Saccade amplitude disconjugacy induced by aniseikonia: role of monocular depth cues

The conjugacy of saccades is rapidly modified if the images are made unequal for the two eyes. Disconjugacy persists even in the absence of disparity which indicates learning. Binocular visual disparity is a major cue to depth and is believed to drive the disconjugacy of saccades to aniseikonic images. The goal of the present study was to test whether monocular depth cues can also influence the disconjugacy of saccades. Three experiments were performed in which subjects were exposed for 15-20 min to a 10% image size inequality. Three different images were used: a grid that contained a single monocular depth cue strongly indicating a frontoparallel plane; a random-dot pattern that contained a less prominent monocular depth cue (absence of texture gradient) which also indicates the frontoparallel plane; and a complex image with several overlapping geometric forms that contained a variety of monocular depth cues. Saccades became disconjugate in all three experiments. The disconjugacy was larger and more persistent for the experiment using the random-dot pattern that had the least prominent monocular depth cues. The complex image which had a large variety of monocular depth cues produced the most variable and less persistent disconjugacy. We conclude that the monocular depth cues modulate the disconjugacy of saccades stimulated by the disparity of aniseikonic images.     

Fast disconjugate adaptations of saccades in microstrabismic subjects

In normal subjects, saccade amplitude inequality can be induced almost immediately when the image is made larger for one eye. This disconjugacy allows binocular fusion at the point of regard despite the image size inequality. It persists under subsequent monocular viewing which suggests a fast adaptive mechanism. This study tests whether such disconjugacy can be induced in subjects with microstrabismus who do not have foveal fusion. Three microstrabismic subjects viewed a random dot pattern the size of which was 10% larger in one eye. Within 40 sec horizontal saccades became larger in the eye viewing the larger image by 4–10%; the induced disconjugacy persisted under subsequent monocular viewing. Thus, fast disconjugate adaptation is possible in microstrabismus demonstrating that foveal fusion is not necessary to achieve it.     

Disconjugate adaptation of saccades: contribution of binocular and monocular mechanisms.

We studied the effects of prism-induced disparity on static and intrasaccadic alignment in six normal human subjects. A ten diopter base-out prism, calling for convergence, was placed in front of the central field of the right eye, so that at the center the eye viewed through the prism; at left and right, outside the prism. During 15 min of training, subjects made repetitive saccades solely in the right field of vision (C-R-C sequence). This paradigm required relative divergence for centrifugal (C-R) saccades and relative convergence for centripetal (R-C) saccades, as well as increase of the amplitude for all saccades made by the right eye. We found that during training, all subjects incorporated the necessary change in alignment into the saccades. After training the resultant intrasaccadic disconjugacy persisted when tested during monocular viewing, indicating that motor learning had occurred. Subjects demonstrated increased divergence for C-R and increased convergence for R-C saccades, in accordance with the change acquired during adaptation to the prism. In addition, five subjects developed increased divergence for C-L saccades, for which they did not train. Smaller and less consistent divergence was also observed for L-C saccades. Changes in intrasaccadic alignment were accompanied by changes in the relative velocities of the two eyes' saccades and slowing of the peak velocities in both eyes during training. Static alignment showed a general tendency toward convergence that did not parallel the changes in the intrasaccadic alignment, suggesting that saccade adaptation is system-specific. The pattern of transfer of the intrasaccadic disconjugacy to saccades in the untrained field and the changes in the relative speeds of the two eyes cannot be explained by monocular adjustment of the saccades. Our results indicate that both a binocular mechanism--saccade-vergence interaction--and monocular adaptation contribute to disconjugate adaptation of saccades.     

Disconjugate adaptation of vertical saccades in superior oblique palsy

Vertical eye movements along the midline were recorded in a patient with recent (1 month) right eye superior oblique muscle palsy. The patient showed severe right eye hypertropia and impairment of the yoking of the eyes during and after vertical saccades, particularly downward saccades. One month later, the right eye hypertropia was spontaneously reduced. Yoking of vertical saccades was also improved. To test whether a central adaptive mechanism could be responsible for the improvement of the yoking of vertical saccades, we tested the ability of the patient to adapt to optical aniseikonia, image size inequality. Vertical saccades developed disconjugacy that reduced the disparity of the aniseikonic images. Disconjugacy persisted for upward saccades, even under subsequent monocular viewing. This suggests a capacity for visually driven adaptation of saccade yoking that could be used to reduce the deficits caused by the paresis. Importantly, the disparity reducing oculomotor learning mechanism can function even when no bifoveal fusion can be obtained.     

Horizontal saccade disconjugacy in strabismic monkeys

PURPOSE: Previous studies have shown that binocular coordination during saccadic eye movement is affected in humans with large strabismus. The purpose of this study was to examine the conjugacy of saccadic eye movements in monkeys with sensory strabismus. METHODS: The authors recorded binocular eye movements in four strabismic monkeys and one unaffected monkey. Strabismus was induced by first occluding one eye for 24 hours, switching the occluder to the fellow eye for the next 24 hours, and repeating this pattern of daily alternating monocular occlusion for the first 4 to 6 months of life. Horizontal saccades were measured during monocular viewing when the animals were 2 to 3 years of age. RESULTS: Horizontal saccade testing during monocular viewing showed that the amplitude of saccades in the nonviewing eye was usually different from that in the viewing eye (saccade disconjugacy). The amount of saccade disconjugacy varied among animals as a function of the degree of ocular misalignment as measured in primary gaze. Saccade disconjugacy also increased with eccentric orbital positions of the nonviewing eye. If the saccade disconjugacy was large, there was an immediate postsaccadic drift for less than 200 ms. The control animal showed none of these effects. CONCLUSIONS: As do humans with large strabismus, strabismic monkey display disconjugate saccadic eye movements. Saccade disconjugacy varies with orbital position and increases as a function of ocular misalignment as measured in primary gaze. This type of sensory-induced strabismus serves as a useful animal model to investigate the neural or mechanical factors responsible for saccade disconjugacy observed in humans with strabismus.     

Role of attention and eye preference in the binocular coordination of saccades in strabismus

This study examines squint change and the binocular coordination of horizontal and vertical saccades in an adult subject with incomitant strabismus (20 or 40 prism diopters) strongly depending on the eye used for fixating. The patient had no binocular vision and was diagnosed ‘horror fusionis’ since her childhood. We found the angle of horizontal squint to be smaller when the patient was fixating with the preferred eye than with the nonpreferred eye. The squint was smaller when both eyes viewed and one eye fixated attentionally than when the nonfixating eye was closed. This suggests the importance of binocular visual stimulation. We found no significant changes in the amplitude of the disconjugacy of the saccades. However, when the preferred, left eye fixated attentionally (under binocular viewing) or monocularly, the pattern of the disconjugacy changed: the majority of the saccades showed divergent disconjugacy. This pattern is qualitatively similar to that seen in normal subjects. In this patient, divergent disconjugacy helped to decrease the convergent squint at the end of the saccades. Interestingly, vertical squint was small and did not depend on viewing conditions. The binocular coordination of vertical saccades was almost normal, at least in the binocular viewing condition. We conclude that the visual input from both eyes allows a rudimentary binocular cooperation that helps to keep the squint small and renders disconjugacy of horizontal saccades strategically divergent to reduce temporally the squint.     

Disconjugate oculomotor learning caused by feeble image-size inequality: differences between secondary and tertiary positions

In order to examine the minimum value of image-size inequality capable of inducing lasting disconjugacy of the amplitude of saccades, six normal emmetropic subjects were exposed for 16 min to 2% image size inequality. Subjects were seated at 1 m in front of a screen where a random-dot pattern was projected and made saccades of 7.5 and 15 deg along the horizontal and vertical principal meridians and to tertiary positions in the upper and lower field. During the training period, compensatory disconjugacy of the amplitude of the saccades occurred for the principal horizontal and vertical meridians; such increased disconjugacy persisted after training, suggesting learning. In contrast, for horizontal saccades to or from tertiary positions made in the upper and lower field, no consistent changes in the disconjugacy occurred, either during training or after the training condition. In an additional experiment, three subjects read sequences of words with the 2% magnifier in front of their dominant eye: in such a task, horizontal saccades to or from tertiary positions at the upper or lower field showed appropriate and lasting disconjugacy for two of the three subjects. We conclude that even a 2% image size inequality stimulates oculomotor learning, leading to persistent disconjugacy of saccades. The small disparity created by the image-size inequality is thus compensated by the oculomotor system rather than tolerated by the sensory system (e.g. by enlarging the Panum's area).     

Disconjugate Adaptation of the Vertical Oculomotor System

Conjugate post-saccadic eye drift can be induced in normal humans if a visual pattern is made to drift after every saccade. This study examines the ability of normal humans to create disconjugate vertical post-saccadic drift. Identical fuseable patterns were presented dichoptically, one to each eye. At the end of each vertical saccade one pattern drifted up and the other down, by 5% of the saccade amplitude. Five subjects were trained for 2–3 hr. Eye movements were recorded with eye coils. Normal vertical saccades along the midline were remarkably conjugate and post-saccadic drift was minimal. Training produced only small disconjugate post-saccadic drift (0.14 deg) but substantial saccade amplitude disconjugacy (0.70 deg). For several subjects, the induced disconjugacies persisted even for saccades in the dark indicating that adaptive changes occurred in the binocular coordination of vertical saccades. Apparently vertical disparate post-saccadic retinal slip is not sufficient to stimulate significantly the saccade pulse-step matching mechanism which is believed to control post-saccadic eye drift. The changes we observed aimed to reduce position disparity and not retinal slip in each eye. Copyright © 1996 Elsevier Science Ltd.     

Transient torsion during and after saccades

In five normal subjects, we analyzed uncalled for torsion (blips) during and after horizontal and vertical saccades. Torsion was defined as movement out of Listing's plane. During horizontal saccades in downward gaze the abducting eye extorted and the adducting eye intorted. The direction of the blips reversed in upward gaze. Peak torsional amplitudes (up to 1–2 deg) were always reached during saccades; drifts back to Listing's plane outlasted the saccades. Torsion of the extorting eye was larger than that of the intorting eye, producing a transient positive cyclovergence. Torsion and cyclovergence evoked by vertical saccades were also stereotyped in each eye, but showed idiosyncratic differences among subjects. We conclude that Listing's law is violated during saccades. Transient saccade-evoked torsion might reflect properties of the three-dimensional velocity-to-position integrator and/or the ocular plant.     

Vergence errors: some hitherto unreported aspects of fixation disparity.

Measurement of the monocular components of fixation disparity indicated a higher prevalence of asymmetric contributions to the total deviation than previously reported. Furthermore, the exact proportion varied from moment to moment. Two of six subjects showed significant changes in fixation disparity over a period of 1 week. For all six subjects the changes in fixation deviation of one eye were virtually independent of those changes occurring in the other eye. In other words, these monocular variances were uncorrelated. Settings of the monocular components of binocular fixation disparity were accomplished at an accuracy close to that achieved by using a monocular vernier technique. The remaining differences appeared to be due to occasional instabilities during binocular viewing. The usual method of clinical measurement in which only one element is moved is not always equivalent to that determined by summing the two monocular components. The principal process measured by subjective fixation disparity appears to be either oculomotor or localized directional shifts of a monocular nature.     

The role of (micro)saccades and blinks in perceptual bi-stability from slant rivalry

We exposed the visual system to an ambiguous 3D slant rivalry stimulus consisting of a grid for which monocular (perspective) and binocular (disparity) cues independently specified a slant about a horizontal axis. When those cues specified similar slants, observers perceived a single slant. When the difference between the specified slants was large, observers alternatively perceived a perspective- or a disparity-dominated slant. Eye movement measurements revealed that there was no positive correlation between a perceptual flip and both saccades (microsaccades as well as larger saccades) and blinks that occurred prior to a perceptual flip. We also found that changes in horizontal vergence were not responsible for perceptual flips. Thus, eye movements were not essential to flip from one percept to the other. After the moment of a perceptual flip the occurrence probabilities of both saccades and blinks were reduced. The reduced probability of saccades mainly occurred for larger voluntary saccades, rather than for involuntary microsaccades. We suggest that the reduced probability of voluntary saccades reflects a reset of saccade planning.     

Saccadic binocular coordination in alternating exotropia.

We studied the coordination of binocular eye movements in human subjects with alternating exotropia (divergent strabismus). Binocular saccades were recorded in six subjects during binocular and monocular viewing. Subjects were instructed to make saccades between two continuously lit targets (LED's) presented in an isovergence array (with the straight-ahead target 130 cm from the eyes) in a dimly lit room. For saccades up to 20 degrees amplitude, there were no large differences in the dynamics of the saccades between control and exotropic subjects. However, for larger amplitudes subjects frequently alternated the eye of fixation during saccades. That is, subjects fixated the left target with the left eye and the right target with the right eye. The alternation in eye fixation at the end of the saccade was taken into account in the programming of the saccades. The amplitudes of the alternating saccades were approximately equal to the target amplitude minus the strabismus angle. We conclude that for those saccades where alternation occurs, there is not only a change in the eye of fixation, but also a change in the target representation provided by either eye. Thus, in this group of strabismic patients, saccades may be programmed in a retina-centered coordinate system, if we assume that for making a saccade to a new target in the contralateral visual field its representation on the temporal retinal field of the currently fixating eye is suppressed and the retinotopic target information is derived from the non-fixating eye. In executing the saccade, the non-fixating eye automatically becomes the fixating eye.     

Long-term nonconjugate adaptation of human saccades to anisometropic spectacles.

It is generally believed that saccades follow Hering's law in the sense that they are equally large in the two eyes. We demonstrated that saccades are different in size in the two eyes in 8 habitual wearers of anisometropic spectacles, which have lenses of different refractive powers, and therefore supply each eye with a differently sized visual image. The eye provided with the larger visual image made larger saccades than its fellow eye. This nonconjugate adaptation was almost complete for both horizontal and vertical saccades. Post-saccadic drift was also asymmetrically adapted: it reduced any fixation-disparity present at saccadic offset. The nonconjugate adaptation was also expressed in smooth-pursuit eye movements. In addition, these nonconjugate adaptations were present during monocular viewing, which shows that they were hard-programmed.     

Alfred Bielschowsky (1871-1940) A life for strabismology

Purpose The purpose of the present study was to accurately document the oculomotor misalignments and instabilities associated with the non-decussating retinal-fugal fiber syndrome, a rare inborn, isolated, achiasmatic condition. 1–3 To date, the achiasmatic syndrome described has thus far been identified in three unrelated females. 1–4 A comparable achiasmatic condition has also been identified in a canine breed. 5,6 Materials and Methods The unique, inborn visual pathway malformation in the form of an isolated absence of the optic chiasm was confirmed by metabolic assay, the visual evoked potential (VEP) misrouting paradigm and neuroradiological evaluation, including magnetic resonance imaging (MRI). Horizontal and vertical, left and right eye, oculomotor scleral search coil recordings were measured, in one of the achiasmats, at 15 years of age. Comparable oculomotor recordings were implemented in three controls, including a normal age-matched control, an adult control and an adult with idiopathic congenital nystagmus (CN). In addition to central and eccentric target fixation with binocular and monocular viewing, binocular and monocular pursuit and optokinetic nystagmus (OKN) also were recorded. Results Following a binocular and monocular fixation paradigm, classic congenital nystagmus (CN) profiles were recorded in the achiasmat in the horizontal planes together with see-saw nystagmus (SSN) in the vertical planes; an alternating esotropia and vertical tropias also were documented. The CN showed interocular conjugacy and waveforms typically exhibited well-defined foveation periods. In general, both achiasmatic horizontal and vertical eye movements as well as corresponding interocular misalignments varied with stimu-lus and recording conditions. Moreover, horizontal eye movements showed sustained interocular conjugacy while vertical eye movements typically showed disconjugacy. Previous oculomotor studies in the achiasmatic canine breed revealed comparable oculomotor instabilities, albeit the latter were reported to present primarily with unyoked eye movements and uniocular saccades. In the present study, in addition to target fixation with binocular and monocular viewing, binocular and monocular pursuit and OKN responses also were recorded. For the achiasmat, high-gain pursuit results, as with eccentric fixation, emphasized a preference for fixation with the adducting eye. Also at eccentric gaze with monocular viewing, the eye under cover showed, relative to the fixating eye, a hypodeviation concomitant with adduction and a hyperdeviation concomitant with abduction. OKN profiles in the achiasmat with stimuli presented under both normal viewing and open-loop, retinal-field locked conditions proved rather complex; however, when an OKN response was identified, reversed OKN tracking was not apparent. Conclusions In general, the oculomotor results reported herein demonstrate that the non-decussating retinal-fugal fiber syndrome is an afferent visual pathway disorder associated with vertical and horizontal misalignments concurrent with congenital nystagmus and also with the rarer see-saw nystagmus.     

Short-term nonconjugate adaptation of human saccades to anisometropic spectacles.

It has been demonstrated before that the long-term wearing of anisometropic spectacles may induce nonconjugate adaptations of saccades. Saccades then become different in size in the two eyes. We examined the time-course and the limits of such adaptations of horizontal and vertical saccades during the short-term (1-6 hr) wearing of anisometropic spectacles. After only 1 hr of conditioning to 2 D of anisometropia, the nonconjugate size-adaptations were almost complete along the horizontal meridian. For progressively larger anisometropias (up to 8 D) the adaptative nonconjugacies after 1 hr became also systematically larger. An anisometropia larger than 6 D did not further increase the rate of adaptation during the first 6 hr of conditioning, which suggests that about 6 D of difference in spectacle correction, causing size differences of about 12%, may be the upper limit of the nonconjugate adaptive range of the saccadic subsystem. Post-saccadic drift of horizontal saccades was also adequately changed. In addition, nonconjugate adaptations had developed in smooth-pursuit eye movements. All of these plastic changes persisted during monocular viewing, indicating that the basic programming of these eye movements was changed.     

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.     

Binocular coordination of saccades in children with strabismus before and after surgery

PURPOSE: To examine the quality of binocular coordination of saccades in children with various types of strabismus and the effect of strabismus surgery. METHODS: Eight subjects were tested (5-15 years old): five with convergent strabismus, three with divergent strabismus. A standard saccade paradigm was used to elicit horizontal saccades to target LEDs (5 degrees to 15 degrees ). Saccades from both eyes were recorded simultaneously with the photograph-electric Skalar IRIS device (Delft, The Netherlands). This task was run before and about 3 weeks after strabismus surgery. RESULTS: Before surgery, the difference in the amplitude of the saccade between the left eye and the right eye was larger (15% of the saccade size) than in normal children of similar age. After strabismus surgery for all subjects the squint angle was reduced, and the amplitude of the disconjugacy of saccades decreased significantly, dropping to normal values (6%). As in normal children, postsaccadic eye drift (both its conjugate and its disconjugate components) was small in amplitude. The difference compared with normal subjects was that disconjugate drift did not restore the disconjugacy of the saccade itself (e.g., in normal subjects drift is convergent when saccade disconjugacy is divergent and vice versa). Rather, disconjugate drift tended to drive the eyes toward static eye misalignment (e.g., the drift was mostly convergent for convergent strabismics and divergent for divergent strabismics). Surgery had no significant effect on either component of the drift. CONCLUSIONS: The improvement of the binocular coordination of the saccades could be due, at least partially, to central adaptive mechanisms rendered possible by surgical realignment of the eyes. Separate mechanisms control the binocular coordination of saccades and the alignment of the eyes during the postsaccadic fixation period.     

Binocularity during reading fixations: Properties of the minimum fixation disparity

The present study was based on the physiologically reasonable assumption that the binocular system aims for a reduction of fixation disparity during fixation and that the minimum amount of fixation disparity reflects the optimal binocular status. We measured eye movements (EyeLink II) of 18 participants, while they read 60 sentences from the Potsdam-Sentence-Corpus (PSC) at a viewing distance of 60 cm. The minimum fixation disparity was frequently reached directly after the post-saccadic drift, sometimes at the end of fixation and sometimes somewhere in between. Minimum fixation disparity was strongly influenced only by fixation position (within the sentence) while the amplitude of incoming saccade had a negligible effect. Moreover, the effect of fixation position on minimum fixation disparity was correlated with the individual ability to compensate for binocular disconjugacy (due to saccades) while fixating during reading. Generally, we found fixation disparity to be correlated between conditions of reading and fixating single targets, while the reading fixation disparity tended to be more crossed (eso).     

Changes in Listing's plane after sustained vertical fusion

PURPOSE: To determine whether prolonged fusion of an imposed vertical disparity leads to a change in the orientation of Listing's plane, even when measured during monocular viewing. METHODS: Four normal subjects (age range, 24-37 years) wore Fresnel prisms of increasing power for 72 hours to produce a final left-over-right disparity (range, 7-11 prism diopters [approximately 3.9 - 6.2 degrees]) that was still fusible. Eye movements were measured binocularly, using three-axis search coils, as subjects fixed on an array of light-emitting diodes (LEDs) arranged on a flat screen, 124 cm away. A regression was used to fit the data points to a plane (Listing's plane) during monocular and binocular viewing. From each planar fit, the horizontal and vertical components of primary position (the direction of gaze that is perpendicular to Listing's plane) were calculated. Baseline data were collected in the unadapted state, either just before or at least 4 days after wearing the prisms. RESULTS: After the period of viewing through the prisms, there was a change in vertical phoria (prism adaptation) ranging from 1.6 to 3.3. There was a significant (P < 0.01) shift of the relative orientation of the vertical component of primary position between the two eyes of 6.3 +/- 1.7 degrees (right eye value minus left eye, up being positive, each measured during monocular viewing). There was no consistent pattern of change in the horizontal component of primary position. CONCLUSIONS: Prolonged fusion of a vertical disparity is associated with a change in the orientation of Listing's plane that persists under monocular viewing. Possible mechanisms include phoria adaptation, the prolonged fusional effort itself, and the residual disparity that must be overcome by sensory mechanisms.     

Binocular coordination of saccades in Duane Retraction Syndrome

Disconjugate oculomotor adaptation is driven by the need to maintain binocular vision. Since binocular vision in Duane Retraction Syndrome (DRS) patients is normal in half of their horizontal field of gaze (i.e., sound-side of gaze), we wondered whether oculomotor adaptive capabilities are efficient despite such a severe impairment of eye motility towards the other half of the horizontal field of gaze (i.e., affected-side gaze). We compared properties of horizontal saccades of patients with congenital unilateral Duane Retraction Syndrome type I in binocular viewing and monocular viewing conditions by simultaneously recording both eyes with the search coil technique. Our results show a mismatch between the pulse and the step signal of the innervation for saccades. When tested in the affected eye viewing condition (sound eye covered), the eyes showed not only similarly-directed increases of the saccadic gain (pulse signal) in the two eyes but also disjunctive post-saccadic drifts (step signal). This behavior suggests that visuomotor errors presented only to the affected eye were transferred to the sound eye, producing conjugate changes of the saccadic command. The post-saccadic command remained unchanged, however, and controlled the final position of each eye separately. This suggests that monocular adaptation is possible only for the step of innervation (i.e., controlling the final eye position) but not for the pulse of innervation (i.e., controlling the saccadic gain), even though the peculiarity of unilateral DRS type I offers a clear advantage for separate pathways of control for the two eyes.