Perception via the deviated eye in strabismus

Abstract

Misalignment of the eyes can lead to double vision and visual confusion. However, these sensations are rare when strabismus is acquired early in life, because the extra image is suppressed. To explore the mechanism of perceptual suppression in strabismus, the visual fields were mapped binocularly in 14 human subjects with exotropia. Subjects wore red/blue filter glasses to permit dichoptic stimulation while fixating a central target on a tangent screen. A purple stimulus was flashed at a peripheral location; its reported color ("red" or "blue") revealed which eye's image was perceived at that locus. The maps showed a vertical border between the center of gaze for each eye, splitting the visual field into two separate regions. In each region, perception was mediated by only one eye, with suppression of the other eye. Unexpectedly, stimuli falling on the fovea of the deviated eye were seen in all subjects. However, they were perceived in a location shifted by the angle of ocular deviation. This plasticity in the coding of visual direction allows accurate localization of objects everywhere in the visual scene, despite the presence of strabismus.

Figure 1.

Perception via the deviated eye in subject 1. a, Visual field of the left eye (circles, blue shading) plotted in a hemispheric perimeter, after patching the right eye. It extended from 90° temporally to 55° nasally. When the exotropic right eye was uncovered, the range of targets seen by the subject expanded horizontally to 180° (squares). b, Visual field of the right eye (circles, red shading), after patching the left eye. Opening the exotropic left eye increased the range of detected targets to 180° (squares). With either eye fixating, uncovering the exotropic eye added 35° (gray shading), indicating that targets landing on peripheral nasal retina of the deviated eye were perceived. The asterisk in each plot represents the approximate location of the deviated eye's fovea.

Figure 2.

Dichoptic visual field testing for mapping of suppression scotomas in strabismic subjects. Each row shows an example of a different stimulus color: blue, red, and purple. Initially, the subject is sitting in the dark, wearing colored glasses (red for right eye; blue for left eye). The color of the fixation cross at the center of the tangent screen varies randomly between red or blue on individual trials. After the eye trackers detect fixation within an “on-target” window, a colored 1° spot appears peripherally following a variable delay of 500–2000 ms. The spot is presented for 200 ms. The subject's task is to identify verbally its color. Fixation must be maintained on the central cross. The red and blue spots represent control trials; the purple spots composed of isoluminant red and blue provide information about visual suppression.

Figure 3.

Suppression scotomas in subject 1. Visual field maps compiled from interleaved trials with either the left (a) or right (b) eye fixating on a cross at the center of the tangent screen. The center of gaze for the fixating eye has been set at the origin for all trials. The top row shows purple stimulus trials. Most points were tested four times; jitter in the location of each stimulus trial (white circles) reflects a correction corresponding to the difference in position between the fixation cross and the fixating eye, as measured by the eye tracker. The position of the deviated eye for each trial is plotted as a small black dot, forming a cluster underneath the letter for that eye. The fill color of the white circles indicates the subject's verbal response to a spot at that location: “blue,” left eye perceiving; “red,” right eye perceiving. The color shading is a smoothed Kriging interpolation of the data points. The middle row shows control trials with a red stimulus, with 99 of 99 correct responses. The bottom row shows control trials with a blue stimulus, with 106 of 111 correct responses. Forty-eight of 49 blank trials were correctly ignored.

Figure 4.

Responses during binocular fusion in subject 1. Plot of responses to purple stimuli (white circles) delivered while the eye trackers detected fixation of both (B) eyes at the origin. Responses of either “blue” or “red” were intermingled in a noisy pattern that bore little resemblance to the distribution of responses recorded during periods of exotropia (Fig. 3, top row).

Figure 5.

Dichoptic visual field testing in a 30-year-old man with exotropia from a traumatic partial oculomotor nerve palsy. Testing was conducted approximately a year after the onset of double vision. The plots show responses to trials with the left (a) or right (b) eye fixating at the center. Top row, Purple stimuli usually evoked a response of “both,” depicted with a purple fill color because the subject lacked visual suppression. In contrast, exotropic patients with visual suppression had a different pattern of responses to purple stimuli (Fig. 3 top). Red (middle row) and blue (bottom row) stimulus trials were usually identified accurately, with either eye fixating.

Figure 6.

Dichoptic perimetry in 12 subjects (a–l) with exotropia. For each set of plots, the left panel shows responses with the left (L) eye fixating and the right panel shows responses with the right (R) eye fixating. Fields subtend 60° horizontally by 30° vertically, with points tested approximately four times at every 5° interval. The blue shading denotes regions where the subject responded “blue,” signifying perception of a purple spot via the left eye alone. The red shading indicates regions where the subject responded “red” to the purple spot, corresponding to perception by the right eye alone. The black dots represent the position of the deviated eye on each trial. Subjects c and e had intermittent exotropia but did not fuse during testing.

Figure 7.

Schematic illustration of the portions of the visual field perceived with the left eye (blue) and right eye (red), while an exotropic subject fixates centrally with the left eye. There is suppression of part of the temporal retina (gray) in each eye, to avoid diplopia. Diplopia would arise if the temporal retinal locus in the deviating eye (dashed line) overlapping with the fovea in the fixating eye were perceptually active. The amount of temporal retina which is suppressed depends on the size of the ocular deviation: the smaller the deviation, the larger the region of suppression. If the subject switches to fixate centrally with the right eye, there is little change in the position of the border between perceiving and suppressed retina in each eye. F, fovea.

Figure 8.

Dichoptic visual field mapping in subject 2. a, Color-coded responses to a purple spot presented with either the left or right eye fixating at the origin. Testing was extended to ±40° because the exotropia was large, averaging nearly 30°. Afterimage test shows the horizontal position drawn by the patient of a slit flashed onto the left fovea (horizontal) and the right fovea (vertical). b, Dichoptic visual field mapping after surgery. With either eye fixating at the origin, the other eye was crossed, signifying an esotropic deviation. To a purple spot, the subject responded “both” at most locations, indicating that she had diplopia. The afterimage test showed that the right fovea (vertical slit) was still perceived at 23° to the right, although it now projected 15° to the left of the left fovea (horizontal slit). c, Subject 2 after restoration of an exotropia, measuring 5°. The suppression scotomas appear similar to those mapped before the first operation (a), although responses are inconsistent centrally, accounting for the subject's report that diplopia had not resolved entirely. Afterimage test showed an anomalous retinal correspondence of 5°, close to the ocular deviation.