Gaze Control Research Articles

A kinematic model for 3-D head-free gaze-shifts.

Rotations of the line of sight are mainly implemented by coordinated motion of the eyes and head. Here, we propose a model for the kinematics of three-dimensional (3-D) head-unrestrained gaze-shifts. The model was designed to account for major principles in the known behavior, such as gaze accuracy, spatiotemporal coordination of saccades with vestibulo-ocular reflex (VOR), relative eye and head contributions, the non-commutativity of rotations, and Listing's and Fick constraints for the eyes and head, respectively. The internal design of the model was inspired by known and hypothesized elements of gaze control physiology. Inputs included retinocentric location of the visual target and internal representations of initial 3-D eye and head orientation, whereas outputs were 3-D displacements of eye relative to the head and head relative to shoulder. Internal transformations decomposed the 2-D gaze command into 3-D eye and head commands with the use of three coordinated circuits: (1) a saccade generator, (2) a head rotation generator, (3) a VOR predictor. Simulations illustrate that the model can implement: (1) the correct 3-D reference frame transformations to generate accurate gaze shifts (despite variability in other parameters), (2) the experimentally verified constraints on static eye and head orientations during fixation, and (3) the experimentally observed 3-D trajectories of eye and head motion during gaze-shifts. We then use this model to simulate how 2-D eye-head coordination strategies interact with 3-D constraints to influence 3-D orientations of the eye-in-space, and the implications of this for spatial vision.

Saccadic movement deficiencies in adults with ADHD tendencies.

The goal of the present study was to explore deficits in gaze detection and emotional value judgment during a saccadic eye movement task in adults with attention deficit/hyperactivity disorder (ADHD) tendencies. Thirty-two participants, consisting of 16 ADHD tendencies and 16 controls, were recruited from a pool of 243 university students. Among the many problems in adults with ADHDs, our research focused on the deficits in the processing of nonverbal cues, such as gaze direction and the emotional value of others' faces. In Experiment 1, a cue display containing a face with emotional value and gaze direction was followed by a target display containing two faces located on the left and right side of the display. The participant's task was to make an anti-saccade opposite to the gaze direction if the cue face was not emotionally neutral. ADHD tendencies showed more overall errors than controls in making anti-saccades. Based on the hypothesis that the exposure duration of the cue display in Experiment 1 may have been too long, we presented the cue and target display simultaneously to prevent participants from preparing saccades in advance. Participants in Experiment 2 were asked to make either a pro-saccade or an anti-saccade depending on the emotional value of the central cue face. Interestingly, significant group differences were observed for errors of omission and commission. In addition, a significant three-way interaction among groups, cue emotion, and target gaze direction suggests that the emotional recognition and gaze control systems might somehow be interconnected. The result also shows that ADHDs are more easily distracted by a task-irrelevant gaze direction. Taken together, these results suggest that tasks requiring both response inhibition (anti-saccade) and gaze-emotion recognition might be useful in developing a diagnostic test for discriminating adults with ADHDs from healthy adults.

Direct projections from the dorsal premotor cortex to the superior colliculus in the macaque (macaca mulatta).

The dorsal premotor cortex (PMd) is part of the cortical network for arm movements during reach-related behavior. Here we investigate the neuronal projections from the PMd to the midbrain superior colliculus (SC), which also contains reach-related neurons, to investigate how the SC integrates into a cortico-subcortical network responsible for initiation and modulation of goal-directed arm movements. By using anterograde transport of neuronal tracers, we found that the PMd projects most strongly to the deep layers of the lateral part of the SC and the underlying reticular formation corresponding to locations where reach-related neurons have been recorded, and from where descending tectofugal projections arise. A somewhat weaker projection targets the intermediate layers of the SC. By contrast, terminals originating from prearcuate area 8 mainly project to the intermediate layers of the SC. Thus, this projection pattern strengthens the view that different compartments in the SC are involved in the control of gaze and in the control or modulation of reaching movements. The PMD-SC projection assists in the participation of the SC in the skeletomotor system and provides the PMd with a parallel path to elicit forelimb movements.

Effects of training and motivation on auditory P300 brain–computer interface performance

ObjectivesBrain–computer interface (BCI) technology aims at helping end-users with severe motor paralysis to communicate with their environment without using the natural output pathways of the brain. For end-users in complete paralysis, loss of gaze control may necessitate non-visual BCI systems. The present study investigated the effect of training on performance with an auditory P300 multi-class speller paradigm. For half of the participants, spatial cues were added to the auditory stimuli to see whether performance can be further optimized. The influence of motivation, mood and workload on performance and P300 component was also examined. MethodsIn five sessions, 16 healthy participants were instructed to spell several words by attending to animal sounds representing the rows and columns of a 5×5 letter matrix. Results81% of the participants achieved an average online accuracy of ⩾70%. From the first to the fifth session information transfer rates increased from 3.72bits/min to 5.63bits/min. Motivation significantly influenced P300 amplitude and online ITR. No significant facilitative effect of spatial cues on performance was observed. ConclusionsTraining improves performance in an auditory BCI paradigm. Motivation influences performance and P300 amplitude. SignificanceThe described auditory BCI system may help end-users to communicate independently of gaze control with their environment.

Fast gaze reorientations by combined movements of the eye, head, trunk and lower extremities.

Large reorientations of the line of sight, involving combined rotations of the eyes, head, trunk and lower extremities, are executed either as fast single-step or as slow multiple-step gaze transfers. In order to obtain more insight into the mechanisms of gaze and multisegmental movement control, we have investigated time-optimal gaze shifts (i.e. with the instruction to move as fast as possible) during voluntary whole-body rotations to remembered targets up to 180° eccentricity performed by standing healthy humans in darkness. Fast, accurate, single-step movement patterns occurred in approximately 70 % of trials, i.e. considerably more frequently than in previous studies with the instruction to turn at freely chosen speed (30 %). Head-in-space velocity in these cases was significantly higher than during multiple-step transfers and displayed a conspicuously regular bell-shaped profile, increasing smoothly to a peak and then decreasing slowly until realignment with the target. Head-in-space acceleration was on average not different during reorientations to the different target eccentricities. In contrast, head-in-space velocity increased with target eccentricity due to the longer duration of the acceleration phase implemented during trials to more distant targets. Eye saccade amplitude approached the eye-in-orbit mechanical limit and was unrelated to eye/head velocity, duration or target eccentricity. Overall, the combined movement was stereotyped such that the first two principal components accounted for data variance almost up to gaze shift end, suggesting that the three mechanical degrees of freedom under consideration (eye-in-orbit, head-on-trunk and trunk-in-space) are on average reduced to two kinematic degrees of freedom (i.e. eye, head-in-space). Synchronous EMG activity in the anterior tibial and gastrocnemius muscles preceded the onset of eye rotation. Since the magnitude and timing of peak head-in-space velocity were scaled with target eccentricity and because head-on-trunk and trunk-in-space displacements were on average linearly correlated, we propose a separate controller for head-in-space movement, whereas the movement of the eye-in-space may be, in contrast, governed by global, i.e. gaze feedback. The rapid progression of the line of sight can be sustained, and the reactivation of the vestibulo-ocular reflex would be postponed, until gaze error approaches zero only in association with a strong head-in-space neural control signal.

Usability and Workload of Access Technology for People With Severe Motor Impairment

Background. Eye trackers are widely used among people with amyotrophic lateral sclerosis, and their benefits to quality of life have been previously shown. On the contrary, Brain-computer interfaces (BCIs) are still quite a novel technology, which also serves as an access technology for people with severe motor impairment. Objective. To compare a visual P300-based BCI and an eye tracker in terms of information transfer rate (ITR), usability, and cognitive workload in users with motor impairments. Methods. Each participant performed 3 spelling tasks, over 4 total sessions, using an Internet browser, which was controlled by a spelling interface that was suitable for use with either the BCI or the eye tracker. At the end of each session, participants evaluated usability and cognitive workload of the system. Results. ITR and System Usability Scale (SUS) score were higher for the eye tracker (Wilcoxon signed-rank test: ITR T = 9, P = .016; SUS T = 12.50, P = .035). Cognitive workload was higher for the BCI (T = 4; P = .003). Conclusions. Although BCIs could be potentially useful for people with severe physical disabilities, we showed that the usability of BCIs based on the visual P300 remains inferior to eye tracking. We suggest that future research on visual BCIs should use eye tracking–based control as a comparison to evaluate performance or focus on nonvisual paradigms for persons who have lost gaze control.

Oculomotor capture by irrelevant onsets with and without color contrast.

It is widely known that irrelevant onsets (i.e., items appearing in previously empty locations) can automatically capture attention and attract our gaze. Some studies have shown that onset capture is stronger when the onset distractor matches the target feature, indicating that onset capture can be modulated by feature-based (top-down) tuning to the target. However, it is less clear whether and to what extent the perceptual saliency of the distractor can further modulate this effect. This study examined the effects of target similarity, competition between target and distractor, and bottom-up color contrast on the ability of onset distractor to capture the gaze, by varying the color (contrast) and stimulus-onset asynchrony of the onset distractor. The results clearly show that competition and feature-based attention modulate capture by the irrelevant onset to a large extent, whereas bottom-up color contrasts do not modulate onset capture. These results indicate the need to revise current accounts of gaze control.

The bilateral central vestibular system: its pathways, functions, and disorders.

The bilateral anatomical organization of the vestibular system provides three functional advantages: optimal differentiation of head motion and orientation, sensory substitution of a unilateral peripheral failure, and central compensation of a peripheral or central vestibular tone imbalance. The structure is based on bilaterally ascending and descending pathways and at least four crossings: three in the brain stem and one in the cortex. The resulting sensorimotor functions can be subdivided into three major groups: (1) reflexive control of gaze, head, and body in three spatial planes (yaw, pitch, roll) at the brain stem/cerebellar level; (2) perception of self-motion and control of voluntary movement and balance at the cortical/subcortical level; and (3) higher vestibular cognitive functions (e.g., spatial memory and navigation). The bilateral representation of the vestibular system in multiple multisensory cortical areas and the vestibular dominance of the nondominant hemisphere raise the question of how one global percept of motion and orientation in space is formed.

Cognitive control of gaze in bipolar disorder and schizophrenia

The objective of the present study was to compare two components of executive functioning, response monitoring and inhibition, in bipolar disorder (BP) and schizophrenia (SZ). The saccadic countermanding task is a translational paradigm optimized for detecting subtle abnormalities in response monitoring and response inhibition. We have previously reported countermanding performance abnormalities in SZ, but the degree to which these impairments are shared by other psychotic disorders is unknown. 18 BP, 17 SZ, and 16 demographically matched healthy controls (HC) participated in a saccadic countermanding task. Performance on the countermanding task is approximated as a race between movement generation and inhibition processes; this model provides an estimate of the time needed to cancel a planned movement. Response monitoring was assessed by the reaction time (RT) adjustments based on trial history. Like SZ patients, BP patients needed more time to cancel a planned movement. The two patient groups had equivalent inhibition efficiency. On trial history-based RT adjustments, however, we found a trend towards exaggerated trial history-based slowing in SZ compared to BP. Findings have implications for understanding the neurobiology of cognitive control, for defining the etiological overlap between schizophrenia and bipolar disorder, and for developing pharmacological treatments of cognitive impairments.

Impairment of shooting performance by background complexity and motion.

In many visual displays such as virtual environments, human tasks involve objects superimposed on both complex and moving backgrounds. However, most studies investigated the influence of background complexity or background motion in isolation. Two experiments were designed to investigate the joint influences of background complexity and lateral motion on a simple shooting task typical of video games. Participants had to perform the task on the moving and static versions of backgrounds of three levels of complexity, while their eye movements were recorded. The backgrounds displayed either an abstract (Experiment 1) or a naturalistic (Experiment 2) virtual environment. The results showed that performance was impaired by background motion in both experiments. The effects of motion and complexity were additive for the abstract background and multiplicative for the naturalistic background. Eye movement recordings showed that performance impairments reflected at least in part the impact of the background visual features on gaze control.

Higher landing accuracy in expert pilots is associated with lower activity in the caudate nucleus.

The most common lethal accidents in General Aviation are caused by improperly executed landing approaches in which a pilot descends below the minimum safe altitude without proper visual references. To understand how expertise might reduce such erroneous decision-making, we examined relevant neural processes in pilots performing a simulated landing approach inside a functional MRI scanner. Pilots (aged 20–66) were asked to “fly” a series of simulated “cockpit view” instrument landing scenarios in an MRI scanner. The scenarios were either high risk (heavy fog–legally unsafe to land) or low risk (medium fog–legally safe to land). Pilots with one of two levels of expertise participated: Moderate Expertise (Instrument Flight Rules pilots, n = 8) or High Expertise (Certified Instrument Flight Instructors or Air-Transport Pilots, n = 12). High Expertise pilots were more accurate than Moderate Expertise pilots in making a “land” versus “do not land” decision (CFII: d′ = 3.62±2.52; IFR: d′ = 0.98±1.04; p<.01). Brain activity in bilateral caudate nucleus was examined for main effects of expertise during a “land” versus “do not land” decision with the no-decision control condition modeled as baseline. In making landing decisions, High Expertise pilots showed lower activation in the bilateral caudate nucleus (0.97±0.80) compared to Moderate Expertise pilots (1.91±1.16) (p<.05). These findings provide evidence for increased “neural efficiency” in High Expertise pilots relative to Moderate Expertise pilots. During an instrument approach the pilot is engaged in detailed examination of flight instruments while monitoring certain visual references for making landing decisions. The caudate nucleus regulates saccade eye control of gaze, the brain area where the “expertise” effect was observed. These data provide evidence that performing “real world” aviation tasks in an fMRI provide objective data regarding the relative expertise of pilots and brain regions involved in it.

Microsaccade production during saccade cancelation in a stop-signal task

We obtained behavioral data to evaluate two alternative hypotheses about the neural mechanisms of gaze control. The “fixation” hypothesis states that neurons in rostral superior colliculus (SC) enforce fixation of gaze. The “microsaccade” hypothesis states that neurons in rostral SC encode microsaccades rather than fixation per se. Previously reported neuronal activity in monkey SC during the saccade stop-signal task leads to specific, dissociable behavioral predictions of these two hypotheses. When subjects are required to cancel partially-prepared saccades, imbalanced activity spreads across rostral and caudal SC with a reliable temporal profile. The microsaccade hypothesis predicts that this imbalance will lead to elevated microsaccade production biased toward the target location, while the fixation hypothesis predicts reduced microsaccade production. We tested these predictions by analyzing the microsaccades produced by 4 monkeys while they voluntarily canceled partially prepared eye movements in response to explicit stop signals. Consistent with the fixation hypothesis and contradicting the microsaccade hypothesis, we found that each subject produced significantly fewer microsaccades when normal saccades were successfully canceled. The few microsaccades escaping this inhibition tended to be directed toward the target location. We additionally investigated interactions between initiating microsaccades and inhibiting normal saccades. Reaction times were longer when microsaccades immediately preceded target presentation. However, pre-target microsaccade production did not affect stop-signal reaction time or alter the probability of canceling saccades following stop signals. These findings demonstrate that imbalanced activity within SC does not necessarily produce microsaccades and add to evidence that saccade preparation and cancelation are separate processes.

Optical limitations guide behavioral algorithms in Drosophila.

Optical limitations guide behavioral algorithms in Drosophila.

Extracellular matrix molecules exhibit unique expression pattern in the climbing fiber-generating precerebellar nucleus, the inferior olive

Extracellular matrix (ECM) accumulates around different neuronal compartments of the central nervous system (CNS) or appears in diffuse reticular form throughout the neuropil. In the adult CNS, the perineuronal net (PNN) surrounds the perikarya and dendrites of various neuron types, whereas the axonal coats are aggregations of ECM around the individual synapses, and the nodal ECM is localized at the nodes of Ranvier. Previous studies in our laboratory demonstrated on rats that the heterogeneous distribution and molecular composition of ECM is associated with the variable cytoarchitecture and hodological organization of the vestibular nuclei and may also be related to their specific functions in gaze and posture control as well as in the compensatory mechanisms following vestibular lesion. Here, we investigated the ECM expression pattern in the climbing fiber-generating inferior olive (IO), which is functionally related to the vestibular nuclei. By using histochemical and immunohistochemical methods, the most characteristic finding was the lack of PNNs, presumably due to the absence of synapses on the perikarya and proximal dendrites of IO neurons. On the other hand, the darkly stained dots or ring-like structures in the neuropil might represent the periaxonal coats around the axon terminals of olivary synaptic glomeruli. We have observed positive ECM reaction for the hyaluronan, tenascin-R, hyaluronan and proteoglycan link protein 1 (HAPLN1) and various chondroitin sulfate proteoglycans. The staining intensity and distribution of ECM molecules revealed a number of differences between the functionally different subnuclei of IO. We hypothesized that the different molecular composition and intensity differences of ECM reaction is associated with different control mechanisms of gaze and posture control executed by the visuomotor-vestibular, somatosensory and integrative subnuclei of the IO.

Eye-hand coordination during visuomotor adaptation with different rotation angles.

This study examined adaptive changes of eye-hand coordination during a visuomotor rotation task. Young adults made aiming movements to targets on a horizontal plane, while looking at the rotated feedback (cursor) of hand movements on a monitor. To vary the task difficulty, three rotation angles (30°, 75°, and 150°) were tested in three groups. All groups shortened hand movement time and trajectory length with practice. However, control strategies used were different among groups. The 30° group used proportionately more implicit adjustments of hand movements than other groups. The 75° group used more on-line feedback control, whereas the 150° group used explicit strategic adjustments. Regarding eye-hand coordination, timing of gaze shift to the target was gradually changed with practice from the late to early phase of hand movements in all groups, indicating an emerging gaze-anchoring behavior. Gaze locations prior to the gaze anchoring were also modified with practice from the cursor vicinity to an area between the starting position and the target. Reflecting various task difficulties, these changes occurred fastest in the 30° group, followed by the 75° group. The 150° group persisted in gazing at the cursor vicinity. These results suggest that the function of gaze control during visuomotor adaptation changes from a reactive control for exploring the relation between cursor and hand movements to a predictive control for guiding the hand to the task goal. That gaze-anchoring behavior emerged in all groups despite various control strategies indicates a generality of this adaptive pattern for eye-hand coordination in goal-directed actions.

Fuzzy Integral-Based Gaze Control of a Robotic Head for Human Robot Interaction.

During the last few decades, as a part of effort to enhance natural human robot interaction (HRI), considerable research has been carried out to develop human-like gaze control. However, most studies did not consider hardware implementation, real-time processing, and the real environment, factors that should be taken into account to achieve natural HRI. This paper proposes a fuzzy integral-based gaze control algorithm, operating in real-time and the real environment, for a robotic head. We formulate the gaze control as a multicriteria decision making problem and devise seven human gaze-inspired criteria. Partial evaluations of all candidate gaze directions are carried out with respect to the seven criteria defined from perceived visual, auditory, and internal inputs, and fuzzy measures are assigned to a power set of the criteria to reflect the user defined preference. A fuzzy integral of the partial evaluations with respect to the fuzzy measures is employed to make global evaluations of all candidate gaze directions. The global evaluation values are adjusted by applying inhibition of return and are compared with the global evaluation values of the previous gaze directions to decide the final gaze direction. The effectiveness of the proposed algorithm is demonstrated with a robotic head, developed in the Robot Intelligence Technology Laboratory at Korea Advanced Institute of Science and Technology, through three interaction scenarios and three comparison scenarios with another algorithm.

Control of binocular gaze in a high-precision manual task

We investigated the precision of binocular gaze control while observers performed a high-precision manual movement, which involved hitting a target hole in a plate with a hand-held needle. Binocular eye movements and the 3D-position of the needle tip were tracked. In general the observers oriented their gaze to the target before they reached it with the needle. The amplitude of microsaccades scaled with the distance of the needle tip. We did not find evidence for the coordination of version and vergence during microsaccades which could be expected if those movements displaced gaze between the needle and the target hole. In a control experiment observers executed small saccades between marks on a slanted plane. Even when the observers executed saccades as small as the microsaccades in the needle experiment, we observed a coordinated displacement of the point of gaze on the horizontal and depth axis. Our results show that the characteristics of eye movements such as the frequency and amplitude of microsaccades are adapted online to the task demands. However, a coordinated control of version and vergence in small saccades is only observed if a movement of gaze on a slanted trajectory is explicitly instructed.

Personality traits modulate subcortical and cortical vestibular and anxiety responses to sound-evoked otolithic receptor stimulation

ObjectiveStrong links between anxiety, space-motion perception, and vestibular symptoms have been recognized for decades. These connections may extend to anxiety-related personality traits. Psychophysical studies showed that high trait anxiety affected postural control and visual scanning strategies under stress. Neuroticism and introversion were identified as risk factors for chronic subjective dizziness (CSD), a common psychosomatic syndrome. This study examined possible relationships between personality traits and activity in brain vestibular networks for the first time using functional magnetic resonance imaging (fMRI). MethodsTwenty-six right-handed healthy individuals underwent fMRI during sound-evoked vestibular stimulation. Regional brain activity and functional connectivity measures were correlated with personality traits of the Five Factor Model (neuroticism, extraversion-introversion, openness, agreeableness, consciousness). ResultsNeuroticism correlated positively with activity in the pons, vestibulo-cerebellum, and para-striate cortex, and negatively with activity in the supra-marginal gyrus. Neuroticism also correlated positively with connectivity between pons and amygdala, vestibulo-cerebellum and amygdala, inferior frontal gyrus and supra-marginal gyrus, and inferior frontal gyrus and para-striate cortex. Introversion correlated positively with amygdala activity and negatively with connectivity between amygdala and inferior frontal gyrus. ConclusionsNeuroticism and introversion correlated with activity and connectivity in cortical and subcortical vestibular, visual, and anxiety systems during vestibular stimulation. These personality-related changes in brain activity may represent neural correlates of threat sensitivity in posture and gaze control mechanisms in normal individuals. They also may reflect risk factors for anxiety-related morbidity in patients with vestibular disorders, including previously observed associations of neuroticism and introversion with CSD.

Quiet Eye Training Improves Small Arms Maritime Marksmanship

Quiet eye training—teaching task-specific gaze control—has been consistently shown to optimize the acquisition of motor skills. The present study aimed to examine the potential benefits of a quiet eye training intervention in a simulated maritime marksmanship task that involved shooting fast approaching moving targets with a decommissioned general-purpose machine gun. Twenty participants were randomly assigned to a quiet eye trained (QET) or technical trained (TT) group and completed 2 baseline, 20 training, and 2 retention trials on the moving-target task. Compared to their TT counterparts, the QET group displayed more effective gaze control (longer quiet eye durations and greater target locking) and more accurate performance (smaller radial error of both the initial shot and average of all shots) at retention. These findings highlight the potential for quiet eye training to be used to support the training of marksmanship skills in military settings.

High-precision control of binocular gaze

High-precision control of binocular gaze