Motion Information via the Nonfixating Eye Can Drive Optokinetic Nystagmus in Strabismus.

Two to five percent of all children are affected by developmental strabismus, a disorder in which the normal development of binocular vision is disrupted and the eyes become permanently misaligned.1–3 The misalignment of the two eyes can cause diplopia (double vision) and visual confusion. In diplopia, an object is projected to the fovea of one eye as well as to the peripheral retina of the deviated eye, and visual confusion occurs due to the projection of different objects in the environment to the foveae of the two eyes.4 However, patients with developmental strabismus do not experience diplopia and visual confusion because of two adaptive mechanisms adopted by the brain: visual suppression and anomalous retinal correspondence.4–6 Visual suppression of the images from one eye (deviated eye) results in temporary blind fields in the retina, known as scotomas, that are present in binocular viewing conditions but not in monocular viewing conditions. It could be that the fovea of the deviated eye is suppressed to avoid visual confusion, and that portions of temporal hemiretina in exotropes and nasal hemiretina in esotropes are suppressed to prevent diplopia.1,6–8 However, Economides et al.9 mapped areas of visual suppression in exotropic human subjects by using a color discrimination task and found that the fovea and portions of the temporal retina immediately adjacent to the fovea in the deviated eye are not suppressed in exotropes. They also showed that visual confusion is avoided by anomalous retinal correspondence (ARC), in which the fovea of the viewing eye is paired with a noncorresponding location in the deviated eye. Strabismic patients with relatively little amblyopia can switch the eye of fixation spontaneously depending on the location of the object they want to fixate, and this fixation-switch feature of strabismus is likely the result of visual suppression of portions of each eye's retina.7,10–12 Studies from our lab have replicated fixation-switch behavior in a monkey model for strabismus, and analyzing the spatial patterns of fixation switch in strabismic monkeys has provided insight into how visual information from the two eyes is processed and converted into action in strabismus.13,14 Fundamentally our results supported the idea that fixation-switch behavior follows from suppression of a portion of temporal retina in exotropes and a portion of nasal retina in esotropes. However, the fovea and portions of the temporal retina immediately adjacent to the fovea (portions of the nasal retina adjacent to the fovea in esotropes) were apparently not suppressed because the animals switched fixation when the target appeared in these retinal locations, thereby in agreement with the suppression maps of Economides et al.9 A novel finding was that the transition zone between preference for right eye fixation and preference for left eye fixation was “fuzzy” in that the animals could choose either eye to fixate the target appearing at certain spatial locations, suggesting that visual suppression can be partial. Agaoglu and colleagues13 proposed a framework for fixation-switch behavior wherein the oculomotor system has retinal error information from both eyes, and the choice of fixating eye is made according to the strength of retinal error representations from each eye. Economides et al.15 also examined fixation-switch behavior in human exotropes and showed a coupling between perceptual state and spatial patterns of fixation-switch behavior. The overall motivation for the current study was to continue to investigate the nature of the visual information available to the brain from the two eyes that it can use to drive eye movements. Specifically, we asked whether motion information available only to the deviated eye could be used by the oculomotor system to drive eye movements. Similar to studies that employed dichoptically presented drifting grating stimuli with motion in opposite directions to assess eye dominance or interocular suppression from optokinetic motor responses,16–22 our strategy was to present an optokinetic stimulus (a drifting grating) only to the deviated eye of the strabismic monkeys and determine whether it was sufficient to generate an optokinetic nystagmus (OKN). Our investigation suggests that optokinetic oculomotor responses can indeed be generated by a stimulus that falls on/around the fovea of the deviated eye, supporting the overall hypothesis that the oculomotor system has retinal information available from both eyes in strabismus. Some of these data have been presented before (Agaoglu S, et al. IOVS 2014;55:ARVO E-Abstract 2573).