H. Collewijn

Binocular co-ordination of human horizontal saccadic eye movements

1. The binocular co‐ordination of human horizontal saccades was analysed for the first time systematically over the full oculomotor range with a precise and accurate scleral sensor coil technique. Effects of amplitude (1.25‐80 deg), direction (adduction vs. abduction and centrifugal vs. centripetal) and eccentricity (symmetrical about primary or between primary and secondary positions) were systematically investigated in three subjects). 2. To minimize extraneous effects of stimulus presentation on the programming of saccades, subjects were instructed to voluntarily change their gaze between two continuously visible targets. These were positioned on an iso‐vergence locus, and thus contained no stimulus for disjunctive eye movements. 3. Under these conditions the amplitudes of the primary saccades of the two eyes were remarkably accurate; undershooting of the target by about 0.5 deg (independent of amplitude in the range 10‐70 deg) was typical. This finding contrasts with the undershooting by about 10% described in the literature as characteristic for other stimulus conditions. 4. Saccadic peak velocities saturated at a mean asymptotic level of 502 +/‐ 32 (S.D.) deg/s for saccades of 40 deg and larger. The duration was linearly related to amplitude for saccades up to 50 deg; for saccades of larger sizes the duration increased progressively more steeply. Skewness values (acceleration time as a fraction of total saccadic duration) decreased from about 0.45 for saccades up to 10 deg to about 0.20 for saccades of 50 deg and larger. 5. Binocular saccades showed an abduction‐adduction asymmetry and were not well yoked dynamically. The saccades of the abducting eye consistently had a larger size, a higher peak velocity, a shorter duration and were more skewed than the concomitant adducting saccades of the fellow eye. As a result, the eyes diverged transiently by as much as 3 deg during horizontal saccades. 6. Saccades also showed a marked centrifugal‐centripetal asymmetry. Peak velocities of saccades towards the primary position were about 10% higher than peak velocities of corresponding centrifugal saccades. 7. These directional asymmetries were the main source of variability in the pool of saccades. In comparison, intra‐ and intersubject variability was minor in our sample. 8. Post‐saccadic drift consisted of a vergence and a version component. The vergence component of this drift was a continuation of the vergence movement occurring during saccades. The version component, generally smaller than the vergence component, was directed towards the target position.(ABSTRACT TRUNCATED AT 400 WORDS)

Human ocular counterroll: assessment of static and dynamic properties from electromagnetic scleral coil recordings

SummaryStatic and dynamic components of ocular counterroll as well as cyclorotatory optokinetic nystagmus were measured with a scleral search coil technique. Static counterroll compensated for about 10% of head roll when the head was tilted to steady positions up to 20 deg from the upright position. The dynamic component of counterroll, which occurs only while the head is moving, is much larger. It consists of smooth compensatory cyclorotation opposite to the head rotation, interrupted frequently by saccades moving in the same direction as the head. During voluntary sinusoidal head roll, cyclorotation compensated from 40% to more than 70% of the head motion. In the range 0.16 to 1.33 Hz, gain increased with frequency and with the amount of visual information. The lowest values were found in darkness. The gain increased in the presence of a visual fixation point and a further rise was induced by a structured visual pattern. Resetting saccades were made more frequently in the dark than in the light. These saccades were somewhat slower than typical horizontal saccades. Cyclorotatory optokinetic nystagmus could be induced by a patterned disk rotating around the visual axis. It was highly variable even within a same subject and had in general a very low gain (mean value about 0.03 for stimulus velocities up to 30 deg/s). It is concluded that cyclorotational slip velocity on the retina is considerably reduced by counterroll during roll of the head, although the residual cyclorotation after the head has reached a steady position is very small.

Direction-selective units in the rabbit's nucleus of the optic tract

A class of direction-selective (DS) units, histologically localized within the nucleus of the optic tract (NOT) was isolated in the rabbits pretectum. These units typically had a maintained discharge of 25-50 action potentials/sec and large receptive fields (up to 40 X 150 degrees) in the visual streak area of the contralateral eye. They were excited by a visual pattern moving in one direction and inhibited by motion in the opposite direction. The reactions were sustained. Excitatory and inhibitory acceptance angles were each 180 degrees. Most units were excited by anterior motion of the stimulus and reacted to a wide range of velocities (0.01-20 degrees/sec). Random checkerboard patterns (elements 0.8 degrees), grids of black and white stripes (1, 2 and 4 degrees wide) and single black and white edges were all effective, with a decreasing response magnitude in roughly this order. A stimulus area of 2 X 2 degrees was already effective; response increased with area and was maximal for 15 X 15 degrees and larger stimuli. Latency for visual stimulation was 60 +/- 10 (S.D.) msec, for electrical stimulation of the chiasm 2.2 +/- 0.3 (S.D.) msec. Synaptic latency and presynaptic conduction velocity were estimated at 0.7 msec and 13m/sec, respectively. A strong convergence of retinal DS fibers upon NOT units is postulated. Since most properties of NOT units are compatible with those of optokinetic nystagmus, and electrical stimulation of the NOT elicits vigorous nystagmus, these data suggest that these cells are the essential afferent link in the optokinetic reflex arc.

Human gaze stability in the horizontal, vertical and torsional direction during voluntary head movements, evaluated with a three-dimensional scleral induction coil technique

The stability of gaze in three dimensions (horizontal, vertical and torsion) was measured with a new type of scleral search coil in eight emmetropic observers. Subjects held the head still or oscillated it at 0.16-0.67 Hz (amplitude about 10 deg) in the horizontal, vertical or torsional plane while fixating a point target at optical infinity. Veridical gaze and head coordinates were calculated with full correction for non-linear goniometric relations and for cross-coupling artifacts due to misalignments of the coil on the eye. The amount of gaze instability in the horizontal and vertical direction was virtually identical. With the head still, in either of these directions the mean standard deviation of gaze position (inclusive saccades) was about 7 min arc; mean non-saccadic retinal image speeds were 20-30 min arc/sec. During head oscillation these values increased to about 16 min arc and 1 deg/sec; a mean of about 2.5% of the head motion remained uncorrected by the compensatory eye movements. These findings agree well with our earlier results for the horizontal plane; the effect of the corrections was relatively small because the adventitious cross-coupling of horizontal and vertical to torsional head movements proved to be usually smaller than 10%. However, the corrections were important when head torsion was deliberately produced. Gaze stability in the torsional plane was considerably inferior to that in the horizontal and vertical plane. With the head held still, the mean SD of torsional gaze position was about 17 min arc; mean torsional non-saccadic retinal image speed was about 46 min arc/sec. Gain of the torsional compensatory eye movements was frequency dependent and rose from about 0.26 in static conditions (0 Hz) to about 0.42 at 0.16 Hz and 0.64 at 0.67 Hz. Accordingly, position instability and speed of the retinal image in torsion were about an order of magnitude larger than in the horizontal and vertical direction.

Binocular retinal image motion during active head rotation.

Abstract Horizontal binocular eye and head movements of 4 human subjects were recorded by means of the sensor coil-rotating magnetic field technique while they actively rotated their heads about a vertical axis and maintained fixation on a distant target. The frequency and peak-to-peak amplitude of these rotations ranged from about 0.25 Hz to 5 Hz and 30° to 15′. Eye movement compensation of such head rotations was far from perfect and compensation was different in each eye. Average retinal image speed was on the order of 4 deg/sec within each eye and the speed of the changes in retinal image position between the eyes was on the order of 3 deg/sec. Vision, subjectively, remained fused, stable and clear. Attention is called to implications of these results for visual and oculomotor physiology.

Eye movements and stereopsis during dichoptic viewing of moving random-dot stereograms

The dynamic properties of the version and vergence system were studied in relation to stereopsis for movements of the whole visual scene. Large random-dot stereograms (30 X 30 deg arc), moving laterally, were viewed dichoptically by human subjects without a fixed visual frame of reference. Sinusoidal movements in counterphase of the two half-images constituting the stereogram induced sinusoidal ocular vergence movements. The gain of vergence depended on the frequency as well as the amplitude of stimulus movement, while the phase lag depended only on the frequency. Fusion and stereopsis were retained up to a maximal velocity of change in relative position of the two half-images between 6 and 13.5 deg/sec. Sinusoidal movement of one half-image while the other one remained stationary induced sinusoidal ocular version as well as vergence movements. For version gains were higher and phase lags were smaller than for vergence. At the retinal level, residual overall binocular disparities between the two half-images up to 2 deg arc were tolerated without loss of stereopsis. The presence of sinusoidally varying overall binocular disparities and ocular vergence movements without perception of motion in depth suggests that these variables are not adequate cues for perception of (change in) depth.

Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit

Abstract Approximately 25 per cent of the rabbits retinal ganglion cells are directionselective. These cells respond maximally to movement of a visual stimulus in a particular (“preferred”) direction. The class of direction-selective cells can be further subdivided into two groups; the “on-off” and “on-type” direction-selective cells. It has been suggested that the on-off cells may play a role in controlling the slow phase of optokinetic nystagmus. To test this hypothesis, we determined how the responses of directionselective cells, of both types, varied as a function of stimulus velocity. The stimulus was similar to those normally used to elicit nystagmus i.e. a continuous black and white striped grating. The velocity response curves for the direction-selective cells were compared to data on the open loop eye movement velocity of the slow phase of optokinetic nystagmus in rabbits. The results of this comparison indicate that the slow phase is primarily controlled by the on-type direction-selective cells with a secondary contribution from on-off cells at higher stimulus velocities.

Motion perception during dichoptic viewing of moving random-dot stereograms.

The relation between binocular and monocular motion perception was investigated. A random-dot stereogram (30 X 30 deg arc), containing a central figure seen in front of the background in stereoscopic vision, was viewed dichoptically by human subjects without a fixed visual frame of reference. The images seen by the right and left eye were moved laterally according to a triangular wave form, in counterphase, but with variable amplitude ratios. Under this condition only purely lateral movement and no motion in depth of the stereogram as a whole was perceived, while stereoscopic vision of the figure-background relation was maintained. The magnitude of the binocularly perceived lateral motion, signalled by manual tracking of the perceived displacement, equalled the algebraic mean of the monocular motion percepts. As a special case, when the two images forming the stereogram were moved with equal velocities but in opposite directions they were perceived as a completely stationary, fused image in stereoscopic depth. Only the addition of a stationary reference (a bar or grating seen by both eyes) resulted in the perception of motion in depth. We conclude that a visual frame of reference is essential for perception of motion in depth but not for perception of lateral movements. Moreover, it seems likely that not absolute binocular disparity (retinal locus differences) but relative binocular disparity (differences in angular distance between two or more corresponding features in the two retinal images) is a cue for perception of depth.

Compensatory eye movements during active and passive head movements: fast adaptation to changes in visual magnification.

Rotational eye and head movements were recorded with great precision with scleral and cranial search coils in a rotating magnetic field. Compensatory eye movements were recorded in light and darkness during active as well as passive head movements in the frequency range 0.33‐1.33 Hz. From the recorded, nominal gaze movements the effective gaze was reconstructed taking into account magnification or reduction factors of corrective spectacles. Effective gain was calculated as the ratio between the velocities of the effective corrective eye movements and the head movements. In the light, effective gain of compensatory eye movements during active head motion was mostly between 0.97 and 1.03. It was never precisely unity and differed systematically between subjects and between the two eyes of each subject. During passive head motion in the light, gain was lower by about 3% than during active motion. During active head movement in the dark, gain was mostly between 0.92 and 1.00; values were about 5% lower than during active motion in the light. During passive head movement in the dark, gain was about 13% lower than during active motion, and the variability of the oculomotor response increased. Adaptation of these base‐line conditions was induced by fitting the subjects with magnifying or reducing spectacles for periods of 40 min to 24 h. The largest required change in amplitude of eye movements was 36%. When active head movements were made, the amplitude of compensatory eye movements in the light as well as in the dark adjusted rapidly. Most of the adaptation of the vestibulo‐ocular reflex in the dark was completed in about 30 min. This rate is much faster than that found in previous experiments requiring larger adaptive changes. Differential adaptation to unequal demands for the two eyes proved to be very hard or impossible. In a mild conflict situation the system adjusted to an intermediate level, distributing the error symmetrically between the eyes. When the discrepancy was large, the adaptive process of both eyes was controlled by the one eye which provided the most meaningful information. It is concluded that the system generating compensatory eye movements performs best during active rather than passive head movements, and that adaptation to moderate changes in optimal gain are made very rapidly.

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° s-1 for vergence changes of 5° to between 150 and 200° s-1 for vergence changes of 34°. Differences between convergence and divergence were idiosyncratic. Asymmetrical vergence, requiring a vergence of 11° combined with a version of 45°, 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° s-1 for a change of vergence of 11°); much faster than the smooth, symmetrical vergence change of comparable size (14°). 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. We also found that asymmetric vergence was largely saccadic and conclude that the generation of saccades of unequal sizes in each of the eyes is a normal feature of oculomotor performance whenever gaze is shifted between targets that differ in distance as well as direction.