The latency of saccades,vergence, and combined eye movements in children and in adults

PURPOSE: To examine the latency of eye movements in three-dimensional space (saccade, vergence, and combined saccade-vergence) in children and adults. METHODS: Fifteen normal children (4.5-12 years of age) and 15 normal adults (22-44 years of age) were tested. A standard paradigm was used to elicit pure lateral saccades at far and close viewing distance, pure vergence (convergence and divergence), and saccade combined with vergence movements. Horizontal eye movements from both eyes were recorded simultaneously by the oculometer, a photoelectric device. RESULTS: The mean latency in saccades, vergence, and combined eye movements was longer in children than in adults; the variability of such latency values was also larger in children. There was a progressive decrease with age in mean latency. All latencies approached or reached adult levels at approximately 10 to 12 years of age. Latency of saccades at close viewing distance was shorter than that at far in both adults and children. Convergence latency was longer than divergence latency in adults and most of the children. Latency of components of combined movements was longer than that of corresponding pure movements. Children initiated combined movements by triggering the vergence component first, whereas adults did not show a dominant pattern. The percentage of synchronous start of the two components was significantly higher in adults. CONCLUSIONS: Saccade- and vergence-triggering mechanisms are distinct and mature progressively and in parallel with age. The capacity for synchronization of the two components of combined eye movements develops more slowly and remains below adult level, even at the age of 12 years.     

Latency of saccades, vergence, and combined movements in children with early onset convergent or divergent strabismus

The goal of this study was to examine latency of horizontal eye movements in the natural space (saccades, vergence, and combined saccade-vergence movements) in children with early onset convergent or divergent strabismus. Ten children were tested (8-11 years old): three with divergent strabismus, seven with convergent strabismus. A paradigm was used to elicit pure lateral saccades at far and near distance, pure vergence (convergence and divergence) and saccades combined with vergence movements. Horizontal eye movements from both eyes were recorded simultaneously by a photoelectric device (Oculometer, Dr. Bouis). The latency of saccades (at far and near distance), of vergence (convergence and divergence), and of combined movements greatly varies among subjects and has tendency to be longer than that observed in normal children of matched age, however, these differences reach significance in only a few cases. Children with divergent strabismus and residual gross binocular vision show abnormally longer vergence latencies than children with convergent strabismus without binocular vision. The initiation of combined movements does not show a dominant pattern, such as preceding vergence, as is found in normal children. Finally, strabismus surgery has no major effect on latencies. We conclude that there is no overall deficiency in latencies of eye movements in 3D space in children with early onset strabismus. Most likely, monocular visual input can be efficient as normal binocular vision for vergence movements. In a few subjects with divergent strabismus and fragile, intermittent binocular vision, latencies can be abnormally long, just because of the fragile binocular input and/or attention effort needs to use it. The absence of a pattern of initiation similar to normal children could be due to attention and fixation capabilities.     

Speed and accuracy of saccades, vergence and combined eye movements in subjects with strabismus before and after eye surgery

The purpose of the study was to examine spatio-temporal characteristics of horizontal eye movements in the natural space (saccade, vergence and combined movements) in young subjects with early onset convergent or divergent strabismus. Nine young subjects (8-20 years old) were tested: three with divergent strabismus, six with convergent strabismus. A standard paradigm was used to elicit pure horizontal saccades at far and at close viewing distance, pure vergence along the median plane (convergence and divergence) and saccades combined with vergence movements. Horizontal eye movements from both eyes were recorded by a photoelectric device. Eye movements were recorded before surgery, and, for the majority of the subjects, two times after surgery. Before surgery the accuracy of convergence and divergence movements in their pure or combined form was poor with respect to normal values. The mean velocity of convergence was also abnormally slow. Strabismus surgery improved significantly the accuracy of these types of eye movements. The speed of pure convergence and of divergence combined movements increased significantly after surgery. We concluded that poor vergence eye movement’s performance, particularly those found for convergence in strabismic subjects could be due to impairment in the central structures related to sensory disparity inputs. Adaptive mechanisms promoted by the realignment of the eyes could be at the origin of the improvement in the vergence performances observed in our subjects after strabismus eye surgery.     

Binocular eye movements during accommodative vergence

Binocular eye position was monitored by the photoelectric technique during accommodative vergence. Contrary to previous reports indicating that accommodative vergence was a uniocular phenomenon, without exception, binocular accommodative vergence movements were recorded. The total vergence amplitude in the viewing eye was reduced, on the average, by approximately 88% with respect to the vergence movement measured in the covered eye. Some saccadic eye movements that occurred during vergence movements were likewise reduced in amplitude in the viewing eye by up to 20%. Smooth eye movements were utilized to counteract the vergence movement in the viewing eye. This smooth movement alone, or in conjunction with a late saccade, returned the eye to the target and helped to maintain the retinal image of the target coincident with the foveal center for the duration of the accommodative vergence movement. Thus, there appears to be a fixation-holding mechanism which produced a general attenuation of both vergence and some saccadic movements in the viewing eye. Although this control strategy produced violations of Hering's law with respect to the magnitude of the movements in the eyes but not with respect to the direction of the movement, it was implemented in the interest of retaining the target within the sensitive foveal region.     

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 degrees 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 degrees to 10 degrees ). 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.     

Visual field defects for vergence eye movements and for stereomotion perception

An objective visual field can be mapped in terms of stimulus-induced eye movement. The authors used the scleral coil technique to record vergence and conjugate eye movements while stimulating different visual field locations with a 3 X 3 deg target whose image vergence was oscillated. For each of three subjects tested there was a visual field location where vergence eye movements were much weaker than in a control location of equal retinal eccentricity. On the other hand, conjugate eye movements driven from these two locations by lateral motion were similar. Field defects for ocular vergence coincided with regions in which oscillating retinal disparity failed to produce a sensation of motion in depth, although visual responses to static disparity were normal, and psychophysical thresholds for lateral motion showed no defect with either binocular or monocular viewing. It was concluded, therefore, that the perceptual stereomotion scotomata were not due to a monocular loss, but to a defective binocular interaction between motion signals from the left and right eyes, and that this defective interaction was specific for opposed rather than parallel motion in the two eyes. Furthermore, the visual loss was specific for motion rather than for position. The correlation between the field defects for ocular vergence and stereomotion perception leads the authors to suggest that the same defect in binocular interaction is responsible for both the eye movement and sensory abnormalities. Two candidate hypotheses are proposed: one is framed in terms of a single population, and the other in terms of two populations of cortical neurons.     

The variation of torsion with vergence and elevation

Two recently developed kinematic models of human eye movements predict systematic departures from Listing's law which are associated with changes in vergence. This vergence-dependent torsion t is proportional to elevation e and vergence v, that is t = kev/2. The proposed value for k is either 1 (Van Rijn, L. J., & Van den Berg, A. V. (1993). Vision Research, 33, 691-708) or 1/2 (Minken, A. W. H., Gielen, C. C. A. M., & Van Gisbergen, J. A. M. (1995). Vision Research, 35, 93-102). One implication of both models is that an eye with a constant fixation direction should exhibit systematic torsional variation during movements of the other eye. This paper therefore examines the torsion produced by moving a fixation target inwards and outwards along the line-of-sight of the right eye at five different viewing elevations (0, +/- 15 and +/- 30 degrees). In a monocular analysis, each eye generally showed intorsion during convergence at positive elevation angles, whereas extorsion occurred at negative elevations; the opposite was true during divergence. However, the torsion response was visibly different between the five subjects, and depended on the direction of target motion. In a binocular analysis, cycloversion (mean of left and right eye torsion) varied dramatically both between subjects and between convergence and divergence; however, cyclovergence (torsional difference) was much less variable. Least-squares methods were used to estimate the constant k from monocular torsion, yielding values between 0.2 and 1.0; however, corresponding estimates based on cyclovergence were all close to 1/2. These findings support suggestions that a binocular control system couples the three-dimensional movements of the eyes, and that an existing model of monocular torsion should be generalised to the binocular case.     

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.     

Dynamics of horizontal vergence movements: interaction with horizontal and vertical saccades and relation with monocular preferences

We studied the dynamics of pure vergence shifts and vergence shifts combined with vertical and horizontal saccades. It is known from earlier studies that horizontal saccades accelerate horizontal vergence. We wanted to obtain a more complete picture of the interactions between version and vergence. Therefore we studied pure version (horizontal and vertical), pure vergence (divergence and convergence) and combinations of both in five adult subjects with normal binocular vision and little phoria (< 5 degrees). The visual targets were LED's in isovergence arrays presented at two distances (35 and 130 cm) in a dimly lit room. Two targets were continuously lit during each trial and gaze-shifts were paced by a metronome. The two subjects with a strong monocular preference made vergence eye movements together with small horizontal saccades during pure vergence tasks. The other subjects, who did not have a strong monocular preference, made pure vergence movements (without saccades). These findings, suggest that monocular preferences influence the oculomotor strategy during vergence tasks. Vergence was facilitated by both horizontal and vertical saccades but vergence peak-velocity during horizontal saccades was higher than during vertical saccades.     

Disconjugate adaptation to long-standing, large-amplitude, spectacle-corrected anisometropia

A 12-yr-old anisometropic patient had worn corrective eyeglasses (right eye, -0.50 +1.50 x 125; LE, -9.75 +2.50 x 60) for 7 yr, and then changed to contact lenses. Eye movements were recorded before and after the change to contact lenses using binocular search coils. In habitual spectacle viewing, the patient showed disconjugate adaptation. During monocular viewing, for example, ocular alignment changed by as much as 4 degrees during a 20 degrees saccade. Also, during monocular viewing, with either eye, placing the spectacle lens in front of the eye caused an increase in the disconjugate adaptive response compared with viewing without lenses. This finding emphasizes the context specificity of adaptive responses. After switching to contact lenses, the patient still wore his spectacles for 20-40 min each day. Although there was little residual disconjugate adaptation for vertical saccades, he showed considerable adaptation for horizontal saccades, especially for gaze changes that required divergence. The persistence of a partial state of disconjugate adaptation allowed the patient to use immediate, disparity-induced, horizontal vergence to aid ocular alignment in either the contact-lens-viewing or the spectacle-viewing condition. A more complete reversion to conjugacy occurred after nine days of exclusive use of his contact lenses. Then, in a short-term experiment, two minutes of binocular viewing through the eyeglasses induced a considerable reversion toward the previous state of disconjugate adaptation (up to 1.25 degrees of vergence change during monocular viewing). Finally, the waveform of the adapted (to spectacles) intrasaccadic vergence change with monocular viewing was similar to the waveform of the unadapted intrasaccadic vergence change during binocular refixations between targets that required a combined saccade and vergence. This finding suggests a common mechanism for adaptation to spectacle-corrected anisometropia and for normal binocular vergence-saccade interactions.     

Dissociated vertical deviation and eye torsion: Relation to disparity-induced vertical vergence

We studied the relation between vertical eye movements and binocular torsion in five subjects with dissociated vertical deviation (DVD). During trials, subject viewed a well illuminated Snellen letter chart, with both eyes uncovered during 4 seconds, Subsequently, DVD was induced by covering one eye during 4 seconds. Finally, both eyes were uncovered during 4 seconds. Several trials were recorded for each subject and covered eye. Eye movements were measured with scleral coils. We found that in all subjects, the vertical divergence followed an exponential course with a time constant of 0.67 ± 0.14 seconds on average. In three of the five subjects this vertical divergence was associated with binocular torsion (cycloversion), partly, in the form of a cycloversional nystagmus. The time course of the vertical divergence as well as the direction and nystagmic nature of the cycloversion was similar to the behaviour that was previously observed in disparity induced vertical vergence in normal subjects. In two of the subjects, the torsion that was associated with the vertical divergence was monocular. Our results indicate that DVD and disparity induced vertical vergence share the same characteristics. In addition, they demonstrate that extorsion associated with the elevation in DVD possibly but not necessarily points at a dissociated torsional deviation.     

Version and vergence eye movements in humans: open-loop dynamics determined by monocular rather than binocular image speed

We examined the velocity dependence of the vergence and version eye movements elicited by motion stimuli that were symmetric or asymmetric at the two eyes. Movements of both eyes were recorded with the scleral search coil technique. Vergence was computed as the difference in the positions of the two eyes (left-right) and version was computed as the average position of the two eyes ((left+right)/2). Subjects faced a large tangent screen onto which two identical random-dot patterns were back-projected. Each pattern was viewed by one eye only using crossed-polarizers and its position was controlled by X/Y mirror galvanometers. Viewing was always binocular and horizontal velocity steps (range, 5-240 deg/s) were applied to one (asymmetric stimulus) or both (symmetric stimulus) patterns approximately 50 ms after a centering saccade. With the symmetric stimulus, the motion at the two eyes could be either in the opposite direction (eliciting vergence responses) or in the same direction (eliciting version responses). The asymmetric stimuli elicited both vergence and version. In all cases, minimum response latencies were very short (<90 ms). Velocity tuning curves (based on the changes in vergence and version over the time period, 90-140 ms) were all sigmoidal and peaked when the monocular (i.e., retinal) image velocities were 30-60 deg/s. The vergence (version) responses to symmetric stimuli were linearly related to the vergence (version) responses to asymmetric stimuli when expressed in terms of the monocular rather than the binocular image velocities. We conclude that the dynamical limits for both vergence and version are imposed in the monocular visual pathways, before the inputs from the two eyes are combined.     

Disordered vergence control in dyslexic children.

By means of a synoptophore vergence eye movements were recorded in dyslexic and normal children while they were attempting to track small targets moving in simulated depth. Of the dyslexic children 64% were unable to make proper vergence movements when macular sized fusion targets (2 1/2 degrees) were employed, but their vergence control was better for larger (7 degrees) targets. The normal readers and the remaining dyslexics showed normal vergence responses for both large and small moving fusion stimuli. The results suggest that many dyslexics suffer a disorder of visuomotor control and perception for stimuli falling on the macula; this may explain their characteristic visual problems when reading. Hence recording vergence eye movement responses to small moving fusion stimuli may be useful in the investigation and treatment of children with reading difficulties.     

Noise coupling between accommodation and accommodative vergence

For monocular viewing, the fluctuations in accommodative lens power in the frequency range ½−3 Hz were found to be considerably greater than those in accommodative vergence movements of the covered eye. Considering the close synkinesis between these motor responses for step changes or slow variations in accommodative stimulus, this finding is unexpected. This apparent lack of synkinesis is found to result mainly from the more rapid decrease in small signal linear gain with increasing frequency of the accommodative vergence system than of the accommodation system, rather than from some nonlinear phenomenon.     

On Pulfrich-illusion eye movements and accommodation vergence during visual pursuit

When the Pulfrich illusion is perceived with stationary fixation, and visual pursuit of the pendulum is then initiated, rapid vergence changes occur which correspond to the illusory elliptical path. During steady-state visual tracking of the illusion, however, the eyes move along a planar path without systematic changes in vergence. These latter pursuit movements with monocular filter involve large fixation disparities relative to unobstructed vision (0.5 degree to 1 degree divergence); hence, it is proposed that the planar tracking path probably results from strong dominance of the oculomotor system by stimuli from the unobstructed eye. During visual tracking with monocular filter and a target moving along a nonillusory elliptical path in depth, appropriate changes in vergence occur, but comparable vergence changes also arise when the target is fully hidden from one eye. This response apparently represents a superposition of accommodation vergence upon smooth pursuit movements; similar responses also occur during monocular tracking of a target moving around a circular path in depth.     

Properties of anticipatory vergence responses

PURPOSE: To characterize the dynamic properties of vergence eye movements made between near and far targets that were alternately illuminated with predictable timing. METHODS: Using the magnetic search coil technique, eye movements were measured in 10 normal subjects as they shifted their point of fixation between a near green LED and a distant red laser spot, both aligned on subjects' midlines. Targets were alternately illuminated every 1.25 sec. RESULTS: All subjects showed some anticipatory responses, consisting of vergence movements that preceded target jumps, accompanied by a small saccade. Group median anticipatory interval was 191 msec. Responses preceded target motion in 83% of divergence trials, and 70% of convergence trials. The velocities of both pre- and persaccadic components of anticipatory vergence responses were greater when the near target was positioned at 20-cm compared with at 36 cm. In control experiments, in which target presentation was unpredictable, vergence movements preceded stimuli in only approximately 2% of trials; for the group, vergence responses followed target presentation after a median interval of 183 msec. To determine whether anticipatory vergence movements depended on a memory of prior stimuli, trials were run in four subjects in which oddball stimuli required a different-sized vergence movement. Most responses to oddball stimuli were not significantly different from responses to the preceding stimuli. CONCLUSIONS: Anticipatory vergence movements occur commonly in response to predictable stimulus movements in depth, but uncommonly when the timing of stimulus presentation is not predictable. The speed of anticipatory vergence movements is affected by stimulus amplitude. Properties of these movements are influenced by prior vergence responses, indicating that they depend on working memory.     

Adaptation model of accommodation and vergence

Both accommodation and vergence have been shown to exhibit adaptation after extended near viewing. Normally, when the stimulus to accommodation is removed, the accommodation system returns rapidly towards its tonic position. However, if the stimulus is removed after an extended focusing effort, the decay is much slower. A similar effect can be observed in the vergence system. After prolonged wearing of horizontal prisms, blockage of one eye results in a much slower decay of the vergence output towards its tonic value. No previous models have been shown to simulate quantitatively these effects. An interactive dual-feedback model of accommodation and vergence was developed to simulate the adaptive behaviour found experimentally. The unique feature of the model is that the output of each controller drives a dynamic adaptive component whose output governs the time constant of the controller. The model was able to simulate the rapid and slow decays following short and long viewing intervals in each of the accommodative and vergence systems. It also simulated adaptation during alternate binocular and monocular viewing under the accommodation closed-loop condition. Thus, this model can serve as the basis for detailed quantitative evaluation of adaptive behaviour in the accommodation and vergence systems.     

Dynamic accommodative vergence components in binocular vision

Vergence eye movements are mediated by the coordinated activity of two major motor controllers with independent driving stimuli: retinal disparity and blur. Vergence eye movements produced by dynamic accommodative vergence under binocular viewing conditions support the hypothesis of independent controllers whose influences sum in motor processes, and suggest a neurological strategy which enhances stability without sacrificing movement range or dynamics.     

Perspective vergence: oculomotor responses to line drawings

When a perspective drawing is viewed monocularly, changes in fixation point are accompanied by changes in steady-state vergence; their direction is usually appropriate for the distance relationships implied in the illustration. The absolute magnitude of these responses varies appreciably among subjects; it can be consistently enhanced or reduced by modest changes in the drawing. Similar configurations of stimuli from three-dimensional objects would presumably also contribute to normal vergence movements during binocular viewing; it appears that their importance would increase with target distance. Corresponding changes in pupil diameter, as expected for the "near reflex", were not observed with perspective stimuli. Consistent, directionally appropriate vergence changes, paralleling perception, were also made by most subjects during monocular viewing of a Necker cube, but there, exceptionally large pupillary responses arose.     

Dynamic asymmetries in convergence eye movements under natural viewing conditions

PURPOSE: To clarify differences in the dynamics of convergence eye movements in response to symmetrical stimuli between the dominant eye and the nondominant eye under natural viewing conditions. METHODS: This study was conducted in 11 normal volunteers (age range, 22-30 years). The subject was seated on a chair, and the head was fixed using a bite-block. The dominant eye was determined with the "hole-in-the-card" test. Horizontal positions of the eyes were recorded using an infrared reflection device. Recordings of right eye movements were subtracted from left eye movements to obtain the vergence response. The fixation target was moved toward the center of both eyes from 50 to 20 cm in front of the face at a constant velocity in five steps (20, 30, 40, 50, and 60 cm/s). The target was moved by a pulse motor controlled by a microcomputer. The dynamic properties of each eye movement and the vergence components were analyzed. RESULTS: At velocities < or =40 cm/s, convergence responses consisted of two components: the fusion-initiating component and the fusion-sustaining component. The fusion-initiating component drove the initial faster dynamic portion of the response, and the fusion-sustaining component maintained the latter slower dynamic portion of the response. The mean peak velocity of the fusion-initiating component was significantly greater in the dominant eye than in the nondominant eye. The mean peak latency of the catch-up component was significantly shorter in the dominant eye than in the nondominant eye. CONCLUSIONS: The present study indicated that the trajectory of convergence eye movement under natural viewing conditions consists of two components, the fusion-initiating component and the fusion-sustaining component, and that the convergence response to symmetric stimuli was asymmetric between the dominant eye and the nondominant eye during the fusion-initiating phase. The neural control system of convergence eye movements preferentially drives the dominant eye during the fusion-initiating phase of the response.