Strabismic Subjects Research Articles

Binocular interactions in striate cortical neurons of cats reared with discordant visual inputs

The postnatal development of cortical binocularity is known to be adversely affected by early abnormal visual experience. However, little information exists on how the signals from the two eyes are combined in individual cortical neurons of animals reared with early discordant binocular visual experience. Since this is a fundamental issue in understanding visual cortical development, we used extracellular single-unit recording methods to study binocular integration in striate cortical neurons of strabismic cats. Specifically, we measured the sensitivity of individual cells to the relative interocular spatial phase of dichoptically presented drifting sinusoidal gratings (i.e., to binocular retinal image disparity). Clear alterations in ocular dominance were observed in all strabismic subjects. Nevertheless, the majority of cortical neurons exhibited some form of binocular interactions when both eyes were stimulated together. The most prominent aspect of cortical physiology in the strabismic animals was the relatively high prevalence of suppressive binocular interactions. Suppression was most frequently found in kittens reared with 2 weeks of early optical dissociation and among adult cats that received 2 weeks of early optical dissociation and a prolonged recovery period. However, substantial excitatory binocular interactions were also maintained in these animals. With an extended period of interocular misalignment (3 or 8 months), all forms of binocular interactions, excitatory and suppressive, were drastically reduced and a greater number of neurons were truly monocular. Although the reduction in the strength of binocular interactions occurred in all units irrespective of their monocular spatial properties, the effect was more pronounced among those units tuned to higher spatial frequencies and this spatial-frequency-dependent effect was larger in the subjects receiving longer periods of binocular dissociation. The results suggest that the "breakdown" of cortical binocular properties in strabismic subjects is not an all-or-none process, and that suppressive binocular interactions may be closely associated with the abnormal binocular interactions exhibited by strabismic humans. Furthermore, our findings are consistent with the notion that cortical disparity-detecting mechanisms are spatial-frequency dependent and, thus, can be selectively altered depending on an animal's early visual experience.

Human strabismus: Evaluation of the interhemispheric transmission time and hemiretinal differences using a reaction time task

Experimentally induced strabismus in visually immature cats leads to abnormal development of the posterior corpus callosum. This, in turn, should lead to abnormal interhemispheric integration of unilaterally presented visual information. To test whether strabismus produces deficits in the human commissural visual system, the interhemispheric transmission time (ITT) was compared in strabismic and normal subjects. Simple unimanual reaction times (RT) were tested in 30 subjects in response to a lateralized target presented monocularly at 4° and 35° nasally and temporally from the fovea along the horizontal meridian. This method was also used to examine the effect of strabismus on the central and peripheral portions of each hemiretina. The results showed that in strabismic subjects with or without amblyopia, the ITT did not differ significantly from normals at both eccentricities. In non-amblyopic strabismic patients, RTs in the central and peripheral portions of hemiretina were comparable to normals. However, a reduced speed of response was found in the central visual field (4°) in the amblyopic eye. Our results suggest that the ITT is normal in strabismic subjects and that the longer RTs in the central portion of the nasal and temporal hemiretina of the amblyopic eye may be associated with the severe amblyopic condition.

The spatial extent of binocular suppression in normal and strabismic subjects

The authors investigated and specified the spatial extent of binocular suppression for normal and strabismic subjects at differing retinal eccentricities. Increment luminance thresholds for detecting a probe line which was presented to one eye were measured under the influence of a contralateral suppressing line. Probe sensitivities were obtained as a function of positional disparity of the contralateral suppressing line. Two normals and two strabismics served as subjects. The suppression patterns for the normal and strabismic subjects were similar except for the width of the suppression area. The interocular suppression functions were U-shaped, and there were significant effects of eccentricity. The spatial extent of suppression for normal subjects was between 2 and 20 min arc at the fovea or between 5 and 40 min arc at an eccentricity of 2 degrees. The maximum disparity which produced suppression effects in the strabismics was about half of that obtained for the normals, in either the foveal or near peripheral conditions. The psychophysically obtained U-shaped functions appear to be similar to the neuro-physiological data from cat striate cortex by Kato, Bishop & Orban (1981). Therefore, the authors believe that these results may reflect the operation of an interocular version of the Westheimer function.

Der Freiburger Stereotest - Zur Beurteilung des Stereosehens bei Führerscheinbewerbern

The "Freiburg Stereotest" is a new instrument where disparate pictures are generated by a computer and displayed on one single high resolution video monitor. In the present work, the Freiburg Stereotest was used to check the stereo qualification for certain categories of driver's licence. For this purpose, a determination of the smallest detectable disparity is not reasonable. Rather, it should be checked whether or not a certain disparity, usually well above threshold, is recognized with a sufficient reliability. We have chosen a disparity of 100 arcsec; this value is considered to be an acceptable requirement for certain categories of driver's licence. 6 strabismic subjects were examined binocularly and 10 normal subjects were examined both binocularly and monocularly. Two targets ("busses"), side by side and different in depth by a disparity of 100 arcsec, were presented 78 times and, in a two-alternative forced-choice procedure, a minimum of 66 hits was required to pass the test. Monocular cues were excluded by a systematic variation of the lateral distance between the two targets. The strabismic subjects and the monocularly occluded normal subjects reached random scores only. With both eyes open, 8 of the 10 normal subjects reached scores near 100%, while 2 of them passed the test only when the lateral distance between the two targets was 15 minarc or less. For a lateral distance between the two targets of more than 15 minarc, these 2 subjects showed a learning effect. The Freiburg Stereotest allows to determine with statistical significance whether or not a proband can recognize a certain disparity which may be required for a driver's licence.

The development of optokinetic nystagmus in strabismic and monocularly enucleated subjects

Assymmetries of monocular optokinetic nystagmus (OKN) following anomalous visual experience are thought to be due to disruption at the cortical level. Visual disruption usually results from eye suture (in animals), unilateral dense and central cataracts or strabismus (in humans). Many form-deprived animals and humans frequently show a residual strabismus after lid opening (animals) or cataract extraction and optical correction (humans). We wanted to determine whether strabismus was unique in causing monocular asymmetries of OKN. Two independent observers rated eye movement videotapes of 20 normal subjects, the non-deviating eye of 25 unilateral strabismic subjects and 29 unilaterally eye-enucleated subjects, who were watching either a nasally directed square wave grating, a temporally directed square wave grating, or a blank field. Observers rated the proportion of trials where OKN occurred, the duration of OKN in each trial and the number of beats of OKN within each trial. Monocular OKN was symmetrical in normal subjects for the proportion and duration measures, but half the normal group showed small but significant asymmetries for the beats measure. Subjects in both enucleate and strabismic groups showed asymmetries of OKN favouring nasally directed stimulation, but only the early onset strabismics (as a group) showed asymmetries that were significantly greater (P less than 0.05) than the normal group. Asymmetry scores correlated significantly with age of diagnosis of strabismus for the strabismic group but not with age of enucleation for the enucleate group. The results are discussed in terms of binocular competition.

Vergence Movements in Comitant Strabismus

Vergence movements induced by base-out prisms were recorded, with an infrared eye tracker, for 6 patients with comitant esotropia (i.e., convergent strabismus) and anomalous retinal correspondence and for 6 normal subjects. Vergence movements of strabismic subjects were much slower and showed characteristics different from those of controls. It may be argued that vergence movements are induced by disparity and represent the motor fusion component left over in strabismus. In fact, in this study accommodative as well as proximal vergence had been ruled out. Therefore, the movements recorded can be considered the objective representation of the well-known phenomenon of prism compensation or adaptation, found in many strabismic patients.

The pupillary light reflex in normal and innate microstrabismic cats, I: Behavior and receptive-field analysis in the nucleus praetectalis olivaris

Neurons in the nucleus praetectalis olivaris (NPO) were antidromically identified by electrical stimulation of the nucleus of Edinger-Westphal (EW), the location of preganglionic pupilloconstrictor motoneurons. Electrical stimulation within the NPO leads to bilateral pupil constriction. Single neurons recorded in the NPO respond tonically to light stimuli, and their discharge frequency increases linearly with logarithmic increase in light intensity. This characteristic identifies NPO neurons as luminance detectors. They have large receptive fields mostly lying in the upper and contralateral quadrant of the visual field. Cats with impaired binocular vision show a significantly reduced binocular summation of the pupillary light reflex (BSP), i.e. the increase of pupil constriction during binocular illumination when compared to monocular illumination is less than in normal animals. The investigation of ocular dominance and subthreshold binocular interactions in the NPO of normal and innate microstrabismic cats revealed two possible mechanisms for BSP and its reduction in strabismic subjects. First, the percentage of neurons increasing their discharge rate by illuminating either eye is significantly reduced in the NPO of innate microstrabismic cats (6.6%) when compared to normal cats (22% of all neurons tested). Second, in most NPO neurons of normal cats the subthreshold influence of the ipsilateral eye leads to an increase in neuronal activity during binocular stimulation when compared to monocular stimulation of the contralateral eye (binocular summation). The subthreshold influence of the ipsilateral eye in most NPO neurons of microstrabismic cats, however, is inhibitory, i.e. the neuronal discharge rate during binocular stimulation is decreased when compared to monocular stimulation of the contralateral eye (binocular inhibition). However, there is no significant correlation between BSP and binocularity in the NPO in individual animals. This suggests that BSP may be additionally influenced by visual structures other than NPO.

Effect of target size on anomalous sensory responses in the Bagolini striated lens test.

Different results obtained by different methods of retinal correspondence testing are generally accepted to be a sign of the depth of the anomalous sensory adaptation. The Bagolini striated lens test is considered a standard "natural" test to which others are compared. In this study, the Bagolini striated lens test was performed on 25 strabismic subjects using three target sizes in order to determine if target size might be a factor in response variability. Kappa Measure of Agreement, used to analyze the results statistically, showed a moderately high to high level of agreement among the three targets. This indicates that practitioners can feel confident of consistent test results on the striated lens test using any of the three readily available target sizes selected. A brief literature review has been provided as a guide to the theories of strabismus and correspondence and to emphasize the purpose of this research.

Interocular transfer. An assessment of binocularity in strabismus.

The interocular transfer of the motion aftereffect (MAE) was used to probe for the existence of binocularity in subjects with strabismus. The interocular transfer was measured with coarse and fine gratings subtending 2° and 8° of visual angle. Strabismic subjects were categorized by the extent of their binocular vision, particularly with respect to extrafoveal fusion and retinal correspondence. Subjects classified as having the monofixation syndrome consistently showed a substantial, though less than normal, amount of transfer with the larger 8° gratings. This is consistent with the peripheral binocular cooperation usually found in these subjects, and establishes interocular transfer of the MAE as a suitable test for binocularity in strabismus. The test is especially suitable in patients with suppression in which an existing binocularity may be masked by suppression on clinical testing. The tests were found to be applicable in children as young as eight years. MAE tansfer for large coarse gratings is believed to imply the existence of an early cortical binocularity, which provides the potential for sufficient binocular cooperation to permit stable ocular alignment.

The Brückner Test

A quick and simple clinical test for detection of strabismus was evaluated for three groups of subjects. The test reliably detected the strabismic eye in the first group of strabismic subjects when observers discriminated between brightness of the right and left fundus reflex. The test reliably detected strabismus in the second group of strabismic subjects when observers decided if brightness of the fundus reflexes were equal or unequal. However, the Brückner test yielded false positives when it indicated strabismus in the third group of nonstrabismic subjects. The Brückner test is recommended only as an adjunct to testing for use by professionals, but not as a single test for strabismus detection by lay screeners.

Maldevelopment of visual motion processing in humans who had strabismus with onset in infancy

Binocular experience in infancy is necessary for the normal development of the visual cortex. However, it is not known whether binocular experience also affects the processing of specific kinds of visual information such as motion. We now report deficits in visual motion processing in 7 adult humans who lacked binocularity in infancy because of strabismus. As probes for assessing visual motion processing, we used the initiation of smooth pursuit eye movements and the judgment of target velocity independent of eye movement. Monocular viewing was essential to reveal the deficits. For horizontal pursuit, strabismic subjects showed nasal-temporal asymmetries, such that nasally directed target motion evoked more vigorous pursuit. For vertical pursuit, strabismics showed up-down asymmetries, such that upward target motion evoked more vigorous pursuit. In addition, strabismics had abnormalities in the relative effectiveness of different parts of the visual field for initiating both horizontal and vertical pursuit. Psychophysical judgements of horizontal target velocity revealed deficits analogous motion was perceived as faster than temporally directed motion, even when the 2 directions of motion were actually presented at the same speed. The magnitude of the motion processing deficits in each subject was correlated with the severity of the clinical signs of the strabismus. Our results suggest 2 possible interpretations. Maldevelopments of visual motion processing may cause strabismus in infancy, or alternatively, strabismus in the critical period for visual development may cause a maldevelopment of visual motion processing.

To fixate or not to fixate. The problem of undetected strabismic subjects in visual evoked potential research.

A common strategy in neuropsychological research involves the presentation of stimuli in left and in right visual fields in order to study possible processing differences by the right and left hemispheres of the brain. Examples of strictly behavioral studies are those of Dimond and Beaumont (1973). in which vigilance performance of the two hemispheres was compared, and of Pennal (1977), in which hemispheric asymmetries in color processing were examined. Visual event-related potential (ERP) researchers have used a similar strategy to investigate effects of visual field location on ERP recorded from over both hemispheres (e.g., Andreassi et al., 1975, and Ledlow et al., 1978). In the study by Andreassi et al., the results showed that stimuli presented in the left visual field (LVF) resulted in shorter visual ERP latencies in the right occipital area than in the left, while in the case of stimuli presented in the right visual field (RVF), the opposite occurred. This field effect on visual ERP latencies has also been reported by Ledlow et al. (1978) and by Andreassi et al. (1980). Whether a study is strictly a behavioral one or involves the measurement of ERPs, it is critical that the subject fixate a t the center of the visual field if the two hemispheres are to receive differential stimulation. We became concerned about the ability of subjects to fixate when, in one study (Andreassi et al., 1980), two of 12 subjects did not show the expected contralateral hemisphere latency advantage for eccentric stimuli. This occurred even though eye movement (vertical and horizontal) was monitored by electro-oculography and was stored on tape for later analysis. In our laboratory, we now screen' all potential subjects for visual acuity, strabism w b and depth acuity before their participation in visual ERP studies. Persons with eye muscle imbalance are not always detectable by casual observation and they may readily pass a binocular visual acuity test since they tend to use one eye in viewing. It was reasoned that individuals with strabismus would have difficulty maintaining their line of sight on some central fixation point. Therefore, even though electrooculography (EOG) is measured, these individuals may take up some different fixation point. Also, deviations from center would not be detected and the usual contralateral effect might not be observed. We believe that the absence of the contralateral hemisphere effect indicates that one or the other hemisphere is not being differentially stimulated. The depth acuity test was initiated as an additional check, since individuals with

Binocular interaction in visual-evoked responses: summation, facilitation and inhibition in a clinical study of binocular vision.

Binocular visual-evoked responses (VER) were recorded in normal and strabismic subjects. The percent increase of binocular with respect to monocular response was correlated to the degree of binocular performance expressed by the values of stereopsis in the Titmus stereo test and TNO test. Summation, facilitation and inhibition of binocular responses were found. In no case was a clear relationship found between the degree of binocularity and the amplitude of binocular VER. This limits clinical application of binocular VER recordings in the diagnosis of binocular vision disturbances.

Interocular transfer of the motion aftereffect in strabismus

The interocular transfer of the motion aftereffect (MAE) was measured in three groups of strabismic subjects (six with monofixation, nine with alternation, four with anomalous retinal correspondence) and compared with a group of four normal subjects. The duration of the MAE was measured using sinusoidal gratings of 0.5 c/deg subtending a visual angle of 8. Contrary to previous findings, a substantial amount of MAE transfer was found in some stereoblind individuals with strabismus. The mean amount of transfer for each group was found to correlate with binocularity; the order of decreasing transfer being: normal, monofixation, alternation, and anomalous retinal correspondence (ARC). This reduction in transfer which accompanied the loss of binocularity was asymmetric, that is. right-left transfer did not equal left-right transfer. The amount of asymmetry was found to correlate inversely with the amount of transfer. The direction in which the greatest transfer occurred did not correlate with visual acuity. These data substantiate the overall poor binocularity in subjects with ARC. and the relatively good binocularity of subjects with monofixation. Furthermore, the substantial amount of transfer found in subjects with alternating strabismus may be a measure of potentially achievable binocularity.

Interocular transfer of a visual aftereffect in different kinds of strabismus.

The interocular transfer of the tilt aftereffect may depend upon the level of binocularity possessed by the subject. Visual acuity, eccentric fixation, and suppression may affect the results of such studies independently of the role of binocular cortical cells. This study found no significant difference between normal and strabismic subjects in the ability to appreciate and to transfer the tilt aftereffect.

Disparity-induced vergence responses in normal and strabismic subjects.

Latencies of vergence responses were obtained by presenting vertical line stimuli for 0.5 sec to the fovea of one eye and to various retinal locations of the other eye of four subjects with normal binocular vision, one exotrope with normal retinal correspondence, and four esotropes with anomalous correspondence. Vergence latencies were larger for squinters than nonsquinters and were especially long for the squinters with anomalous correspondence. For three of the four anomalous corresponders, the direction of the vergence movement (convergence or divergence) was based on the location of the stimulus with respect to the anomalous retinal point in the deviating eye--not with respect to the fovea as occurred for the subjects with normal correspondence.

Accommodative and fusional vergence in anomalous correspondence.

Strabismic subjects who have anomalous correspondence often exhibit covariation in their angle of deviation and angle of anomaly. One hypothesis is that these covariation responses represent a neurological link between binocular correspondence and vergence innervation; an alternative is that they are neurologically independent. A description of these two interpretations is followed by certain implications and predictions.

Depth perception in strabismus.

The monocular and binocular depth thresholds of strabismic subjects have been measured with a modified Howard-Dolman apparatus. Seven out of the 14 strabismic subjects tested were found to have binocular thresholds significantly higher than their monocular ones. These strabismic subjects all had small angles of deviation less than 8 prism dioptres and high acuities in both eyes.

Localization of targets by strabismic subjects: Contrasting patterns in constant and alternating suppressors

Strabismic subjects in whom vision in one eye is constantly suppressed localized targets at different points in space when using each eye. Whether they were esotropes or exotropes determined the relation between the two locations and the angle of their vergence error correlated with the magnitude of the interocular discrepancy. These relationships suggest that constant suppressors utilize information about posture of the dominant eye in reaching toward targets presented to the normally suppressed eye. Neither orthotropes nor strabismics in whom vision in each eye is alternately suppressed showed this anomaly. These results were attributed to differences in the way in which visual space is represented, an outcome of the pattern of use of the eyes during early development.

Visual stimuli for strabismic suppression.

The effects of orientation and spatial frequency of grating stimuli upon suppression were examined with a binocular rivalry paradigm in a group of ten strabismic patients and in a control normal group. Duration, frequency, and period of rivalry were examined as functions of differences in orientation and spatial frequency of dichoptic achromatic sinusoidal gratings. Records were made of responses by the sighting and by the nonsighting eye as well as responses during periods of combined binocular vision. Strabismic subjects reported normal binocular rivalry when presented with gratings of dissimilar orientation. Suppression of the deviating eye in strabismic subjects occurred with stimuli of similar orientation and was unaffected by spatial-frequency differences between dichoptic stimuli. Suppression was most intense under conditions that normally stimulate stereopsis and sensory fusion.