Vertical vergence in nonhuman primates depends on horizontal gaze position

ABSTRACT

The goal of this study was to compare vertical fusion capability at different orbital eye positions in normal nonhuman primates and attempt to use this information to isolate the extraocular muscles (EOMs) that mediate vertical vergence. Scleral search coils were used to record movements of both eyes as two normal nonhuman primates (M1, M2) performed a vertical vergence task at different horizontal eye positions. In a control experiment, M1 was also tested at different angles of horizontal vergence. To elicit vertical vergence, a 50° x 50° stimulus comprising a central fixation cross and random dots elsewhere was presented separately to each eye under dichoptic viewing conditions. Vertical disparity was introduced by slowly displacing the stimulus for one eye vertically. Vertical fusion amplitude (maximum disparity that the monkey was able to fuse) and vertical vergence (maximum difference in vertical position of the two eyes) were measured. Vertical fusion capability differed at different orbital eye positions. Monkey M1 had significantly smaller vertical fusion capabilities when the right eye (RE) was abducted than left eye (LE) while M2 had significantly smaller vertical fusion capabilities when the RE was adducted and LE abducted. M1 also showed greater vertical fusion capability for near gaze. M1 data suggested that the vertical recti mediated vertical vergence in the RE and the oblique muscles in the LE while M2 data suggested that the oblique muscles mediated vertical vergence in the RE and the vertical recti in the LE. The variable results within the same animal and across animals suggest that EOM involvement during vertical fusional vergence is idiosyncratic and likely a weighted combination of multiple cyclovertical muscles.     

Divergence limits within the field of vergence limits

The field of vergence limits has been defined as the binocular field of fixation that allows for a specified amount of vergence eye movements at its limits. Within this field, divergence amplitudes were measured in primary, secondary, and tertiary positions of gaze. Six subjects participated. It was found that divergence limits vary minimally with change in direction of gaze. The maximum amplitude of divergence was found 20 degrees below the primary straight ahead position.     

Two stages of programming eye gaze shifts in 3-D space

Accurate saccadic and vergence eye movements towards selected visual targets are fundamental to perceive the 3-D environment. Despite this importance, shifts in eye gaze are not always perfect given that they are frequently followed by small corrective eye movements. The oculomotor system receives distinct information from various visual cues that may cause incongruity in the planning of a gaze shift. To test this idea, we analyzed eye movements in humans performing a saccade task in a 3-D setting. We show that saccades and vergence movements towards peripheral targets are guided by monocular (perceptual) cues. Approximately 200 ms after the start of fixation at the perceived target, a fixational saccade corrected the eye positions to the physical target location. Our findings suggest that shifts in eye gaze occur in two phases; a large eye movement toward the perceived target location followed by a corrective saccade that directs the eyes to the physical target location.     

The effects of sustained vertical gaze deviation on the resting state of the vergence system

Vergence of the eyes in the dark depends on the vertical direction of gaze. In three experiments this phenomenon was studied using eye inclinations and head tilts of 5 min duration during which monocular or binocular near and distant stimuli were inspected. The effects of eye inclination and head tilt on dark vergence were temporally stable; they exhibited even a tendency to increase with the passage of time. On return to horizontal gaze, positive aftereffects were found, that is dark vergence was biased towards its value with a vertically deviated gaze. The effect of vertical gaze direction turned out to be additive to the effect of binocular near fixation. These findings represent evidence against the hypothesis that the effect of vertical gaze direction on dark vergence is mediated by a feedforward signal that is related to voluntary effort in raising or depressing the eyes.     

Plasticity of convergence-dependent variations of cyclovergence with vertical gaze.

Binocular alignment of foveal images is facilitated by cross-couplings of vergence eye movements with distance and direction of gaze. These couplings reduce horizontal, vertical and cyclodisparities at the fovea without using feedback from retinal image disparity. Horizontal vergence is coupled with accommodation. Vertical vergence that aligns tertiary targets in asymmetric convergence is thought to be coupled with convergence and horizontal gaze. Cyclovergence aligns the horizontal retinal meridians during gaze elevation in symmetrical convergence and is coupled with convergence and vertical gaze. The latter vergence-dependent changes of cyclovergence have been described in terms of the orientation of Listing's plane and have been referred to as the binocular extension of Listing's law. Can these couplings be modified? Plasticity has been demonstrated previously for two of the three dimensions of vergence (horizontal and vertical). The current study demonstrates that convergence-dependent changes of the orientation of Listing's plane can be adapted to either exaggerate or to reduce the cyclovergence that normally facilitates alignment of the horizontal meridians of the retinas with one another during gaze elevation in symmetrical convergence. The adaptability of cyclovergence demonstrates a neural mechanism that, in conjunction with the passive forces determined by biomechanical properties of the orbit, could play an active role in implementing Listing's extended law and provide a means for calibrating binocular eye alignment in three dimensions.     

Conjugate ocular oscillations during shifts of the direction and depth of visual fixation.

PURPOSE: To characterize dynamic properties of combined saccade-vergence eye movements that occur as the point of visual fixation is shifted between objects lying in different directions and at different depths. METHODS: Using the scleral search-coil technique, eye movements were measured in 10 normal subjects as they made voluntary, disjunctive gaze shifts comprising a range of saccades and vergence movements. RESULTS: By analyzing eye acceleration records, the authors identified small-amplitude (0.2-0.7 degrees), high-frequency (23-33 Hz), conjugate horizontal oscillations of the eyes during the vergence movement that followed the initial saccade. When the shift of the fixation point required a large vergence component (17 degrees , every subject showed these oscillations; they were present in approximately a third of responses. Approximately 5% of responses showed oscillations that had horizontal and vertical components. Oscillations were less prominent with shifts that had smaller vergence components and were absent after saccades made between targets located at optical infinity. CONCLUSIONS: These findings suggest that a common mechanism gates both the saccadic and vergence components of disjunctive gaze shifts, a likely candidate being the pontine omnipause neurons. When a saccade is immediately followed by a prolonged vergence movement, the omnipause neurons remain silent, leading to small-amplitude saccadic oscillations. Shifts in the point of visual fixation that require a large vergence movement may be a useful experimental strategy to induce saccadic oscillations.     

Fixation disparity,accommodation, dark vergence and dark focus during inclined gaze*

We investigated several oculomotor functions at different angles of vertical inclination of the gaze direction from 15 deg upwards to 45 deg downwards. The mean accommodative resting state (measured in a dark visual field) increased when the eyes or the head were declined from 0 to 45 deg. Fixation disparity (the vergence error in minutes of arc relative to the principle visual directions) became more eso when a fusion target at a viewing distance of 40 cm was lowered: declining the gaze by 45 deg changed mean fixation disparity by 1.8 min arc with eye inclination (keeping the head upright), and by 0.9 min arc with head inclination (with eye position unchanged relative to the head). When the eyes were lowered, the individual rate of eso change in fixation disparity was correlated with the amount of the subjects’ near shifts in the resting position of vergence, measured in darkness. Significant test-retest correlations between repeated measurements showed that the effects of eye inclination on vergence varied in a reproducible way among individuals with good binocular vision.     

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.     

Stereothresholds with simulated vergence variability and constant error

Stereothresholds are elevated by vergence constant error (fixation disparity), vergence noise, or both. This study investigated the separate and combined effects of simulated vergence constant error and variability on stereothresholds in four normal observers. Targets were 30 arc min bright vertical lines presented separately to the two eyes for 150 ms in darkness. Vergence constant error, simulated as a pedestal disparity, was induced by altering the screen positions of the stereo half-images relative to a previously visible binocular fixation point. Vergence variability was simulated simultaneously by disconjugate motion (amplitude=0-0.5 deg per eye; frequency=2 or 4 Hz) of a pair of scanning mirrors in a Wheatstone stereoscope that was used to present the images to each eye. Various combinations of pedestal disparity and simulated vergence variability produce equivalent stereothresholds whenever the calculated mean deviation (sigma/instantaneous vergence errors//N) of the stimulus from the fixation plane is the same. In particular, stereothresholds are optimal for mean deviations up to approximately 1.4 arc min and then increase according to a power function with an exponent of 0.61. The results imply that vergence constant errors and vergence variability impair stereothresholds because of the resulting mean deviation from the horopter.     

Rapid and slow-velocity vergence eye movements *

Previously we have measured rapid-velocity vergence responses to targets at different distances that provided no disparity or accommodative stimulation. To evaluate the possibility that this rapid-velocity vergence occurs during succades. the latencies or eye movement between two long dim luminous rods were compared under two conditions. Rapid-velocity vergence with an average latency of ≈300ms was elicited when subjects alternately viewed horizontal rods at distances of 38 and 78 cm, and with a vertical separation of 5.2°. Horizontal saccades with a comparable latency were measured when the rods were equidistant and oriented vertically. The correlation between the mean latencies of vergence and saccadic movements was 0.97, sugesting that the two movements occurred together. In a second experiment vegence responses were measured when the subject looked between u bright vertical line on a screen at 76cm and ii second pair of lines (vertically displaced between 0.15 and 3°) with crossed disparity to simulate a target al 38cm. Slow-velocity vergence often occurred alone when the vertical separation between targets was small: rapid-velocity vergence intruded when the separation between the targets was larger. The results can be accounted for if proximity and disparity stimulation act through a single vergence controller, the output of which produces slow- or rapid-velocity vergence depending upon whether the saccadic system is concurrently active.     

Rotation of Listing's plane during vergence.

When visually fixating targets on an isovergence surface, the position of each eye was constrained to a plane. Thus, Listing's law holds during vergence. The planes were, however, rotated temporally with respect to those when viewing distant targets. The effect of this rotation was to produce a torsion which depended on eye elevation; extorsion of the two eyes for downward gaze and intorsion for upward gaze. The saccadic velocity command was relatively unaffected during vergence. Computer simulations suggest that the saccadic tonic command and the vergence command interact multiplicatively in three dimensions.     

Temporal dynamics of ocular position dependence of the initial human vestibulo-ocular reflex

PURPOSE: While an ideal vestibulo-ocular reflex (VOR) generates ocular rotations compensatory for head motion, during visually guided movements, Listing's Law (LL) constrains the eye to rotational axes lying in Listing's Plane (LP). The present study was conducted to explore the recent proposal that the VOR's rotational axis is not collinear with the head's, but rather follows a time-dependent strategy intermediate between LL and an ideal VOR. METHODS: Binocular LPs were defined during visual fixation in eight normal humans. The VOR was evoked by a highly repeatable transient whole-body yaw rotation in darkness at a peak acceleration of 2800 deg/s2. Immediately before rotation, subjects regarded targets 15 or 500 cm distant located at eye level, 20 degrees up, or 20 degrees down. Eye and head responses were compared with LL predictions in the position and velocity domains. RESULTS: LP orientation varied both among subjects and between individual subject's eyes, and rotated temporally with convergence by 5 +/- 5 degrees (+/-SEM). In the position domain, the eye compensated for head displacement even when the head rotated out of LP. Even within the first 20 ms from onset of head rotation, the ocular velocity axis tilted relative to the head axis by 30% +/- 8% of vertical gaze position. Saccades increased this tilt. Regardless of vertical gaze position, the ocular rotation axis tilted backward 4 degrees farther in abduction than in adduction. There was also a binocular vertical eye velocity transient and lateral tilt of the ocular axis. CONCLUSIONS: These disconjugate, short-latency axis perturbations appear intrinsic to the VOR and may have neural or mechanical origins.     

Effect of monocular visual loss upon stability of gaze

Using the eye-coil/magnetic field method, we measured horizontal and vertical movements of both eyes in four patients with monocular loss of vision while they attempted steady, binocular fixation of a visual target. We also measured gaze stability in two normal subjects while they fixed upon a target monocularly, and in one patient with congenital, bilateral blindness. In the patients with monocular visual loss, gaze instability was greater in the blind eye, both vertically and horizontally, compared either with their seeing eye or with nonviewing eyes of control subjects. Gaze instability due to monocular blindness resulted from: (1) low-frequency, low-amplitude, bidirectional drifts that were more prominent vertically; and (2) unidirectional drifts, with nystagmus, that were more prominent in the horizontal plane. Gaze-evoked nystagmus, however, was not a feature of monocular blindness. Thus, the gaze instability of monocular blindness may reflect disruption of: (1) a monocular visual stabilization system; (2) fusional vergence mechanisms; or (3) both. In contrast, bilateral congenital blindness led to nystagmus with horizontal and vertical components and a wandering null point, indicative of an abnormal neural integrator.     

A new method for determining squint angle in primary and all secondary positions using the first and fourth Purkinje images

A new objective method is presented for measuring the squint angle in all gaze positions. While the subject fixates an object at a distance d, his eyes are illuminated one at a time from above or from the side with a collimated infrared beam. A high-sensitivity infrared camera observes the first and fourth Purkinje images from below. Camera and light source are mounted on the same holder, which can be turned around horizontal and vertical axes. The examiner turns the holder while observing the Purkinje images on a TV monitor until both images lie either on a vertical line (to measure a horizontal deviation) or on a horizontal line (to measure a vertical deviation). In either of these cases the direction of the incident light, which is determined by the position of the holder, and the direction of the optical axis of the eye coincide. Advantages of the method include: the angle between the optical axis and the fixation line can be easily determined; the subject does not have to fixate with both eyes; and the accuracy is +/- 1 degree.     

Direction of heading and vestibular control of binocular eye movements.

To optimize visual fixation on near targets against translational disturbances, the eyes must move in compliance with geometrical constraints that are related to the distance as well as the speed and direction relative to the target. It is often assumed that the oculomotor system uses the vestibular signals during such movements mainly to stabilize the foveal image irrespective of the peripheral vision. To test this hypothesis, trained rhesus monkeys were asked to maintain fixation on isovergence targets at different horizontal eccentricities during 10 Hz oscillations along different horizontal directions. We found that the two eyes moved in compliance with the geometrical constraints of the gaze-stabilization hypothesis, although response gains were generally small ( approximately 0.5). The best agreement with the gaze stabilization hypothesis occurred for heading directions within +/-30 degrees from straight-ahead, whereas lateral movements exhibited greater variability and larger directional errors that reflected the statistical response variability inherent in the non-linear dependence on heading direction. In contrast to undercompensatory version (conjugate) components, the disjunctive part of the response (vergence) exhibited unity or higher than unity gains. The high vergence gains might reflect a strategy that aims at maintaining the binocular coordination of the gaze lines despite the low gain of the version movements.     

Convergence reduces ocular counterroll (OCR) during static roll-tilt

When humans are roll-tilted around the naso-occipital axis, both eyes roll or tort in the opposite direction to roll-tilt, a phenomenon known as ocular counterroll (OCR). While the magnitude of OCR is primarily determined by vestibular, somatosensory, and proprioceptive input, direction of gaze also plays a major role. The aim of this study was to measure the interaction between some of these factors in the control of OCR. Videooculography was used to measure 3D eye position during maintained whole body (en bloc) static roll-tilt in darkness, while subjects fixated first on a distant (at 130 cm) and then a near (at 30 cm) head-fixed target aligned with the subject's midline. We found that while converging on the near target, human subjects displayed a significant reduction in OCR for both directions of roll-tilt--i.e. the interaction between OCR and vergence was not simple addition or subtraction of torsion induced by vergence with torsion induced by roll-tilt. To remove the possibility that the OCR reduction may be associated with the changed horizontal position of the eye in the orbit during symmetric convergence, we ran an experiment using asymmetric convergence in which the distant and near targets were aligned directly in front of one eye. We found the magnitude of OCR in this asymmetric convergence case was also reduced for near viewing by about the same amount as in the symmetric vergence condition, confirming that the convergence command rather than horizontal position of the eye underlies the OCR reduction, since there was no horizontal movement of the aligned eye in the orbit between fixation on the distant and near targets. Increasing vergence from 130 to 30 cm reduced OCR gain by around 35% on average. That reduction was equal in both eyes and occurred in both the symmetric and asymmetric convergence conditions. These results demonstrate the important role vergence plays in determining ocular counterroll during roll-tilt and may support the contention that vergence acts to reduce the conflict facing a stereopsis-generating mechanism.     

Ocular rotation axes during dynamic Bielschowsky head-tilt testing in unilateral trochlear nerve palsy

PURPOSE: To explain the positive Bielschowsky head-tilt (BHT) sign in unilateral trochlear nerve palsy (uTNP) by the kinematics of three-dimensional eye rotations. METHODS: Twelve patients with uTNP monocularly fixed on targets on a Hess screen were oscillated (+/- 35 degrees, 0.3 Hz) about the roll axis on a motorized turntable (dynamic BHT). Three-dimensional eye movements were recorded with dual search coils. Normal data were collected from 11 healthy subjects. RESULTS: The rotation axis of the viewing paretic or unaffected eye was nearly parallel to the line of sight. The rotation axis of the covered fellow eye, however, was tilted inward relative to the other axis. This convergence of axes increased with gaze toward the unaffected side. Over entire cycles of head roll, the rotation axis of either eye remained relatively stable in both the viewing and covered conditions. CONCLUSIONS: In patients with uTNP, circular gaze trajectories of the covered paretic or unaffected eye during dynamic BHT are a direct consequence of the nasal deviation of the rotation axis from the line of sight. This, in turn, is a geometrical result of decreased force by the superior oblique muscle (SO) of the covered paretic eye or, according to Hering's law, increased force parallel to the paretic SO in the covered unaffected eye. The horizontal incomitance of rotation axes along horizontal eye positions can be explained by the same mechanism.     

Variability of monocular visual acuity during binocular viewing.

Two patients observed changes in the visual acuity of one eye when both eyes were viewing simultaneously in certain directions of gaze. While viewing targets presented during the Turville Infinity Balance (TIB) test, the acuity of the affected or amblyopic eye improved when the nonamblyopic eye was covered and binocular vision suspended. The vision of the amblyopic eye was also improved when an appropriate prism was held in front of either eye. The direction of the prism base was based upon the interrelations of horizontal, vertical, and cyclotorsional anisophoria and the amount of prism was the minimum necessary to improve the vision in the amblyopic eye and neutralize vertical fixation disparity. The correlation of variable monocular acuity, stereopsis, and fixation disparity with oculomotor balance is recorded and discussed.     

Perception can influence the vergence responses associated with open-loop gaze shifts in 3D

We sought to determine if perceived depth can elicit vergence eye movements independent of binocular disparity. A flat surface in the frontal plane appears slanted about a vertical axis when the image in one eye is vertically compressed relative to the image in the other eye: the induced size effect (Ogle, 1938). We show that vergence eye movements accompany horizontal gaze shifts across such surfaces, consistent with the direction of the perceived slant, despite the absence of a horizontal disparity gradient. All images were extinguished during the gaze shifts so that eye movements were executed open-loop. We also used vertical compression of one eye's image to null the perceived slant resulting from prior horizontal compression of that image, and show that this reduces the vergence accompanying horizontal gaze shifts across the surface, even though the horizontal disparity is unchanged. When this last experiment was repeated using vertical expansions in place of the vertical compressions, the perceived slant was increased and so too was the vergence accompanying horizontal gaze shifts, although the horizontal disparity again remained unchanged. We estimate that the perceived depth accounted, on average, for 15-41% of the vergence in our experiments depending on the conditions.     

Changes in vestibulo-ocular reflex (VOR) anticipate changes in vergence angle in monkey.

The axis of head rotation is usually different from the axis of eye rotation. Geometrical considerations show that the eyes translate with respect to visual targets located near the head. In order to accurately stabilize retinal images against this translation, the vestibulo-ocular reflex (VOR) must be modulated inversely with the target's distance. The neural correlate of viewing distance used to modulate the VOR is not known. Since vergence angle is related inversely to viewing distance, an efference copy of instantaneous vergence angle or proprioceptive afferent information from extraocular muscles could be used to adjust the VOR. To examine this hypothesis, we compared the time-course of changes in the VOR with the time-course of changes in vergence angle. The VOR was induced by briefly rotating monkeys about a vertical axis at different times during the execution of vergence eye movements. We found that the amplitude of the VOR changed systematically during the course of a vergence eye movement. On average, the changes in the amplitude of vestibular induced eye movements anticipated changes in vergence angle by 50 msec, but in some instances, up to 200 msec of anticipation was observed. These data suggest that a central command signal rather than an afferent or efferent copy of vergence eye position was used to modulate the VOR.