Gaze Control Research Articles

Estimating brainstem dysfunction with video Head-impulse test(vHIT) in idiopathic REM sleep behavior disorder(iRBD) patients (P6-13.006)

<h3>Objective:</h3> In this study, we aimed to differentiate the characteristics of video nystamnography, including vHIT, in iRBD patients from healthy controls, which in known as the prodrome of degenerative disease. <h3>Background:</h3> iRBD is known as the prodrome of alpha-synucleionopathies. Pons plays a pivotal role in the control of gaze. The VOR is a reflex stabilizing gaze during head movement. VOR gain in vHIT is calculate as the ratio of eye velocity to head velocity and reduced by VOR pathway disease. <h3>Design/Methods:</h3> Along 32 iRBD patients confirmed through overnight PSG, 16 patients with AHI of less than 15 were grouped in RBD group and 19 with AHI of 15 or higher as RBD with OSA group. 24 participants without sleep disturbance and underwent VNG were classified into normal group. The VOR gains as well as parameters of pursuit and saccade were measured. These results were compared by Kruskal-Wallis one-way analysis. <h3>Results:</h3> In the horizontal canal, the gain of normal group was 1.02 and the RBD group was 1.00 and the RBD with OSA group was 0.98 in right side, and it was measured as 0.98 in the normal, 0.85 in the RBD group, and 0.88 in the RBD with OSA group in left side. In the right anterior canal, values was 1.14 in the normal group, 1.02 in the RBD group, and 1.00 in the RBD with OSA group. In the left posterior canal, value was 1.10 for the normal group, 1.03 for the RBD group, and 0.97 for the RBD with OSA group. vHIT parameters were not different between RBD and RBD with OSA group. <h3>Conclusions:</h3> We found that VOR gains in iRBD patients were reduced compared to normal controls. AHI did not affect the VOR gains iRBD patients. This study suggests that VOR gains may be crucial determinants estimating brainstem dysfunction in iRBD patients. <b>Disclosure:</b> Dr. Kim has nothing to disclose. Dr. Joo has nothing to disclose. Prof. Joo has nothing to disclose. Hyujin Jo has nothing to disclose.

A frontoparietal network for volitional control of gaze following.

Gaze following is a major element of non-verbal communication and important for successful social interactions. Human gaze following is a fast and almost reflex-like behavior, yet, it can be volitionally controlled and suppressed to some extent if inappropriate or unnecessary, given the social context. In order to identify the neural basis of the cognitive control of gaze following, we carried out an event-related fMRI experiment, in which human subjects' eye movements were tracked while they were exposed to gaze cues in two distinct contexts: a baseline gaze following condition in which subjects were instructed to use gaze cues to shift their attention to a gazed-at spatial target and a control condition in which the subjects were required to ignore the gaze cue and instead to shift their attention to a distinct spatial target to be selected based on a color mapping rule, requiring the suppression of gaze following. We could identify a suppression-related BOLD response in a frontoparietal network comprising dorsolateral prefrontal cortex (dlPFC), orbitofrontal cortex (OFC), the anterior insula, precuneus and posterior parietal cortex (PPC). These findings suggest that over excitation of frontoparietal circuits in turn suppressing the gaze following patch might be a potential cause of gaze following deficits in clinical populations.

Altered Gaze Control During Emotional Face Exploration in Patients With Amyotrophic Lateral Sclerosis.

Up to 50% of patients with amyotrophic lateral sclerosis (ALS) present with cognitive problems and behavioral dysfunctions including recognition of human faces presenting different emotions. We investigated whether impaired processing of emotional faces is associated with abnormal scan paths during visual exploration. Cognitively unimpaired patients with ALS (n = 45) and matched healthy controls (n = 37) underwent neuropsychological assessment and video-based eye tracking. Eye movements were recorded while participants visually explored faces expressing different emotions (neutral, disgusted, happy, fearful, and sad) and houses mimicking faces. Compared with controls, patients with ALS fixated significantly longer to regions which are not relevant for emotional information when faces expressed fear (p = 0.007) and disgust (p = 0.006), whereas the eyes received less attention in faces expressing disgust (p = 0.041). Fixation duration in any area of interest was not significantly associated with the cognitive state or clinical symptoms of disease severity. In cognitively unimpaired patients with ALS, altered gaze patterns while visually exploring faces expressing different emotions might derive from impaired top-down attentional control with possible involvement of subliminal frontotemporal areas. This may account for indistinctness in emotion recognition reported in previous studies because nonsalient features retrieve more attention compared with salient areas. Current findings may indicate distinct emotion processing dysfunction of ALS pathology, which may be different from, for example, executive dysfunction.

Interhemispheric competition during sleep

Our understanding of the functions and mechanisms of sleep remains incomplete, reflecting their increasingly evident complexity1–3. Likewise, studies of interhemispheric coordination during sleep4–6 are often hard to connect precisely to known sleep circuits and mechanisms. Here, by recording from the claustra of sleeping bearded dragons (Pogona vitticeps), we show that, although the onsets and offsets of Pogona rapid-eye-movement (REMP) and slow-wave sleep are coordinated bilaterally, these two sleep states differ markedly in their inter-claustral coordination. During slow-wave sleep, the claustra produce sharp-wave ripples independently of one another, showing no coordination. By contrast, during REMP sleep, the potentials produced by the two claustra are precisely coordinated in amplitude and time. These signals, however, are not synchronous: one side leads the other by about 20 ms, with the leading side switching typically once per REMP episode or in between successive episodes. The leading claustrum expresses the stronger activity, suggesting bilateral competition. This competition does not occur directly between the two claustra or telencephalic hemispheres. Rather, it occurs in the midbrain and depends on the integrity of a GABAergic (γ-aminobutyric-acid-producing) nucleus of the isthmic complex, which exists in all vertebrates and is known in birds to underlie bottom-up attention and gaze control. These results reveal that a winner-take-all-type competition exists between the two sides of the brain of Pogona, which originates in the midbrain and has precise consequences for claustrum activity and coordination during REMP sleep.

Stimulation of non-motor subthalamic nucleus impairs selective response inhibition via prefrontal connectivity.

Given the inconsistent results in the past, there is an ongoing debate whether and how deep brain stimulation in the subthalamic nucleus modifies cognitive control processes like response inhibition in persons with Parkinson's disease. In this study, we examined how the location of the stimulation volume within the subthalamic nucleus affects the performance in an antisaccade task but also how its structural connectivity is related to response inhibition. Antisaccade error rates and latencies were collected in 14 participants on and off deep brain stimulation in a randomized order. Stimulation volumes were computed based on patient-specific lead localizations using preoperative MRI and postoperative CT scans. Structural connectivity of the stimulation volumes with pre-defined cortical oculomotor control regions as well as whole-brain connectivity was estimated using a normative connectome. We showed that the detrimental effect of deep brain stimulation on response inhibition, measured as antisaccade error rate, depended upon the magnitude of the intersection of volumes of activated tissue with the non-motor subregion of the subthalamic nucleus and on its structural connectivity with regions of the prefrontal oculomotor network including bilateral frontal eye fields and right anterior cingulate cortex. Our results corroborate previous recommendations for avoidance of stimulation in the ventromedial non-motor subregion of the subthalamic nucleus which connects to the prefrontal cortex to prevent stimulation-induced impulsivity. Furthermore, antisaccades were initiated faster with deep brain stimulation when the stimulation volume was connected to fibres passing the subthalamic nucleus laterally and projecting onto the prefrontal cortex, indicating that improvement of voluntary saccade generation with deep brain stimulation may be an off-target effect driven by stimulation of corticotectal fibres directly projecting from the frontal and supplementary eye fields onto brainstem gaze control areas. Taken together, these findings could help implement individualized circuit-based deep brain stimulation strategies that avoid impulsive side effects while improving voluntary oculomotor control.

Gaze Control for Active Visual SLAM via Panoramic Cost Map

This paper focuses on improving the positioning accuracy of the visual simultaneous localization and mapping (VSLAM) through actively controlling the gaze of the positioning camera mounted on an autonomous mobile robot. We present a gaze control method for the VSLAM with a novel panoramic cost map. In the method, we add a panoramic camera besides the positioning camera to aid the gaze control of the positioning camera. The panoramic camera is modeled as a unit sphere model and the positioning camera is modeled as a pinhole model that is concentric with the unit sphere model. The panoramic camera captures a panoramic image for the evaluation of an environment. The effective factors, such as feature points and moving objectives, of the VSLAM are detected in the panoramic image. When the pinhole model pointing at a specific orientation, a cost value can be calculated according to the effective factors. After calculating the above-mentioned cost in all available orientations of the pinhole model, a panoramic cost map that is determined by the individual costs can be established. Next, a target orientation is selected according to the panoramic cost map and the positioning camera is rotated to the target orientation by a pan-tilt. The test results in different scenery show that the proposed method can improve the positioning accuracy of the VSLAM compared to stationary orientation.

Modeling brain dynamics and gaze behavior: Starting point bias and drift rate relate to frontal midline theta oscillations

Frontal midline theta oscillatory dynamics have been implicated as an important neural signature of inhibitory control. However, most proactive cognitive control studies rely on behavioral tasks where individual differences are inferred through button presses. We applied computational modeling to further refine our understanding of theta dynamics in a cued anti-saccade task with gaze-contingent eye tracking. Using a drift diffusion model, increased frontal midline theta power during high-conflict, relative to low-conflict, trials predicted a more conservative style of responding through the starting point (bias). During both high- and low-conflict trials, increases in frontal midline theta also predicted improvements in response efficiency (drift rate). Regression analyses provided support for the importance of the starting point bias, which was associated with frontal midline theta over the course of the task above-and-beyond both drift rate and mean reaction time. Our findings provide a more thorough understanding of proactive gaze control by linking trial-by-trial increases of frontal midline theta to a shift in starting point bias facilitating a more neutral style of responding.

Serotonergic current responses of neurons in rat oculomotor neural integrators.

The prepositus hypoglossi nucleus (PHN) and the interstitial nucleus of Cajal (INC) are involved in controlling horizontal and vertical gaze, respectively. Previous studies have shown that PHN neurons exhibit depolarized or hyperpolarized responses to serotonin (5-hydroxytryptamine, 5-HT). However, serotonergic modulation of INC neurons has not been examined. Furthermore, the relationship between 5-HT-induced responses and neuron types based on neurotransmitter phenotypes has not been clarified. In this study, we investigated 5-HT-induced current responses in PHN and INC neurons and the distributions of distinct current responses in different neuron types, using whole cell recordings of wild-type and transgenic rat brain stem slices. Local application of 5-HT to the cell soma confirmed that slow inward (SI) and slow outward (SO) currents were mediated by 5-HT2 and 5-HT1A receptors, respectively. Furthermore, fast inward (FI) currents that were mediated by 5-HT3 receptors were observed. These three current responses were observed in both PHN and INC neurons. Analyses of the distributions of the three current responses revealed that fluorescently identified glutamatergic and inhibitory neurons in the PHN showed high proportions of SI and SO currents, respectively, whereas glutamatergic and inhibitory neurons in the INC showed mainly SO currents. When PHN and INC neurons were characterized on the basis of firing patterns, the proportions of the currents depended on the firing patterns. The different distributions of 5-HT-induced currents suggest distinct serotonergic modulation modes specific to horizontal and vertical gaze control.NEW & NOTEWORTHY Serotonergic modulation of vertical gaze control (interstitial nucleus of Cajal, INC) is less understood than that of horizontal gaze control (prepositus hypoglossal nucleus, PHN). Here, we report 5-HT-induced fast inward currents in addition to the previously reported slow inward and outward currents. The distributions of these currents in INC neurons based on neurotransmitter phenotypes differ from those in PHN neurons. These results suggest distinct serotonergic modulation modes in horizontal and vertical gaze control centers.

Evaluation of several gaze control methods for a board game with no time pressure

The present study aimed to evaluate six methods of gaze control of pieces in board games without time pressure designed for disabled users who cannot use a keyboard or mouse. Checkers was used as an example game in the experiment, however, the pieces could only be moved one square (i.e. there were no flying kings), but the same control methods with only minor modifications can be used in most board games. By experimenting, we determined that the control method with dwell-time equal to about 600-700ms was the more practical and worked better for users, while the gesture control worked poorly, and the control method involving directly the board was rated higher than the one based on using the buttons around the board.

Minified Augmented Reality as a Terrestrial Analog for G-Transitions Effects in Lunar and Interplanetary Spaceflight

Brief periods of extreme gravitational transition are anticipated during interplanetary spaceflight, including transitions between microgravity, hypogravity, and hypergravity. Rapid sensorimotor adaptation will occur following these G-transitions which may affect astronaut performance including gaze control and dynamic visual acuity. Significant decrements in dynamic visual acuity could lead to mission compromise or failure (e.g., impairing mission critical tasks or spacecraft maneuvering). It is crucial to provide astronauts with the training necessary to overcome these physiological barriers they are bound to encounter during spaceflight missions. Minifying lenses in augmented reality may serve as an easily applicable, low-cost, method to simulate vestibulo-ocular dysfunction that occurs during gravitational transitions. In this paper, we review the effects of G-transitions on the vestibulo-ocular system and report on the novel development of minified augmented reality as a potential simulator and training tool for future spaceflight. We also report the results from an early validation study with a mean decrease in DVA (0.370 LogMAR) with 80% minifying effect, as well as a mean increase of DVA post-minifying (0.030 LogMAR). These early results suggest that minified augmented reality may serve as an accessible terrestrial analog for G-transitions, thus having potential for pre-mission training, particularly for lunar and interplanetary spaceflight.

Drivers’ gaze patterns when resuming control with a head-up-display: Effects of automation level and time budget

The removal of drivers’ active engagement in driving tasks can lead to erratic gaze patterns in SAE Level 2 (L2) and Level 3 (L3) automation, which has been linked to their subsequential degraded take-over performance. To further address how changes in gaze patterns evolve during the take-over phase, and whether they are influenced by the take-over urgency and the location of the human-machine interface, this driving simulator study used a head-up display (HUD) to relay information about the automation status and conducted take-over driving experiments where the ego car was about to exit the highway with variations in the automation level (L2, L3) and time budget (2 s, 6 s). In L2 automation, drivers were required to monitor the environment, while in L3, they were engaged with a visual non-driving related task. Manual driving was also embodied in the experiments as the baseline. Results showed that, compared to manual driving, drivers in L2 automation focused more on the HUD and Far Road (roadway beyond 2 s time headway ahead), and less on the Near Road (roadway within 2 s time headway ahead); while in L3, drivers’ attention was predominantly allocated on the non-driving related task. After receiving take-over requests (TORs), there was a gradual diversion of attention from the Far Road to the Near Road in L2 take-overs. This trend changed nearly in proportion to the time within the time budget and it exaggerated given a shorter time budget of 2 s. While in L3, drivers’ gaze distribution was similar in the early stage of take-overs for both time budget conditions (2 s vs. 6 s), where they prioritized their early glances to Near Road with a gradual increase in attention towards Far Road. The HUD used in the present study showed the potential to maintain drivers’ attention around the road center during automation and to encourage drivers to glance the road earlier after TORs by reducing glances to the instrument cluster, which might be of significance to take-over safety. These findings were discussed based on an extended conceptual gaze control model, which advances our understanding of gaze patterns around control transitions and their underlying gaze control causations. Implications can be contributed to the design of autonomous vehicles to facilitate the transition of control by guiding drivers’ attention appropriately according to drivers’ attentional state and the take-over urgency.

The visual control of gaze, steering, and obstacle avoidance in experienced quadcopter pilots

The visual control of gaze, steering, and obstacle avoidance in experienced quadcopter pilots

Towards Developing a Data Management System for Individuals with Upper/Lower Extremities Dysfunctions

<h3>Research Objectives</h3> The data management system was designed to integrate an individual's profile to track their progress and receive the recommended advice from the expert. <h3>Design</h3> Experimental study. <h3>Setting</h3> In the Biorobotics Lab. <h3>Participants</h3> Ten healthy participants (Mean age 27.86 years old). <h3>Interventions</h3> An assistive robotic device performing 19 essential daily tasks was controlled by a participant in a power wheelchair using a finger and chin Joystick along with eye gaze control. After the study, the participants were asked to fill out a user satisfaction survey. <h3>Main Outcome Measures</h3> We assessed the data management system in three modes: (I) Store and visualize data, (II) Track the progress of the participants, and (III) Get recommendations from experts based on the data. <h3>Results</h3> The system was successfully utilized to store, monitor, and visualize the experimental data of everyday life activities while maintaining confidentiality and security. From the results, we can conclude that the data management system has successfully fulfilled its desired goal concerning the fact to monitor individuals with disability remotely and efficiently with their regular improvement. <h3>Conclusions</h3> The successful completion of the data management system ensured the overall quality of care. In our next step, we will test the feasibility and usability of the system with upper/lower extremities dysfunction. <h3>Author(s) Disclosures</h3> The authors have no conflict of interest to declare.

Eyes can draw: A high-fidelity free-eye drawing method with unimodal gaze control

EyeCompass is a novel free-eye drawing system enabling high-fidelity and efficient free-eye drawing through unimodal gaze control, addressing the bottlenecks of gaze-control drawing. EyeCompass helps people to draw using only their eyes, which is of value to people with motor disabilities. Currently, there is no effective gaze-control drawing application due to multiple challenges including involuntary eye movements, conflicts between visuomotor transformation and ocular observation, gaze trajectory control, and inherent eye-tracking errors. EyeCompass addresses this using two initial gaze-control drawing mechanisms: brush damping dynamics and the gaze-oriented method. The user experiments compare the existing gaze-control drawing method and EyeCompass, showing significant improvements in the drawing performance of the mechanisms concerned. The field study conducted with motor-disabled people produced various creative graphics and indicates good usability of the system. Our studies indicate that EyeCompass is a high-fidelity, accurate, feasible free-eye drawing method for creating artistic works via unimodal gaze control.

Portable High-Speed Optical Gaze Controller with Vision Chip

It is important to miniaturize robot systems while maintaining advantages such as high responsiveness and functionality for human-machine interactions and for achieving integration with other robotic systems such as drones. In this research, we focused on the miniaturization of a high-speed visual feedback system, and developed a “portable saccade mirror,” which is a system that can realize active target tracking using 1000 Hz image capturing, processing, and feedback actuation with only 3 ms latency in a handheld device. By using a three-dimensionally-stacked vision chip, the proposed system achieved high speed, low latency, low power consumption and compact size, and therefore, can be considered as a good example of a miniaturized high-speed visual feedback system. In this study, we evaluated the performance of the proposed system in comparison with the conventional optical gaze controller, and demonstrated some applications, such as tracking field scope and panorama target scanning.

ABC of Gaze and Ocular Oscillations.

The chief goal of all eye movements is to maintain the image of an object steady on the retina especially the macula to preserve visual acuity. Gaze palsy refers to lack of the conjugate movements due to a failure of supranuclear control mechanisms. Supranuclear control is maintained by not one, but multiple eye movement systems and gaze mechanisms. Supranuclear gaze palsies can be associated with a myriad of aetiologies- from trauma or metabolic abnormalities to stroke, demyelinating disorders and space occupying lesions like tumours. Culprit lesions may be in frontal motor centres, brainstem gaze centres gaze or interconnecting segments. While the brainstem network for horizontal gaze lies in pons, that for vertical gaze is situated in midbrain. Further, ocular oscillations and nystagmus are abnormal eye movements that disrupt a steady fixation of gaze. It is prudent to be aware of various gaze pathways and their anatomical corelates in order to establish a topographic relationship of clinical findings. A systematic clinical examination may provide deep insights on the patho-physiological mechanisms along with aiding in localizing the lesion accurately. This review deals with systematic clinical approach to various gaze control systems.

Mental Workload Artificial Intelligence Assessment of Pilots’ EEG Based on Multi-Dimensional Data Fusion and LSTM with Attention Mechanism Model

EEG has been proved to be an effective tool for researchers’ cognition and mental workload by detecting the changes of brain activity potential. The mental workload of pilots in aviation flight is closely related to the characteristics of flight tasks. The previous methods have problems such as lack of objectivity, low EEG analysis ability and lack of real-time analysis ability. In order to solve these problems, this paper proposes a multi-dimensional data fusion brain workload calculation method based on flight effect evaluation, which integrates vision, operational behavior and visual gaze, and classifies and analyzes them in combination with EEG data. This method evaluates the mental workload of pilots from three aspects: visual gaze behavior, control behavior and flight effect in the simulated flight experimental environment, and realizes a more objective mental workload analysis. Then, the synchronously collected EEG data are segmented and sampled to form a dataset, and an LSTM neural network model integrating attention mechanism is established, in which the attention mechanism is used to improve the feature processing ability of the network model for the classification of complex EEG data. After machine learning training, the final model can achieve 94% detection accuracy for 2-s EEG data, and has the ability of real-time analysis in the application environment. Compared with the previous similar LSTM model, the accuracy is improved by 6%, which also shows the effectiveness of the model.

Conserved subcortical processing in visuo-vestibular gaze control

Gaze stabilization compensates for movements of the head or external environment to minimize image blurring. Multisensory information stabilizes the scene on the retina via the vestibulo-ocular (VOR) and optokinetic (OKR) reflexes. While the organization of neuronal circuits underlying VOR is well-described across vertebrates, less is known about the contribution and evolution of the OKR and the basic structures allowing visuo-vestibular integration. To analyze these neuronal pathways underlying visuo-vestibular integration, we developed a setup using a lamprey eye-brain-labyrinth preparation, which allowed coordinating electrophysiological recordings, vestibular stimulation with a moving platform, and visual stimulation via screens. Lampreys exhibit robust visuo-vestibular integration, with optokinetic information processed in the pretectum that can be downregulated from tectum. Visual and vestibular inputs are integrated at several subcortical levels. Additionally, saccades are present in the form of nystagmus. Thus, all basic components of the visuo-vestibular control of gaze were present already at the dawn of vertebrate evolution.

Classics to Contemporary of Saccadic Dysmetria and Oscillations.

Clear vision requires accurate gaze shift from one object to the other and steadily maintaining it when eyes are at the target. The rapid gaze shifts are assured by the high-frequency burst in the brainstem neuronal firing, the mechanism relying on the tight cerebellar supervision. The cerebellar oversight is equally essential for maintaining gaze on the object of interest. The cerebellar significance on the motor control of gaze and the consequences of cerebellar illness are known for almost three quarters of the century - since David Cogan published the classic paper titled "Ocular Dysmetria, Flutter Like Oscillations of the Eyes, and Opsoclonus." In this classic series of cases, three disorders of gaze shifting and gaze holding were described in a number of etiologies, ultimately manifesting in a final common pathway involving the cerebellum. Since the 1950s, there had been substantial progress in contemporary neurology, experimental neuroscience literature has expanded, and computational models of ocular motor control have flourished in the field. In this short commentary, I will highlight Cogan's cerebellar classic in the context of contemporary research on motor control of saccades.

Oculomotor plant and neural dynamics suggest gaze control requires integration on distributed timescales.

A fundamental principle of biological motor control is that the neural commands driving movement must conform to the response properties of the motor plants they control. In the oculomotor system, characterizations of oculomotor plant dynamics traditionally supported models in which the plant responds to neural drive to extraocular muscles on exclusively short, subsecond timescales. These models predict that the stabilization of gaze during fixations between saccades requires neural drive that approximates eye position on longer timescales and is generated through the temporal integration of brief eye velocity-encoding signals that cause saccades. However, recent measurements of oculomotor plant behaviour have revealed responses on longer timescales. Furthermore, measurements of firing patterns in the oculomotor integrator have revealed a more complex encoding of eye movement dynamics. Yet, the link between these observations has remained unclear. Here we use measurements from the larval zebrafish to link dynamics in the oculomotor plant to dynamics in the neural integrator. The oculomotor plant in both anaesthetized and awake larval zebrafish was characterized by a broad distribution of response timescales, including those much longer than 1s. Analysis of the firing patterns of oculomotor integrator neurons, which exhibited a broadly distributed range of decay time constants, demonstrates the sufficiency of this activity for stabilizing gaze given an oculomotor plant with distributed response timescales. This work suggests that leaky integration on multiple, distributed timescales by the oculomotor integrator reflects an inverse model for generating oculomotor commands, and that multi-timescale dynamics may be a general feature of motor circuitry. KEY POINTS: Recent observations of oculomotor plant response properties and neural activity across the oculomotor system have called into question classical formulations of both the oculomotor plant and the oculomotor integrator. Here we use measurements from new and published experiments in the larval zebrafish together with modelling to reconcile recent oculomotor plant observations with oculomotor integrator function. We developed computational techniques to characterize oculomotor plant responses over several seconds in awake animals, demonstrating that long timescale responses seen in anaesthetized animals extend to the awake state. Analysis of firing patterns of oculomotor integrator neurons demonstrates the sufficiency of this activity for stabilizing gaze given an oculomotor plant with multiple, distributed response timescales. Our results support a formulation of gaze stabilization by the oculomotor system in which commands for stabilizing gaze are generated through integration on multiple, distributed timescales.