Monocular Eye Movements Research Articles

Effect of binocular vision during target shooting in archery.

This study aimed to evaluate the difference between binocular and monocular vision and eye movements during the competition using video-oculography (VOG). Experiment 1 included 14 participants to evaluate differences in arrow convergence. Then, seven participants in Experiment 1 were randomly selected and included in Experiment 2, which evaluated eye movements during archery using VOG. The target used an 80-cm waterproof target face and was set at a distance of 30 m. All players shot the target 36 times using their bows and arrows. Experiments 1 and 2 evaluated the distribution of arrows in each score and the number of focus points, respectively, between binocular and monocular conditions. The arrows, which include the area of 9 points, were significantly greater in the binocular condition (11.85 ± 5.04 shots) than in the monocular condition (9.36 ± 5.41 shots) in Experiment 1 (P = 0.047). The players focused on the target under both binocular and monocular conditions, although the players were switching off fixation between the target and shooting sight under the binocular condition in Experiment 2. These behaviors indicated that the players were trying to accurately shoot the target by exploring the distance between themselves and the target as a cue for depth perception.

A distributed saccade-associated network encodes high velocity conjugate and monocular eye movements in the zebrafish hindbrain

Saccades are rapid eye movements that redirect gaze. Their magnitudes and directions are tightly controlled by the oculomotor system, which is capable of generating conjugate, monocular, convergent and divergent saccades. Recent studies suggest a mainly monocular control of saccades in mammals, although the development of binocular control and the interaction of different functional populations is less well understood. For zebrafish, a well-established model in sensorimotor research, the nature of binocular control in this key oculomotor behavior is unknown. Here, we use the optokinetic response and calcium imaging to characterize how the developing zebrafish oculomotor system encodes the diverse repertoire of saccades. We find that neurons with phasic saccade-associated activity (putative burst neurons) are most frequent in dorsal regions of the hindbrain and show elements of both monocular and binocular encoding, revealing a mix of the response types originally hypothesized by Helmholtz and Hering. Additionally, we observed a certain degree of behavior-specific recruitment in individual neurons. Surprisingly, calcium activity is only weakly tuned to saccade size. Instead, saccade size is apparently controlled by a push–pull mechanism of opposing burst neuron populations. Our study reveals the basic layout of a developing vertebrate saccade system and provides a perspective into the evolution of the oculomotor system.

Functional architecture underlying binocular coordination of eye position and velocity in the larval zebrafish hindbrain

BackgroundThe oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into persistent position coding output, which plays a crucial role in retinal image stability. For a mechanistic understanding of the integrator function and eye position control, knowledge about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning to motor variables remains uncharacterized.ResultsHere, we recorded cellular calcium signals while evoking monocular and binocular optokinetic eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical distributions of motoneurons and internuclear neurons in the nucleus abducens as well as those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned to eye position and/or velocity to variable extents and is only activated after surpassing particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) mainly codes for eye position, in rhombomeres 7/8, a velocity-to-position coding gradient exists along the rostro-caudal axis, which likely corresponds to the oculomotor structures storing velocity and position, and is in agreement with a feedforward mechanism of persistent activity generation. Position encoding neurons are recruited at eye position thresholds distributed across the behaviourally relevant dynamic range, while velocity-encoding neurons have more centred firing thresholds for velocity. In the abducens, neurons coding exclusively for one eye intermingle with neurons coding for both eyes. Many of these binocular neurons are preferentially active during conjugate eye movements and less active during monocular eye movements. This differential recruitment during monocular versus conjugate tasks represents a functional diversification in the final common motor pathway.ConclusionsWe localized and functionally characterized the repertoire of oculomotor neurons in the zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular code and suggest that generation of persistent activity is organized along the rostro-caudal axis in the hindbrain.

Epileptic ictal strabismus: a case report and review of the literature

Ictal strabismus, sometimes associated with epileptic nystagmus, is an extremely rare epileptic phenomenon, suggestive of cortical involvement in monocular eye movement control. We describe a patient with ictal disconjugate contraversive horizontal eye deviation of cortical origin as the main clinical feature of a focal seizure. A 17-year-old, previously healthy woman had a seizure characterized by initial rightward conjugate eye deviation, followed by convergent strabismus due to adduction of the right eye towards the nose without conjugate left eye abduction (esotropia), forced leftward head deviation with impaired awareness, and subsequent evolution into a bilateral tonic-clonic seizure. Postictal and interictal neurological status were unremarkable; more specifically, neuro-ophthalmological examination revealed no nystagmus or altered eye motility. Ictal EEG showed a rhythmic theta activity over the right posterior temporal region, involving fronto-central regions when strabismus appeared. MRI showed cortical dysplasia in the right temporal lobe. Due to the low spatial resolution of scalp EEG, we could not identify with precision the symptomatogenic zone underlying ictal strabismus. However, the concomitant appearance of rhythmic theta activity over the right fronto-central region and the leftward head version with MRI perfusion sequences, showing cerebral blood flow increase in the right frontal eye field area, suggest involvement of the right frontal lobe. [Published with video sequence on www.epilepticdisorders.com].

The surgical management of restrictive strabismus caused by thyroid-associated ophthalmopathy

Objective To investigate the clinical features of restrictive strabismus caused by thyroid-associated ophthalmopathy (TAO) and the effect of rectus tenotomy for restrictive strabismus. Methods Thirty-seven TAO patients with restrictive strabismus were collected in our hospital. For every patient, the most restricted extraocular muscles were determined by monocular cover, eye movement and passive traction test. Rectus tenotomy only or combined with shortening the antagonist mucle was performed on the most restricted one or more muscles.The position of eyes, eyes movements and diplopia were measured pre- and post-operatively. Results All the patients had good results.Thirty-two patients (86.5%) had the elimination of diplopia, significant improvement of eye movements in every direction and the strabismus angle less then 5°. Four cases had obvious improvements and one case was undercorrection. Four patients had postoperative complicated eyelid retraction. Conclusion Rectus tenotomy can effectively eliminate restrictive strabismus caused by TAO. Key words: Thyroid-associated ophthalmopathy; Strabismus, restrictive; Rectus tenotomy

Smooth pursuit eye movements in patients with macular degeneration.

Currently, there are no quantitative studies of smooth pursuit, a behavior attributed to the fovea, in individuals with macular degeneration (MD). We hypothesize that pursuit in MD patients depends on the relative positions of the scotoma and target trajectory. We tested this hypothesis with a scanning laser ophthalmoscope (SLO), which allows for direct visualization of the target on the damaged retina. Monocular microperimetry and eye movements were assessed in eleven individuals with differing degrees of MD. Observers were asked to visually track a 1.7° target that moved in one of eight radial directions at 5°/s–6°/s. Consistent with our hypothesis, pursuit metrics depended on whether the target moved into or out of scotoma. Pursuit gains decreased with increasing scotoma extent in the target's heading direction (p = 0.017). Latencies were higher when the scotoma was present along the target trajectory (in either starting or heading directions, p < 0.001). Furthermore, an analysis of retinal position shows that targets fell on the fixational locus nearly 50% of the time. The results suggest that MD patients are capable of smooth pursuit eye movements, but are limited by target trajectory and scotoma characteristics.

Neural circuits that drive binocular eye movements: implications for understanding and correcting strabismus.

Strabismus is the misalignment of the eyes and is estimated to be present in ~2% to 4% of the North American infant population. Surprisingly, to date, there is no consensus regarding the cause of strabismus. While it is commonly thought to be the result of dysfunctional orbital and/or eye muscle properties (reviewed in Refs. 1, 2), recent work emphasizes that strabismus can also be caused by the brain’s inability to transform binocular visual inputs into the motor commands required for coordinated eye motion at cortical as well as subcortical levels (reviewed in Refs. 3, 4). To gain a better understanding of the underlying changes in sensorimotor control that are responsible for strabismus, researchers have begun to perform studies in nonhuman primates. Typically, eye misalignment is induced using either surgical or visual methods (e.g., the weakening of the eye muscles or nerves versus the wearing of prism goggles). As adults, these strabismic monkeys make eye movements much like strabismus patients (i.e., consistent with estropia or exotropia). A study in this month’s issue of IOVS by Walton et al. demonstrates that when strabismus is induced in young monkeys either by the wearing of prism goggles or by medial rectus tenotomy, the activity of individual abducens nucleus neurons is reduced compared to that observed in monkeys raised with normal visual input. Since abducens neurons control the eye muscles that drive horizontal eye movements, these results provide evidence that changes in either sensory input or the eye muscles during development can have profound effects on the set point of the motor pathways required for accurate binocular control. In normal animals, the premotor and motoneurons that control eye movements preferentially encode the movement of an individual eye rather than the conjugate component of each eye movement (reviewed in Ref. 8). In their current study, Walton and colleagues found that this is also true for abducens neurons in strabismic monkeys. Moreover, both neuronal monocular tuning and eye movement sensitivities were normal. Instead, the authors’ data indicate a marked loss of tonic activity in the motoneuron input to the eye muscles. While premotor pathways are also altered in strabismic monkeys (the stimulation of premotor saccadic neurons in the pons produces abnormally disconjugate eye movements, and neurons in the supraoculomotor area [SOA] statically encode the angle of strabismus), there is currently no clear explanation for the observed loss of tonic activity in abducens. In this context, further studies of visuomotor pathways, as well as the abducens internuclear neuron to medial rectus motoneuron pathway, will likely reveal key abnormalities. For instance, Van Horn et al. recently identified a subclass of neurons in the rostral superior colliculus that robustly encode vergence angle in normal animals, suggesting this as a potentially interesting site to explore. Ultimately, such targeted experiments, comparing how the brain is normally circuited to how it develops in animals with different forms of strabismus, are needed to develop more optimally directed therapies for correcting this relatively common condition.

Effect of artificial scotomas on open-loop disparity vergence eye movements.

To investigate the effect of an artificial scotoma on open-loop disparity vergence responses (DVRs) and vergence control mechanisms, we examined open-loop DVRs to disparity stimuli using monocular artificial scotomas in normal subjects. Using a mirror haploscope with two computer monitors, we delivered disparity stimuli on a pair of random dot patterns subtending 40 by 30 degrees at 47 cm from each eye. The scotomas were black circles located in the center of a random dot pattern for the left eye. Eye movements of both eyes were recorded with a magnetic search coil system. We first found that the amplitudes of DVRs were gradually decreased and the latency of DVRs was moderately increased as the size of the scotomas was increased. Second, monocular responses from each eye were symmetrical although the stimuli to each eye were asymmetrical. The results suggest that the monocular eye movements in disparity vergence are controlled by a binocular central mechanism, not driven separately by monocular inputs in the open-loop window.

Epileptic monocular nystagmus and ictal diplopia as cortical and subcortical dysfunction.

We present the case of a patient with ictal monocular nystagmus and ictal diplopia who became seizure-free after resection of a right frontal focal cortical dysplasia (FCD), type 2B. Interictal neuroophthalmological examination showed several beats of a monocular nystagmus and a spasm of the contralateral eye. An exclusively ictal monocular epileptic nystagmus could be an argument for an exclusively cortical involvement in monocular eye movement control. The interictal findings in our patient, however, argue for an irregular ictal activation of both the cortical frontal eye field and the brainstem.

Brow Motility in Mitochondrial Myopathy

To quantify the range of brow excursion in patients with mitochondrial myopathy and chronic progressive external ophthalmoplegia (CPEO). Comparative case series. Digital image processing techniques were used to quantify the upper eyelid resting position, brow excursion, and monocular eye movements (ductions) in 19 patients with mitochondrial myopathy and CPEO and in 27 healthy control subjects. All patients with CPEO had ptosis ranging from 0.6 to 8 mm. For most patients, eye motility limitation was symmetrical. Elevation was the most affected eye movement. Patient's brow motility was on average 56.7% of the motility seen in the control group, and did not correlate with age or eye motility in any direction. Seventy-six percent of the brows displayed more than 2 mm of excursion. In patients with CPEO, the occipitofrontalis muscle is less affected than the extraocular muscles. Most patients display a useful degree of brow excursion that theoretically can be used to clear the visual axis after a conservative brow suspension.

Visual strategies of sub-elite cricket batsmen in response to different ball velocities

When different interceptive skills are considered, humans tend not to pursuit track the approaching object along its entire trajectory to the point of interception. Previous research of cricket batsmen facing medium paced deliveries reported pursuit visual tracking of the ball for the first 100–150 ms of flight followed by a saccade to the predicted ball bounce location. The aim of this study was to examine eye movements of batsmen while facing a range of slow to medium pace delivery speeds. Thirteen sub-elite batsmen faced 36 deliveries from a ball machine in which the projection speed was randomly varied across a range of 17–25 ms −1. The foveal gaze of the batsmen was recorded with a monocular eye movement registration system. Gaze strategies differed between participants in several ways, i.e., in the initial location of gaze prior to delivery (on the outlet of the ball machine or “parked” at a location on the predicted flight trajectory), the behavior immediately after ball release (pursuit tracking or saccade), and the behavior in mid-late flight (predictive saccade to the bounce point or “parafoveal” pursuit tracking). Across the range of delivery speeds used in the current study, it was possible to pursuit track the ball from release to bounce point but it was also possible to choose to make saccades along the trajectory. Depending on the spatio-temporal demands of the task and the intentions of the batsman a range of visual search strategies can be employed to support their actions.

Tonic and phasic phenomena underlying eye movements during sleep in the cat

Mammalian sleep is not a homogenous state, and different variables have traditionally been used to distinguish different periods during sleep. Of these variables, eye movement is one of the most paradigmatic, and has been used to differentiate between the so-called rapid eye movement (REM) and non-REM (NREM) sleep periods. Despite this, eye movements during sleep are poorly understood, and the behaviour of the oculomotor system remains almost unknown. In the present work, we recorded binocular eye movements during the sleep-wake cycle of adult cats by the scleral search-coil technique. During alertness, eye movements consisted of conjugated saccades and eye fixations. During NREM sleep, eye movements were slow and mostly unconjugated. The two eyes moved upwardly and in the abducting direction, producing a tonic divergence and elevation of the visual axis. During the transition period between NREM and REM sleep, rapid monocular eye movements of low amplitude in the abducting direction occurred in coincidence with ponto-geniculo-occipital waves. Along REM sleep, the eyes tended to maintain a tonic convergence and depression, broken by high-frequency bursts of complex rapid eye movements. In the horizontal plane, each eye movement in the burst comprised two consecutive movements in opposite directions, which were more evident in the eye that performed the abducting movements. In the vertical plane, rapid eye movements were always upward. Comparisons of the characteristics of eye movements during the sleep-wake cycle reveal the uniqueness of eye movements during sleep, and the noteworthy existence of tonic and phasic phenomena in the oculomotor system, not observed until now.

Vergence nystagmus induced by motion in the ground plane: Normal response characteristics

We displayed backward/forward motion on a computer monitor in the ground plane. Subjects looked at the center of a moving pattern and eye movements of both eyes were recorded with a search coil system. Involuntary nystagmus including vertical version (VV) and horizontal vergence (HV) was recorded. Dynamics of the nystagmus showed that the slow and quick phase of VV and HV were always associated with each other while the monocular horizontal eye movements composed of HV were either symmetrical or asymmetrical. Peak velocity, amplitudes and frequency of the VV and HV responses were quantified. The results suggest that involuntary HV nystagmus can be induced by simple motion from simulated optic flow in the ground plane and the HV nystagmus helps moving subjects to stabilize their gazes on the object of interest.

Gain of Human Torsional Optokinetic Nystagmus Depends on Horizontal Disparity

To investigate the effects of horizontal disparity on torsional optokinetic nystagmus (tOKN) in humans. Ten healthy human subjects were selected for this experiment. Monocular eye movements were recorded three-dimensionally using dual-search coil methods. Torsional OKN was induced by a rotating random-dot pattern (22 degrees in diameter, constant angular velocity: +/-54 deg/s) projected on the virtual screen of the optical see-through, head-mounted display (HMD). The optical distance of the HMD's virtual screen was 2 m. A red LED that could be fixated through the virtual screen of the HMD was located near the center of the rotating random-dot pattern. Horizontal disparity was induced by changing the distance between the fixated target and the subject systematically (1, 1.5, 2, or 3 m; five subjects) or by the prism (+1.5, +0.5, 0, or -0.5 prism-diopter [PD] in each eye; five subjects) in front of the HMD. The average gain with zero horizontal disparity (0.022 +/- 0.008/0.025 +/- 0.014, fixated target at 2 m/fixated target with the plain glass) was significantly higher than the gain with crossed disparity (0.017 +/- 0.003/0.019 +/- 0.008, target at 3 m/with the prism of -0.5 PD) and uncrossed disparity (0.017 +/- 0.002, target at 1 m/with the prism of +1.5 PD; one-way ANOVA, P <0.05). The horizontal disparity of optokinetic stimulus affects tOKN. Nonzero horizontal disparity decreases the gain of tOKN.

The Saccadic system more readily co-processes orthogonal than co-linear saccades

Real-life visual tasks such as tracking jumping objects and scanning visual scenes often require a sequence of saccadic eye movements. The ability of the ocular motor system to parallel process saccades has been previously demonstrated. We recorded the monocular eye movements of five normal human subjects using the magnetic search coil technique in a double step paradigm. Initial target jumps were always purely horizontal or purely vertical. We were interested in the latency to onset of the second saccade as a function of direction in relation to the first saccade. When the inter stimulus interval (ISI) was 150 or 180 ms orthogonal second saccades were of significantly shorter latency than second co-linear saccades. When the ISI was 250 ms the latencies of orthogonal and co-linear second saccades were statistically indistinguishable. Based on these findings it is postulated that the ocular motor system can more readily co-process orthogonal than co-linear saccades.

Differential effects of blinks on horizontal saccade and smooth pursuit initiation in humans.

Blinks executed during eye movements affect kinetic eye movement parameters, e.g., peak velocity of saccades is decreased, their duration is increased, but their amplitude is not altered. This effect is mainly explained by the decreased activity of premotor neurons in the brainstem: omni-pause neurons (OPN) in the nucleus raphe interpositus. Previous studies examined the immediate effect of blinks directly on eye movements but not their effect when they are elicited several hundred milliseconds before the eye movements. In order to address this question we tested blinks elicited before the target onset of saccades and pursuit and compared the results to the gap effect: if a fixation light is extinguished for several hundred milliseconds, the reaction time (latency) for subsequent saccades or smooth pursuit eye movements is decreased. Monocular eye and lid movements were recorded in nine healthy subjects using the scleral search-coil system. Laser stimuli were front-projected onto a tangent screen in front of the subjects. Horizontal step-ramp smooth pursuit of 20 deg/s was elicited in one session, or 5 deg horizontal visually guided saccades in another experimental session. In one-third of the trials (smooth pursuit or saccades) the fixation light was extinguished for 200 ms before stimulus onset (gap condition), and in another third of the trials reflexive blinks were elicited by a short airpuff before the stimulus onset (blink condition). The last third of the trials served as controls (control condition). Stimulus direction and the three conditions were randomized for saccades and smooth pursuit separately. The latency of the step-ramp smooth pursuit in the blink condition was found to be decreased by 10 ms, which was less than in the gap condition (38 ms). However, the initial acceleration and steady-state velocity of smooth pursuit did not differ in the three conditions. In contrast, the latency of the saccades in the gap condition was decreased by 39 ms, but not in the blink condition. Saccade amplitude, peak velocity, and duration were not different in the three conditions. There was also no difference in blink amplitude and duration of pupil occlusion in the blink condition, neither in saccades nor in smooth pursuit. The latency reduction of smooth pursuit, but not of saccades, may neither be explained by the brief pupil occlusion nor by visual suppression, warning signals, or the startle response. Whether the effects are caused by the influence of blinks on OPNs or other premotor structures remains to be tested.

Three-dimensional eye movement analysis of superior oblique myokymia

Purpose To confirm the idea that sole contraction of the superior oblique muscle causes attacks of superior oblique myokymia (SOM). Design Observational case report. Methods A 43-year-old man presented with episodic monocular oscillatory eye movements. Three-dimensional eye movements were recorded using the magnetic search coil system and analyzed as rotation vector. The attacks of SOM consisted of intorsional, depressive, and abductive fast phases and their exponential decaying slow phases. Results Average direction of rotation axis for the fast phases while fixating straight ahead was 51.5 ± 5.4 degrees from depression axis in vertical-torsional plane, 78.7 ± 4.4 degrees from abduction axis in horizontal-torsional plane, and 76.3 ± 4.3 degrees from abduction axis in horizontal-vertical plane (±SD, n = 50). Time constants of slow phases were less than 0.1 second. Conclusions Quantitative three-dimensional analysis of SOM directly confirmed that the fast phases of SOM attacks were induced by the sole contraction of the superior oblique muscle.

Disparity-Selective Neurons in Area V4 of Macaque Monkeys

Area V4 is an intermediate stage of the ventral visual pathway providing major input to the final stages in the inferior temporal cortex (IT). This pathway is involved in the processing of shape, color, and texture. IT neurons are also sensitive to horizontal binocular disparity, suggesting that binocular disparity is processed along the ventral visual pathway. In the present study, we examined the processing of binocular disparity information by V4 neurons. We recorded responses of V4 neurons to binocularly disparate stimuli. A population of V4 neurons modified their responses according to changes of stimulus disparity; neither monocular responses nor eye movements could account for this modulation. Disparity-tuning curves were similar for different locations within a neuron's receptive field. Neighboring neurons recorded using a single electrode displayed similar disparity-tuning properties. These findings indicate that a population of V4 neurons is selective for binocular disparity, invariant for the position of the stimulus within the receptive field. The finding that V4 neurons with similar disparity selectivity are clustered suggests the existence of functional modules for disparity processing in V4.

Disparity selectivity of neurons in monkey inferior temporal cortex.

The inferior temporal cortex (IT) of the monkey, a final stage in the ventral visual pathway, has been known to process information on two-dimensional (2-D) shape, color, and texture. On the other hand, the dorsal visual pathway leading to the posterior parietal cortex has been known to process information on location in space. Likewise, neurons selective for binocular disparity, which convey information on depth, have been found mainly in areas along the dorsal visual pathway. Here, we report that many neurons in the IT are also selective for binocular disparity. We recorded extracellular activity from IT neurons and found that more than half of the neurons changed their response depending on the disparity added. The change was not attributed to monocular responses or eye movements. Most neurons selective for disparity were "near" or "far" cells; they preferred either crossed or uncrossed disparity, and only a small population was tuned to zero disparity. Disparity-selective neurons were also selective for shape. Most preferred the same type of disparity irrespective of the shape presented. Disparity preference was also invariant for the fronto-parallel translation of the stimuli in most of the neurons. Finally, nearby neurons exhibited similar disparity selectivity, suggesting the existence of a functional module for processing of binocular disparity in the IT. From the above and our recent findings, we suggest that the IT integrates shape and binocular disparity information, and plays an important role in the reconstruction of three-dimensional (3-D) surfaces.

Premotor commands encode monocular eye movements.

Binocular coordination of eye movements is essential for stereopsis (depth perception) and to prevent double vision. More than a century ago, Hering and Helmholtz debated the neural basis of binocular coordination. Helmholtz believed that each eye is controlled independently and that binocular coordination is learned. Hering believed that both eyes are innervated by common command signals that yoke the eye movements (Hering's law of equal innervation). Here we provide evidence that Hering's law is unlikely to be correct. We show that premotor neurons in the paramedian pontine reticular formation that were thought to encode conjugate velocity commands for saccades (rapid eye movements) actually encode monocular commands for either right or left eye saccades. However, 66% of the abducens motor neurons, which innervate the ipsilateral lateral rectus muscle, fire as a result of movements of either eye. The distribution of sensitivity to ipsilateral and contralateral eye movements across the abducens motor neuron pool may provide a basis for learning binocular coordination in infancy and adapting it throughout life.