Asymmetric Vergence Research Articles

A new oculomotor model demystifies "Remarkable Saccades".

Hering's Law of binocular eye movement control guides most oculomotor research and supports diagnosis and treatment of clinical eye misalignment (strabismus). The law states that all eye movements are controlled by a unitary conjugate signal and a unitary vergence signal that sum. Recent evidence of temporally asynchronous inter-eye rotations during vergence (Chandna et al., 2021) challenges the viability of a unitary vergence signal. An alternative theory that might explain these anomalous results posits that the eyes are controlled independently. Yet independent control fails to explain a phenomenon known as "Remarkable Saccades" where an inappropriate saccade occurs from an eye aligned on a target during asymmetric vergence (Enright, 1992). We introduce a new model formulated to describe the Chandna et al. (2021) midline vergence result that generates remarkable saccades as an emergent property. The Hybrid Binocular Control model incorporates independent controllers for each eye with a cortical origin that interact with a unitary conjugate controller residing in brainstem. The model also accounts for behavioral variations in remarkable saccades when observers attend to an eye. Furthermore, it suggests more generally how the eyes are controlled during vergence and other voluntary eye movements, thus challenging documented oculomotor neural circuitry and suggesting that refinements are needed for clinical oculomotor interventions.

Biometric assessment of pseudophakic subjects during objective accommodative stimulation: a prospective observational study

ABSTRACT Clinical relevance: Ultrasound biomicroscopy is an objective method for assessing changes in anterior segment biometry. There is a paucity of data on the reliability of this method. A reliable method for assessing anterior segment changes during physiologically driven accommodation can be a useful tool for clinicians, researchers, and industry. Background: To assess the test–retest reliability of ultrasound biomicroscopy for measurements of change in anterior chamber depth during a distance to near fixation task in pseudophakic subjects. Methods: Subjects were adults with monofocal intraocular lenses implanted in both eyes who completed a 6-month post-operative period and had monocular uncorrected distance visual acuity of 6/15 (0.4 logMAR) or better. The change in anterior chamber depth during a distance to near fixation task was measured with a 35-MHz VuMAX HD ultrasound biomicroscopy device (Sonomed Escalon, New Hyde Park, NY) during two separate visits. An asymmetrical vergence paradigm allowed evaluation of anterior segment biometry at 22-µm axial resolution in one eye, while the fellow eye fixated on the target. To assess the test–retest reliability, 2-sided 95% CI from a paired t test was calculated for the difference in anterior chamber depth change from distance to near between visits. Results: The mean (standard deviation) near-focused anterior chamber depth measured by ultrasound biomicroscopy was 4.331 (0.237) and 4.333 (0.241) mm at visits 1 and 2, respectively. In response to a change in fixation from distance (4 m) to near (40 cm), the mean anterior chamber depth change was −0.012 (0.038) and 0.003 (0.039) mm at visits 1 and 2, respectively. Analysis of the difference in the change in anterior chamber depth between visits was −0.015 mm (95% CI, −0.035 to 0.003). Conclusion: Ultrasound biomicroscopy is a repeatable, objective method for assessing change in anterior segment biometry during physiological changes in fixation from distance to near.

Changes in Perceived Egocentric Direction during Symmetric Vergence

The Wells-Hering's laws of perceived egocentric visual direction (EVD) assume that information about eye position includes equal contributions from both eyes. An implication of this assumption is that only versional eye movements should lead to a change in perceived EVD. Previously, we showed that a differential weighting of eye-position information occurs in some individuals during asymmetric vergence. To extend this finding, we determined here whether a differential weighting of eye-position information occurs also during symmetric vergence eye movements. Open-loop pointing responses to a bright target were obtained in five subjects to estimate the contribution of each eye's position information to perceived EVD during symmetric vergence demands that ranged from 6 prism diopters base in to 18 prism diopters base out. In all five subjects, the slopes of the lines fit to the pointing responses were in the direction that was predicted from an unequal weighting of eye-position information. We conclude that symmetric vergence movements can result in a change in perceived visual direction, contrary to an assumption of the Wells-Hering's laws.

Error Correction in Vergence Eye Movements: Evidence Supporting Hering’s Law

In pure symmetrical vergence eye movements, a fusion initiating component quickly brings the eyes close to the desired position. A small error usually remains after this response which must be corrected to attain the small final vergence error (i.e., fixation disparity). Error correction will usually involve both version and version movements so possible mechanisms include: small saccades, smooth pursuit, symmetrical vergence, or some combination. Alternatively, an asymmetrical vergence or uniocular slow eye movement could be used to achieve the highly precise final position. Saccade-free late fusion sustaining components during the steady state to a symmetrical vergence step stimulus are analyzed using independent component analysis. Results suggest that fine correction is most likely the product of closely coordinated version and vergence components.

Motor nucleus activity fails to predict extraocular muscle forces in ocular convergence

For a given eye position, firing rates of abducens neurons (ABNs) generally (Mays et al. 1984), and lateral rectus (LR) motoneurons (MNs) in particular (Gamlin et al. 1989a), are higher in converged gaze than when convergence is relaxed, whereas LR and medial rectus (MR) muscle forces are slightly lower (Miller et al. 2002). Here, we confirm this finding for ABNs, report a similarly paradoxical finding for neurons in the MR subdivision of the oculomotor nucleus (MRNs), and, for the first time, simultaneously confirm the opposing sides of these paradoxes by recording physiological LR and MR forces. Four trained rhesus monkeys with binocular eye coils and custom muscle force transducers on the horizontal recti of one eye fixated near and far targets, making conjugate saccades and symmetric and asymmetric vergence movements of 16-27°. Consistent with earlier findings, we found in 44 ABNs that the slope of the rate-position relationship for symmetric vergence (k(V)) was lower than that for conjugate movement (k(C)) at distance, i.e., mean k(V)/k(C) = 0.50, which implies stronger LR innervation in convergence. We also found in 39 MRNs that mean k(V)/k(C) = 1.53, implying stronger MR innervation in convergence as well. Despite there being stronger innervation in convergence at a given eye position, we found both LR and MR muscle forces to be slightly lower in convergence, -0.40 and -0.20 g, respectively. We conclude that the relationship of ensemble MN activity to total oculorotary muscle force is different in converged gaze than when convergence is relaxed. We conjecture that LRMNs with k(V) < k(C) and MRMNs with k(V) > k(C) innervate muscle fibers that are weak, have mechanical coupling that attenuates their effective oculorotary force, or serve some nonoculorotary, regulatory function.

Relative contributions of the two eyes to perceived egocentric visual direction in normal binocular vision

Perceived egocentric direction (EVD) is based on the sensed position of the eyes in the orbit and the oculocentric visual direction (eye-centered, OVD). Previous reports indicate that in some subjects eye-position information from the two eyes contributes unequally to the perceived EVD. Findings from other studies indicate that the retinal information from the two eyes may not always contribute equally to perceived OVD. The goal of this study was to assess whether these two sources of information covary similarly within the same individuals. Open-loop pointing responses to an isolated target presented randomly at several horizontal locations were collected from 13 subjects during different magnitudes of asymmetric vergence to estimate the contribution of the position information from each eye to perceived EVD. For the same subjects, the direction at which a horizontally or vertically disparate target with different interocular contrast or luminance ratios appeared aligned with a non-disparate target estimated the relative contribution of each eye’s retinal information. The results show that the eye-position and retinal information vary similarly in most subjects, which is consistent with a modified version of Hering’s law of visual direction.

Correction of Saccade-Induced Midline Errors in Responses to Pure Disparity Vergence Stimuli.

Purely symmetrical vergence stimuli aligned along the midline (cyclopean axis) require only a pure vergence response. Yet, in most responses saccades are observed and these saccades must either produce an error in the desired midline response or correct an error produced by asymmetry in the vergence response. A previous study (Semmlow, et al. 2008) has shown that the first saccade to appear in a response to a pure vergence stimulus usually increased the deviation from the midline, although all subjects (N = 12) had some responses where the initial saccade corrected a vergence induced midline error. This study focuses on those responses where the initial saccade produces an increased midline deviation and the resultant compensation that ultimately brings the eyes to the correct binocular position. This correction is accomplished by a higher level compensatory mechanism that uses offsetting asymmetrical vergence and/or corrective saccades. While responses consist of a mixture of the two compensatory mechanisms, the dominant mechanism is subject-dependent. Since fixation errors are quite small (minutes of arc), some feedback controlled physiological process involving smooth eye movements, and possibly saccades, must move the eyes to reduce binocular error to fixation disparity levels.

Saccadic Behavior during the Response to Pure Vergence Stimuli I: General Properties

If two targets are carefully aligned so that they fall along the cyclopean axis, the required eye movement will be symmetrical with the two eyes turning equally inward or outward. When such “pure vergence stimuli” are used only a “pure vergence movement” is required, yet almost all responses include saccadic eye movements, a rapid tandem movement of the eyes. When saccades occur, they must either produce an error in the desired symmetrical response or correct an error from an asymmetrical vergence response. A series of eye movement responses to pure convergence stimuli (4.0 deg step stimuli) were measured in 12 subjects and the occurrence, timing and amplitude of saccades was measured. Early saccades (within 400 msec of the stimulus onset) appeared in 80% to 100% of the responses. In most subjects, the first saccade increased the asymmetry of the response, taking the eyes away from the midline position. In three subjects, these asymmetry-inducing saccades brought one eye, the preferred or dominant eye, close to the target, but in the other subjects these asymmetry-inducing saccades were probably due to the distraction caused by the transient diplopic image generated by a pure vergence stimulus. While many of these asymmetry-inducing saccades showed saccade-like enhancements of vergence, they were, with the exception of two subjects, primarily divergent and did not facilitate the ongoing convergence movement. All subjects had some responses where the first saccade improved response symmetry, correcting an asymmetry brought about by unequal vergence movements in the two eyes. In five subjects, large symmetry-inducing saccades corrected an asymmetrical vergence response, bringing the eyes back to the midline (to within a few tenths of a degree).

Eye-Movement Responses to Disparity Vergence Stimuli with Artificial Monocular Scotomas

The effects of artificial monocular scotomas on eye-movement responses to horizontal disparity vergence stimuli were studied in six subjects with normal binocular vision. Subjects viewed stereoscopic 1.5° horizontal step disparity vergence stimuli through liquid crystal shutter glasses. The central portion of the stimulus presented to the right eye was removed to simulate monocular artificial scotomas of variable diameters (2° to 10°). Eye movements were recorded with a binocular head-mounted eye tracker. Responses included pure vergence, vergence followed by saccades, and pure saccadic eye movements. The rate of responses with saccadic eye movements increased with the diameter of the artificial scotoma (p < 0.0001); there was an increase in the rate of responses starting with saccades (p < 0.0001), as well as an increase in the rate of saccades after initial vergence responses (p < 0.01). The probability of saccades after initial vergence responses was affected by the open-loop gain of the vergence response (p < 0.001). The open-loop gain decreased with increased diameters of the artificial scotomas (p < 0.0001). As the diameter of the artificial scotomas increased, the amplitude of the initial vergence eye-movement responses decreased, and the prevalence of saccadic eye movements and asymmetric vergence increased. The effects of the diameter of artificial monocular scotomas on eye-movement responses in subjects with normal binocular vision are consistent with the effects of diameter of suppression scotomas on eye-movement responses to disparity vergence stimuli in patients with infantile esotropia.

Symmetrical horizontal vergence contributes to the asymmetrical pursuit of targets in depth

When a target travels slowly and smoothly along the line of sight of one eye, the eye that is aligned with the target remains stationary while the other eye adducts. The mechanism that is commonly invoked is that commands signaling conjugate pursuit and symmetrical vergence are combined. The two signals are in the same direction in the adducting eye but are in the opposite direction in the stationary eye and, so, cancel. Recent data have challenged this view and the idea that the two eyes are controlled independently has been resurrected. Pursuit and vergence movements are difficult to separate when they occur together because they have similar latencies and dynamics. We have developed a method where horizontal vergence is “tagged” by training it to have a vertical vergence component that can then be identified in combined pursuit–vergence movements. Four subjects trained eye movements to have a vertical vergence component by fusing vertical disparities that varied in association with horizontal convergence. Following training, the vertical vergence aftereffect was found whenever horizontal vergence was stimulated regardless of whether the horizontal vergence resulted from movement of the target in the midsagittal plane (symmetrical vergence) or from movement of the target along the line of sight of one eye (asymmetrical vergence). The vertical vergence aftereffect was never observed in association with conjugate movements indicating that asymmetrical slow eye movements are not controlled monocularly but contain a vergence component along with symmetrical smooth pursuit.

Effects of localized lesions in the lateral suprasylvian cortex on convergence eye movement in cats

We evaluated the effects of electrolytic lesions in the extrastriate cortical area on the amplitudes and velocities of vergence eye movements in six alert cats that were trained to track a target moving in depth. Bilateral or unilateral lesions in the lateral suprasylvian (LS) cortex reduced the amplitudes and velocities of vergence eye movements, but the positive correlation between them was maintained. Furthermore, unilateral lesions changed the symmetry of eye movements. Movements of the left eye were decreased by lesions in the right LS cortex, resulting in asymmetric vergence eye movement with right eye predominance, and vice versa. These results support the hypothesis that the LS cortex plays an essential role in controlling vergence eye movement.

Instability of torsion during smooth asymmetric vergence.

Several categories of torsional eye movements obey Listing's law; however, systematic deviations from this law occur during vergence. Two kinematic models attempt to incorporate these deviations, both of which are supported by experimental evidence; however, they lead to different torsion predictions. These discrepancies have been explained in terms of experimental procedures, but it now seems likely from several recent studies that individual differences in torsion patterns may also be important. This study therefore examines the variation of torsion during a smooth asymmetric vergence task in which a fixation target was moved along the line-of-sight of the right eye at 15 degrees elevation; each of five subjects observed five trials of both inward and outward target motion, repeated in two sessions several weeks apart. There were no significant group differences in left or right eye torsion between trials or sessions, suggesting that monocular torsion patterns were relatively stable over time. When examined more closely, however, the torsion patterns shown by some individuals did vary for inward versus outward target motion. Hence, monocular torsion was idiosyncratic and depended on the direction in which fixation was changing (convergence or divergence). In a binocular analysis, cycloversion varied dramatically between subjects and depended on the direction of target motion; however, this was not the case for cyclovergence. In summary, cyclovergence is relatively stable and depends on where the eyes are looking, whereas cycloversion (and hence monocular torsion) is relatively unstable and depends on how they came to be in that particular horizontal and vertical orientation. These findings help to explain the controversy surrounding the torsional behaviour of the human eye during vergence.

Evidence Suggesting Individual Ocular Motor Control of Each Eye (Muscle)

Current models of the ocular motor system are usually presented in their most reduced form, are unilateral in architecture, and precise yoking is presumed. Although this simplifies the models, it does not accurately simulate the actual neuroanatomy and limits the models to simple, stereotyped responses. Studies of normal humans and monkeys have demonstrated striking disconjugacies in normal responses. Normal saccades may be disconjugate, or 1 eye may exhibit a dynamic overshoot. Asymmetric vergence can result in disconjugate saccades, unequal magnification spectacles cause differential saccadic gain adjustment, and saccades to unequal disparities also cause unequal saccades in the 2 eyes. In strabismus, deviated eyes typically do not mimic the movements of the fixating eye nor do their latent or congenital nystagmus waveforms duplicate those of the fixating eye. In spasmus nutans, each eye oscillates independently of the other. In achiasmatic dogs, uni-ocular saccades and uni-ocular nystagmus waveforms are seen; the same may be true in human achiasma. These data from both normals and those with abnormalities suggest that current models for ocular motor control are inadequate representations of the actual system. The inability of unilateral, yoked control (or even bilateral, yoked control) system models to duplicate the ocular motor responses of binocular mammals suggests that their ocular motor systems evolved from the bilateral, independent control systems seen in chameleons. One need only postulate a yoking overlay superimposed on two independent control systems to achieve conjugacy (bilateral, yoked, independent control) of the eyes. Abnormalities producing grossly disconjugate eye movements may then be simulated using the independent control of each eye released by a deficiency in the yoking overlay. Independent control of each eye coupled with the essential bilateral brain stem architecture implies that each individual muscle is driven by independent populations of neurons (burst cells, neural integrator cells, etc.). The agonist muscles of each eye are usually coordinated (yoked) but may function independently if the task dictates or if binocularity did not develop. Models based on the above architecture would be robust and could duplicate the many responses (both normal and abnormal) possible from the neurophysiological system.

Binocular eye orientation during fixations: Listing's law extended to include eye vergence

Any eye position can be reached from a position called the primary position by rotation about a single axis. Listing's law states that for targets at optical infinity all rotation axes form a plane; the so-called Listing plane. Listing's law is not valid for fixation of nearby targets. To document these deviations of Listing's law we studied binocular eye positions during fixations of point targets in the dark. We tested both symmetric (targets in a sagittal plane) and asymmetric vergence conditions. For upward fixation both eyes showed intorsion relative to the position that would have been taken if each eye followed Listing's law. For downward fixation we found extorsion. The in- or extorsion increased approximately linearly with the vergence angle. The direction of the Listing axis and the turn angle about this axis can be described by rotation vectors. Our observations indicate that for fixation of nearby targets the rotation vectors of the two eyes become different and are no longer located in a single plane. However, we find that it is possible to decompose the rotation vector of each eye into the sum of a symmetric and an anti-symmetric part, each with its own properties. (1) The symmetric part is associated with eye version. This component of the rotation vector is identical for both eyes and lies in Listing's plane. In contrast to the classical form of Listing's law, this part of the rotation vector lies in Listing's plane irrespective of the fixation distance. (2) The anti-symmetric part of the rotation vector is related to eye vergence. This component is of equal magnitude but oppositely directed in each eye. The anti-symmetric part lies in the mid-sagittal plane, also irrespective of fixation distance. For fixation of targets at optical infinity the anti-symmetric part equals zero and the eye positions obey the classical form of Listing's law. Thus, the symmetric and anti-symmetric parts of the rotation vectors are restricted to two perpendicular planes. Combining these restrictions in a model, with the additional restriction that the vertical vergence equals zero during fixation of point targets, we arrive at the prediction that the cyclovergence is proportional to the product of elevation and horizontal vergence angles. This was well born out by the data. The model allows to describe the binocular eye position for fixation of any target position in terms of the bipolar coordinates of the target only (i.e. using only three degrees of freedom instead of the six needed for two eyes).

奥行き方向の視線移動の年齢変化に関する検討

Changes in binocular eye movement occur when a subject changes his/her gaze point from a far/near to a near/far target, requiring both symmetric and asymmetric vergence. We measured these changes to investigate the effects of aging on vergence eye movement. Results indicated increases in the latency and time constants of vergence eye movement, decreases in convergence angle changes, and increases in the number of corrective saccades in subjects over 50 years, and increases in time constants in subjects below 10 years, compared with data for subjects between 10 and 50 years. This suggests that young and older subjects do not have the same vergence eye movement characteristics as those between 10 and 50 years. These differences should be considered in research about a subject's depth perception of stereoscopic images.

Effects of Asymmetric Vergence on Compensatory Eye Movements During Active Head Rotation1

The kinematics of the horizontal VOR for near fixation demand that VOR gain should change dependent on the target distance and the orientation of the head with respect to the target, or, equivalently, the amount of ocular vergence and the asymmetry of this vergence. Across two experiments, the gain of the VOR was measured in the right eye of humans who rotated their heads to the right or left while viewing a target placed either 22, 32.5 or 200 cm from the center of head rotation, in conditions with and without visual feedback. When tbe eye was in-line with the target, the measured VOR gain was up to 43% greater than when the eye was in an eccentric position. However, in the eccentric position, higher VOR gains were achieved with visual feedback of the target than without feedback, indicative of a visual component in the compensatory eye movement. Also, by changing the posture of the left eye but keeping the right eye constant, the VOR gain in the right eye was changed substantially during a subsequent head rotation. Hence, the positions of both eyes in their orbits determine the gain of the VOR in each eye.

Ocular vergence under natural conditions. II. Gaze shifts between real targets differing in distance and direction

Horizontal binocular eye movements of three subjects were recorded with the scleral sensor coil--revolving magnetic field technique during voluntary shifts of gaze between pairs of stationary, real, continuously visible targets. The target pairs were located either along the median plane (requiring symmetrical vergence), or on either side of the median plane (requiring asymmetrical vergence). Symmetrical vergence was primarily smooth, but it was often assisted by small, disjunctive saccades. Peak vergence speeds were very high; they increased from about 50 degrees s-1 for vergence changes of 5 degrees to between 150 and 200 degrees s-1 for vergence changes of 34 degrees. Differences between convergence and divergence were idiosyncratic. Asymmetrical vergence, requiring a vergence of 11 degrees combined with a version of 45 degrees, was largely saccadic. Unequal saccades mediated virtually all (95%) of the vergence required in the divergent direction, whereas 75% of the vergence required in the convergent direction was mediated by unequal saccades, with the remaining convergence mediated by smooth vergence, following completion of the saccades. Peak divergence speeds during these saccades were very high (180 degrees s-1 for a change of vergence of 11 degrees); much faster than the smooth, symmetrical vergence change of comparable size (14 degrees). Peak convergent saccadic speeds were about 20% lower. This difference in peak speed was caused by an initial, transient divergence, observed at the beginning of all horizontal saccades. The waveform of disjunctive saccades did not have the same shape as the waveform of conjugate saccades of similar size. The smaller saccade of the disjunctive pair was stretched out in time so as to have the same duration as its larger, companion saccade. These results permitted the conclusion that the subsystems controlling saccades and vergence are not independent. Vergence responses were relatively slow and incomplete with monocular viewing, which excluded disparity as a cue. Monocularly stimulated vergence decreased as a function of the increasing presbyopia of our three subjects. Subjects were able to generate some vergence in darkness towards previously seen and remembered targets. Such responses, however, were slow, irregular and evanescent. In conclusion, vergence shifts between targets, which provided all natural cues to distance, were fast and accurate; they appeared adequate to provide effective binocular vision under natural conditions. This result could not have been expected on the basis of previous observations, all of which had been made with severely reduced cues to depth.(ABSTRACT TRUNCATED AT 400 WORDS)

Dynamics of cover test eye movements.

The dynamics of unilateral cover test eye movements, never before systematically investigated with an objective recording system, are shown to be more complex than textbook accounts of them. We administered the cover test to nine heterophoric subjects by means of electromechanical occluders. Eye movements were recorded using the infrared photoelectric technique. Saccadic and vergence movements of the fixating eye were observed in almost all records when the occluded eye was uncovered. These movements were found in esophores and exophores and in both large and small phoria cases. Such movements were previously described in other asymmetric vergence tasks and appear to obey Hering's law of equal innervation. Uncovering the dominant eye, in cases of clear dominancy, resulted in shorter latency and larger amplitude saccades than did uncovering the nondominant eye. These large saccades were frequently of unequal amplitude in each eye. Trained subjects appear to use dynamic overshoots to increase this saccadic inequality and thereby attain vergence during saccades. Movements after the application of a cover to one eye, while grossly similar to textbook descriptions of them, are found to contain small vergence drifts and refixation (correcting) saccades in the nonoccluded eye.

Hering's law of equal innervation and vergence eye movement.

Hering's hypothesis concerning transverse eye movement states that each eye's movement is the sum of two types of component movement. In a purely formal way, the hypothesis can describe any binocular eye movement. However, a mathematical separation of version and vergence components says nothing about the validity of Hering's hypothesis in its empirical form. Accordingly, one must make explicit the empirical propositions that can be derived from the hypothesis. This paper discusses the formal and empirical aspects of the hypothesis and briefly reviews the relevant experimental evidence. Also discussed are accommodative vergence and asymmetrical vergence; it is argued that they do not necessarily violate Hering's law.

Mechanisms of Foveation in Asymmetric Vergence Eye Movements

Mechanisms of Foveation in Asymmetric Vergence Eye Movements