The results of these investigations have demonstrated that patients with primary microstrabismus have a relatively high grade of binocular vision, but they do not directly support a specific sensory abnormality as the cause of the small ocular deviation. For example, the data do not support the hypothesis that microstrabismus is an oculomotor adaptation to an inherent anomalous correspondence because the state of correspondence is dependent on the retinal locations of the fusion stimuli, which would require specific genetic alterations for disparity mechanisms of the central retina, but not the peripheral retina. In addition, the data do not provide evidence of a genetic absence of a class of disparity detectors, because neither the sensory nor motor fusion responses reveal an absence of a specific class of fine- or coarse-disparity detectors. Therefore, in lieu of a sensory origin, it seems most likely that the sensory characteristics of microstrabismus are a consequence of abnormal visual experience, just as in large-angle strabismus.
The high grades of binocularity with primary microstrabismus found with both perceptual and oculomotor tests provided detailed descriptions of the clinical characteristics that were found by previous clinical investigations.
2 3 4 5 6 For example, all the microstrabismic patients could perceive stereoscopic depth, although they required extensive practice and their stereoacuities were obviously abnormal
(Fig. 2) . The configuration of the tests to quantify stereoacuity was considerably different from the usual clinical tests of stereopsis, with better control of monocular cues with large disparities, the presentation of both crossed and uncrossed disparities, and a large number of observations to develop the psychometric function. In spite of these differences, the assessments of stereopsis were generally similar to those of other studies using clinical tests.
3 4 5 6 32 33 For example, Helveston and von Noorden
3 found some degree of stereopsis with the Wirt test in all their microstrabismic patients with eccentric fixation, Cleary et al.,
5 found very high levels of stereoacuity with the Frisby stereo test in five of nine patients with primary microstrabismus, and recently, Tomac et al.,
6 reported that one half of their patients with primary microesotropia achieved at least gross stereopsis on the Titmus stereo-fly test.
The present studies have extended these findings to demonstrate two important properties of microstrabismus. First, stereoacuities with microstrabismus are basically the same whether they are obtained with or without compensation for the strabismic deviation
(Fig. 3) . This result may simply reflect the effect of abnormal binocular vision during early development. When an interocular deviation in young children causes large, off-horopter disparities in fixated objects, the fine-disparity mechanisms are deprived of adequate stimuli for normal development, whereas allowing normal development of coarse-disparity mechanisms for both central and peripheral stimuli. Consequently, in later life, the level of stereoacuity would be limited by coarse-disparity mechanisms for either bifoveal stimuli or foveal–peripheral stimuli with a strabismic deviation.
A second important finding of the present investigation relates to local versus global stereopsis in microstrabismus. It has often been reported that patients with microstrabismus rarely perceive depth in random-dot stereograms,
7 33 yet for the two subjects that were tested, stereoacuities were equal for local and global stereopsis
(Fig. 3) . These measurements of stereoacuity probably were accomplished because of the specific configuration of the random-dot stereograms, because the mechanisms of disparity-detection should not be different for different forms of stereograms. The clinical versions of random-dot stereograms are small, with small dot elements that must be in precise registration on the two retinas for normal stereoprocessing. These stereograms easily could become decorrelated for strabismic patients by their interocular deviation. The present study used stereograms with extended overall size and large dot elements, so that peripheral fusion could maintain interocular correlation and the strabismic deviation would not decorrelate the two stereoscopic half-views.
The study of motor fusion also provided evidence of high grades of binocularity with responses that were based on either normal or anomalous retinal correspondence, depending on the retinal locations of the stimuli. Similar results with other types of strabismic patients have been reported previously.
34 35 36 The general finding of oculomotor fusion responses in strabismic patients also is in agreement with previous investigations, including the demonstration that the vergence responses can be centered on disparities referenced to the subjective angle (anomalous retinal correspondence) rather than the objective angle of deviation.
37 38 39 40 41 42 43 However, vergence responses do not represent a simple shift in zero retinomotor sites, because clinical data have shown that microstrabismic patients have normal peripheral correspondence and fusion amplitudes for prism-induced disparities, even though they have anomalous correspondence by central vision tests.
3 39 Thus, the coexistence of harmonious anomalous retinal correspondence for small central stimuli and normal fusional response magnitudes for the peripheral, uniform disparities introduced by ophthalmic prisms is a defining characteristic of microstrabismus. The present investigations of prism-induced disparity vergence also found fusion responses that were mediated either by normal correspondence when the fusion stimuli were located peripherally or mediated by anomalous correspondence when the fusion stimuli were restricted to the central visual field
(Fig. 6) . The two states of retinal correspondence produce an interesting dilemma for the strabismic visual system because, under normal binocular viewing, central and peripheral stimuli present conflicting vergence stimuli. Apparently, however, the strabismic adaptation is to ignore the larger disparities associated with nonfixated objects and to respond only to fixated stimuli, using anomalous correspondence. Such an adaptation actually represents an exaggerated response of normal mechanisms of binocular vision, because normal subjects also are relatively insensitive to large disparities from stimuli that are off the horopter, which even for the normal visual system is advantageous for maintaining stable normal eye alignment.
43 44 45 Therefore, just as in large-angle strabismus, anomalous correspondence in microstrabismus may be an adaptation to an oculomotor anomaly that occurs only in central vision, because there are other mechanisms that render the visual system insensitive to large disparities associated with nonfixated objects.
The properties of the abnormal binocularity with microstrabismus seem to be described adequately by developmental constraints and adaptations imposed by visual experience during early childhood, rather than genetic or acquired errors in cortical connections.
46 47 The relationship with abnormal visual experience is also supported by animal experiments, in which abnormal binocularity with similar characteristics has been reported for monkeys reared with short periods of surgically induced esotropia or with optical dissociation of binocular vision.
17 48 Monkeys subjected to these forms of early visual experience demonstrated reduced stereoacuity with normal disparity vergence functions, using the same testing methods as in the present investigations with humans with microstrabismus. The subsequent investigations of cortical physiology on some of these monkeys revealed that, compared with normal monkeys, they had fewer neurons with balanced ocular dominances, generally reduced response amplitudes of binocular neurons, fewer neurons that were sensitive to spatial disparities, and a larger number of neurons exhibiting binocular suppression.
49 Altogether, the alterations from experimental strabismus seem sufficient to explain the abnormal binocularity associated with primary microstrabismus.
The disparity vergence measurements with prisms evaluated closed-loop responses that are important in causal viewing, when slow movements with long latencies are adequate. However, an understanding of the mechanisms of fusional vergence in microstrabismus also requires investigations of open-loop responses.
40 50 In the present investigations, the vergence loop was opened by using stimulus durations that were shorter than the combined latency-plus-eye movement time. Another important methodological consideration was the use of fusion stimuli (small central Gabor patterns) that elicited anomalous retinal correspondence for the subjects with primary microstrabismus, and therefore the positive and negative vergence responses were centered on the point of subjective alignment with anomalous retinal correspondence. In other respects and with some caution because of the possible effects of anomalous retinal correspondence, the results for microstrabismic patients appear to be normal response functions for disparity vergence to stimuli of relatively small magnitude
(Fig. 9) . In fact, the data for those with microstrabismus are indistinguishable from the data of subjects with stereodeficiencies of no known etiology
(Fig. 8B) . Notably, the data for both types of sensory deficits in disparity processing demonstrate vergence responses that were proportional to stimulus magnitudes and continuous across crossed and uncrossed physical disparities.
The systematic relationship found under these experimental conditions reveals two interesting characteristics of the anomalous retinal correspondence in microstrabismus. First, the time constraints for these experiments, a brief (250 msec) fusion stimulus and a two-frame interval (16.66 msec) between the Gabor fusion stimuli and nonius response stimuli, effectively precludes mechanisms based on a disparity-induced remapping of retinal correspondence.
51 52 Second, the disparity vergence functions suggests that the subjects’ disparity vergence mechanisms were as sensitive to small disparities, with the same response amplitude, as subjects with normal retinal correspondence. Further, the normal response function, given the imposed timing paradigm, indicates that the vergence response latencies were also within normal limits. Thus, all the primary response characteristics of their disparity vergence seem to be normal, except that the zero retinomotor location is displaced to a nasal retinal site in the deviating eye.
Another etiological factor that has been proposed for microstrabismus is a genetic–hereditary deficiency in one of the components of disparity-selectivity. The data from the present experiments argue against such an etiological factor by the linearity in vergence responses to crossed and uncrossed disparities
(Fig. 9) and in the detectability of crossed and uncrossed disparities
(Fig. 10) . Mild asymmetries in the sensitivities of disparity-sensitive mechanisms of the type that could cause strabismus are quite common in subjects with normal binocular vision and may account for the occurrence of fixation disparities.
13 14 53 54 However, if the constant frank deviation of microstrabismus is an expression of abnormal imbalances of disparity-selective mechanisms, then the response functions for depth detection and/or disparity vergence should have revealed strong response biases. Such response biases were not present in the disparity functions of subjects with primary microstrabismus, although the sensory disparity detection functions were very shallow. Therefore, these functions demonstrate an independence in sensory and motor sensitivities that is similar, but more apparent, than equivalent data from subjects with normal binocular vision. In this respect, the poor correlation between sensory and motor mechanisms of disparity processing may be considered to be another example of the exaggerations of normal mechanisms of binocular vision that are caused by abnormal visual experience.
Two additional aspects of these experiments are important to the general implications of the results. First, the experimental subjects were a much more homogeneous subgroup of primary microstrabismus than in previous investigations.
2 3 4 5 6 None of the subjects of these experiments exhibited the commonly associated conditions of anisometropia, amblyopia, or eccentric fixation. Second, all the subjects, both the experimental and control groups, were given extensive pretraining on the procedures and observations required for data collection. Consequently, the data should provide a fair representation of the state of their binocular vision, without influence from cognitive factors or naivety in making abstract judgments. Thus, it may be concluded that this specific form of primary microstrabismus represents a highly adapted state of binocular vision,
55 with stable eye alignment, coarse depth perception, and central harmonious anomalous retinal correspondence. It is an interesting condition, and much more work is needed to gain a full understanding of the mechanisms of binocular vision, but patients with this form of primary microstrabismus are not apt to benefit from additional treatment by either medical or nonmedical procedures.
The authors thank Bruce Wick, Janice Wensveen, and Suzy Wickham for the orthoptic workup and referral of their patients with primary microstrabismus.