Maldevelopment of convergence eye movements in macaque monkeys with small- and large-angle infantile esotropia

To describe symmetric convergence eye movements evoked by disparity and/or accommodative cues in esotropic macaque monkeys, with the goal of determining whether these animals have the vergence deficits found in humans with esotropia.

Physical far and near targets were used to evoke large (approximately 8 degrees) symmetric convergence eye movements in four adult macaque monkeys (two with strabismus, two normal), using positive-feedback rewards. One strabismic monkey had infantile-onset, small-angle esotropia (small-eso approximately 2 degrees) induced by alternating occlusion from birth to age 9 months. The other strabismic monkey had naturally occurring, large-angle (approximately 25 degrees) infantile-onset esotropia (large-eso). Visual acuity was normal in each eye as measured by spatial sweep visually evoked potentials (VEPs). Eye movements were recorded using magnetic search coils.

When viewing binocularly, both normal monkeys exhibited accurate, stereotyped symmetric convergence movements that achieved 87% to 96% of the required change in vergence angle by the end of the initial movement. In contrast, the small-eso monkey's convergence response when viewing binocularly was variable, strikingly asymmetric, usually accompanied by a disjunctive saccade, and subnormal, achieving only 56% of required vergence. The convergence response of the large-eso monkey was also asymmetric and weak, achieving 18% of the required vergence and employing conjugate saccades to refixate the near target. Monocular viewing (i.e., accommodative vergence) caused substantial reductions in both convergence amplitudes and velocities in the normal monkeys, but had a minor effect on the vergence behavior of the strabismic animals.

Monkeys with small- and large-angle infantile esotropia have striking maldevelopments of binocular (disparity-driven) convergence and use accommodative vergence and saccades to refixate near targets. Their vergence behavior resembles that in esotropic humans. The maldevelopment may be explained in large part by the paucity of binocular connections recently described in the visual cortex of esotropic macaques.