monocular, visual tracking. To our knowledge, this is the first demonstration of such a capacity. The fine patterns of the eye movements in monocular tracking were composed of alternating, longer, 'smooth' phases and abrupt 'step' events, similar to smooth pursuits and saccades. Monocular tracking differed significantly from binocular tracking with respect to both 'smooth' phases and 'step' events. We suggest that in chameleons, eye movements are not simply 'independent'. Rather, at the gross level, eye movements are (i) disconjugate during scanning, (ii) conjugate during binocular tracking and (iii) disconjugate, but coordinated, during monocular tracking. At the fine level, eye movements are disconjugate in all cases. These results support the view that in vertebrates, basic monocular control is under a higher level of regulation that dictates the eyes' level of coordination according to context.

Elevated Smooth Pursuit Gain in Collegiate Athletes with Sport-related Concussion Immediately Following Injury.

Purpose: Although there is evidence that sport-related concussion (SRC) affects oculomotor function and perceptual ability, experiments are often poorly controlled and are not replicable. This study aims to test the hypothesis that there are decreased values when assessing oculomotor impairment indicating poorer performance in SRC patients. Methods: Fifteen DI athletes presenting with SRC (7 females, 8 males) and 15 student volunteers (CON) (12 females, 3 males) completed a dynamic visual acuity (DVA) task that involved answering the direction of a moving stimulus (Landolt C) while wearing a head-mounted binocular eye tracker. There were 120 trials total with 60 trials presenting at 30º per second and 60 presenting at 90º per second. Various eye movement measurements, including horizontal smooth pursuit eye movements (SPEM) gain and saccadic peak velocity, were analyzed between groups using univariate ANOVAs. Saccade count in SPEM trials, accuracy, and vision were analyzed using Kruskal-Wallis tests. Results: There was no statistical difference in saccadic peak velocity: SRC = 414.7 ± 42º/s, CON = 406.6 ± 40.6º/s. A significant difference was found between SRC patients and healthy controls in horizontal SPEM gain (SRC = 0.9 ± 0.04, CON = 0.86 ± 0.03, F(1,28) = 7.243, P = 0.012) indicating that patients demonstrated compensatory eye movements when tracking the target. There were significantly more saccades in all SPEM trials (P = 0.001). Conclusion: SRCoculomotor deficits manifest as elevated horizontal SPEM gain when assessed within 48 hours of injury and compared to healthy controls within the same age range. SRC demonstrates altered oculomotor ability. While accurate in tracking a stimulus, SRC patients may conduct less controlled eye movements.

Eye did this! Sense of agency in eye movements.

This study investigates the sense of agency (SoA) for saccades with implicit and explicit agency measures. In two eye tracking experiments, participants moved their eyes towards on-screen stimuli that subsequently changed color. Participants then either reproduced the temporal interval between saccade and color-change (Experiment 1) or reported the time points of these events with an auditory Libet clock (Experiment 2) to measure temporal binding effects as implicit indices of SoA. Participants were either made to believe to exert control over the color change or not (agency manipulation). Explicit ratings indicated that the manipulation of causal beliefs and hence agency was successful. However, temporal binding was only evident for caused effects, and only when a sufficiently sensitive procedure was used (auditory Libet clock). This suggests a feebler connection between temporal binding and SoA than previously proposed. The results also provide evidence for a relatively fast acquisition of sense of agency for previously never experienced types of action-effect associations. This indicates that the underlying processes of action control may be rooted in more intricate and adaptable cognitive models than previously thought. Oculomotor SoA as addressed in the present study presumably represents an important cognitive foundation of gaze-based social interaction (social sense of agency) or gaze-based human-machine interaction scenarios. PUBLIC SIGNIFICANCE STATEMENT: In this study, sense of agency for eye movements in the non-social domain is investigated in detail, using both explicit and implicit measures. Therefore, it offers novel and specific insights into comprehending sense of agency concerning effects induced by eye movements, as well as broader insights into agency pertaining to entirely newly acquired types of action-effect associations. Oculomotor sense of agency presumably represents an important cognitive foundation of gaze-based social interaction (social agency) or gaze-based human-machine interaction scenarios. Due to peculiarities of the oculomotor domain such as the varying degree of volitional control, eye movements could provide new information regarding more general theories of sense of agency in future research.

Saccadic re-referencing training with gaze-contingent FRL-'fixation': Effects of scotoma type and size adaptation.

Foveal vision loss makes the fovea as saccadic reference point maladaptive. Training programs have been proposed that shift the saccadic reference point from the fovea to an extrafoveal location, just outside the area of vision loss. We used a visual search task to train normal-sighted participants to fixate target items with a predetermined 'forced retinal location' (FRL) adjacent to a simulated central scotoma. We found that training was comparatively successful for scotomata that had either a sharp or blurry demarcation from the background. Completing the task with sharp-edged scotoma resulted in overall higher training gains. Training with blurry-edged scotoma, however, yielded overall better results when scotoma size was increased after training and participants needed to adapt to a more eccentric FRL, as may be necessary in patients with progressive degenerative eye diseases.