Static and dynamic properties of vergence-induced reduction of ocular counter-roll in near vision.

We have examined the characteristics of vergence-induced reduction of ocular counter-roll in near vision. Monkeys were trained to make convergent and divergent refixations with the head and body either upright or in various roll orientations. During near viewing requiring 17 degrees horizontal vergence, we found that static binocular torsion was suppressed by about 68% (averaged over both eyes, two monkeys and both near target locations). This result is in accordance with a previous study in which binocular torsion was quantified based on the displacement planes of eye positions in far and near viewing. Latency and duration of the change in torsional eye position depended (for each eye differently) on body roll and the depth plane of fixation. For instance, during convergent refixations in left-ear-down orientations, the latencies of the left eye were smaller and the durations were longer than those of the right eye. However, both eyes reached their final positions required to fixate the second visual target at roughly the same time. The different dynamics of the two eyes is explained by the fact that each eye rotated temporally when the eyes converged, a pattern named binocular extension of Listing's law. Coming from or aiming at a common torsional value (normal ocular counter-roll) in convergent or divergent refixations, the required torsion differs in the two eyes. The brain compensates for these differences by adjusting the dynamics of each eye's movement.

Direction specific error patterns during continuous tracking of the subjective visual vertical.

The aim of this study was to characterize the error pattern of continuously tracking the perceived earth-vertical during roll rotations from upright to right or left ear-down and from right or left ear-down to upright. We compared the tracking responses of two paradigms, which either continuously activated the otoliths organs alone (constant velocity tilt) or both the otolith organs and the semicircular canals (constant acceleration tilt). The tracking responses of the subjective visual vertical showed characteristic differences depending on starting position and tilt direction relative to gravity. The error patterns in the constant-velocity and constant-acceleration tilt paradigm were reversed. Estimations during tracking, when otolith information was continuously changing, were more precise compared to estimations following fast tilts to fixed roll tilt positions. We conclude that the central processing underlying these perceptual tracking responses requires, besides the otolith input, information from the vertical semicircular canals.

Common reference system for estimation of the postural and subjective visual vertical.

When tilted subjects are asked to set a luminous line to the perceived earth-vertical in a dark surrounding, they systematically underestimate the true direction of earth-vertical at large tilt angles, a phenomenon first described by Aubert (A-phenomenon). At small tilt angles, subjects usually overestimate the direction of earth-vertical. Overestimation has been first reported by Müller, who termed the notion of E-phenomenon. Since these first reports, this rather remarkable error behavior has been studied extensively. The prevailing notion in most earlier studies was that the erroneous estimation of verticality results from otolith signals, which are thought to represent the major input for spatial orientation, and their interaction with somatosensory signals. To bring the subjects into tilted positions, most investigators used slow tilt velocities or waited for some time to prevent interaction with semicircular canal activity. Here, we tested the hypothesis that vestibular cues about self-orientation relative to gravity are most reliable when both the semicircular canals and the otolith organs are optimally activated. To compare the error behavior in estimations of the visual vertical and perceived body position, we used self-controlled passive tilts at constant velocity or acceleration.

Reciprocal error behavior in estimated body position and subjective visual vertical.

This study investigated the reciprocal relation between estimation of body tilt and visual vertical by using self-controlled passive body tilts at constant velocity (slow tilts with no semicircular canal activation) or constant acceleration (rapid tilts with canal activation). In both conditions, the visual vertical was overestimated in the luminous line setting paradigm, whereas body tilt was underestimated in the position estimation paradigm. These errors were larger after slow than rapid tilts. During slow tilts, the range of actually reached positions was on average underestimated by about 25% with respect to the desired positions. Interestingly, there were no significant differences in the estimated positions for tilts in the roll and pitch plane. Most remarkably, in the range of +/-45 degrees the resulting means of position and luminous line setting errors of the velocity and acceleration paradigms as a function of the desired roll positions were close to zero. Furthermore, the resulting means of the two paradigms showed a high correlation in the tested range of +/-90 degrees. We conclude that: (a). the otoliths provide the main information for the spatial reference for both the estimation of body positions and the luminous line settings, at least in the range of about +/-45 degrees where the resulting mean errors between the two paradigms are close to zero, and (b). coactivation of semicircular canals improves the estimations.

Combined influence of vergence and eye position on three-dimensional vestibulo-ocular reflex in the monkey.

This study examined two kinematical features of the rotational vestibulo-ocular reflex (VOR) of the monkey in near vision. First, is there an effect of eye position on the axes of eye rotation during yaw, pitch and roll head rotations when the eyes are converged to fixate near targets? Second, do the three-dimensional positions of the left and right eye during yaw and roll head rotations obey the binocular extension of Listing's law (L2), showing eye position planes that rotate temporally by a quarter as far as the angle of horizontal vergence? Animals fixated near visual targets requiring 17 or 8.5 degrees vergence and placed at straight ahead, 20 degrees up, down, left, or right during yaw, pitch, and roll head rotations at 1 Hz. The 17 degrees vergence experiments were performed both with and without a structured visual background, the 8.5 degrees vergence experiments with a visual background only. A 40 degrees horizontal change in eye position never influenced the axis of eye rotation produced by the VOR during pitch head rotation. Eye position did not affect the VOR eye rotation axes, which stayed aligned with the yaw and roll head rotation axes, when torsional gain was high. If torsional gain was low, eccentric eye positions produced yaw and roll VOR eye rotation axes that tilted somewhat in the directions predicted by Listing's law, i.e., with or opposite to gaze during yaw or roll. These findings were seen in both visual conditions and in both vergence experiments. During yaw and roll head rotations with a 40 degrees vertical change in gaze, torsional eye position followed on average the prediction of L2: the left eye showed counterclockwise (ex-) torsion in down gaze and clockwise (in-) torsion in up gaze and vice versa for the right eye. In other words, the left and right eye's position plane rotated temporally by about a quarter of the horizontal vergence angle. Our results indicate that torsional gain is the central mechanism by which the brain adjusts the retinal image stabilizing function of the VOR both in far and near vision and the three dimensional eye positions during yaw and roll head rotations in near vision follow on average the predictions of L2, a kinematic pattern that is maintained by the saccadic/quick phase system.

Geometrical properties of three-dimensional binocular eye position in light sleep.

We examined three-dimensional binocular positions in the alert and sleepy monkeys. In contrast to the tightly yoked eye movements observed in alertness, the eyes were usually converged, vertically misaligned and had a much larger torsional variability during light sleep. While in alertness eye position vectors were confined to fronto-parallel planes, the corresponding planes were rotated temporally (e.g. leftward for the left eye) in light sleep. There was no correlation between temporal rotation of the eye position planes and horizontal vergence. All these observations can be explained by randomly innervated extraocular muscles that are rotating the two eyes about anatomically determined axes.

Spatial Organization of the Maculo-Ocular Reflex of the Rat: Responses During Off-Vertical Axis Rotation.

Pigmented, head restrained rats were rotated on a turntable about a tilted axis (off-vertical axis rotation; OVAR) in darkness. Evoked eye movements in the horizontal, vertical and torsional planes were recorded simultaneously with a dual search coil in a magnetic field, horizontal response components of both eyes were recorded with a coil on either eye. OVAR resulted in a persisting horizontal, unidirectional ocular nystagmus, compensatory in direction for the rotation of head in space. Superimposed upon this nystagmus were slower cyclic responses of the eye in the vertical and torsional movement planes, that were tightly phase locked with changing head positions in space: ocular depression/elevation with right ear up/down and ocular intorsion/extorsion with nose up/down. Simultaneous recordings of horizontal response components from both eyes revealed phase and gain differences between the horizontal movement components of both eyes, that resulted in a cyclic modulation of the vergence angle. Convergence of the lines of sight during nose up and divergence during nose down, adequate compensatory responses in light for changes in the viewing distance, were actually observed in darkness. Thus the utricular maculo-ocular reflex takes part of the visual consequences of a translational gaze shift into account. It reduces expected retinal disparities by appropriate and rapid vertical, torsional and vergence response components in the same way as canal-ocular reflexes 'compensate' for direction and velocity of expected retinal image slip during head rotation.