A Rhesus Monkey With a Naturally Occurring Impairment of Disparity Vergence. II. Abnormal Near Response Cell Activity in the Supraoculomotor Area.

Purpose: Convergence insufficiency is a very common disorder that can have significant adverse effects on school performance. When reading, children with this disorder often experience diplopia and headaches. We have recently obtained a rhesus monkey with a naturally occurring impairment of vergence eye movements. In the companion paper, we report behavioral testing that shows a pattern of impairments similar to what clinicians observe in human children with convergence insufficiency, including a receded near point, an exophoria that increases as target distance decreases, and difficulty maintaining an appropriate vergence angle when presented with a large field stimulus at near. For the present case report, we wondered whether these behavioral deficits would be associated with abnormal discharge patterns in brainstem neurons related to vergence eye movements. Methods: Single unit activity was recorded from near and far response cells in the supraoculomotor area in the vergence-impaired monkey, while he performed a smooth vergence tracking task or fixated visual targets at different distances. Results: We found an abnormally weak sensitivity to both vergence angle and vergence velocity. Nonetheless, these neurons modulated in association with contextually inappropriate slow vergence movements that occurred in the absence of saccades but not for slow divergence drifts that immediately followed converging saccades. Modulation of activity was more robust when additional depth cues were available. Conclusions: These data suggest that disorders affecting vergence eye movements may be associated with impoverished sensory input to the near and far response cells and, perhaps, aberrant tuning in vergence-related neurons.

Activity of near-response cells during disconjugate saccades in strabismic monkeys.

Infantile strabismus is a common disorder characterized by a chronic misalignment of the eyes, impairment of binocular vision, and oculomotor abnormalities. Nonhuman primates with strabismus, induced in infancy, show a pattern of abnormalities similar to those of strabismic children. This allows strabismic nonhuman primates to serve as an ideal animal model to examine neural mechanisms associated with aberrant oculomotor behavior. Here, we test the hypothesis that impairment of disparity vergence and horizontal saccade disconjugacy in exotropia and esotropia are associated with disrupted tuning of near- and far-response neurons in the supraoculomotor area (SOA). In normal animals, these neurons carry signals related to vergence position and/or velocity. We hypothesized that, in strabismus, these neurons modulate inappropriately in association with saccades between equidistant targets. We recorded from 62 SOA neurons from 4 strabismic animals (2 esotropes and 2 exotropes) during visually guided saccades to a target that stepped to different locations on a tangent screen. Under these same conditions, SOA neurons in normal animals show no detectable modulation. In our strabismic subjects, we found that a subset of SOA neurons carry weak vergence velocity signals during saccades. In addition, a subset of SOA neurons showed clear modulation associated with slow fluctuations of horizontal strabismus angle in the absence of a saccade. We suggest that abnormal SOA activity contributes to fixation instability but plays only a minor role in the horizontal disconjugacy of saccades that do not switch fixation from one eye to the other. NEW & NOTEWORTHY The present study is the first to investigate the activity of neurons in the supraoculomotor area (SOA) during horizontally disconjugate saccades in a nonhuman primate model of infantile strabismus. We report that fluctuations of horizontal strabismus angle, during fixation of static targets on a tangent screen, are associated with contextually inappropriate modulation of SOA activity. However, firing rate modulation during saccades is too weak to make a major contribution to horizontal disconjugacy.

Neural mechanisms of oculomotor abnormalities in the infantile strabismus syndrome.

Infantile strabismus is characterized by numerous visual and oculomotor abnormalities. Recently nonhuman primate models of infantile strabismus have been established, with characteristics that closely match those observed in human patients. This has made it possible to study the neural basis for visual and oculomotor symptoms in infantile strabismus. In this review, we consider the available evidence for neural abnormalities in structures related to oculomotor pathways ranging from visual cortex to oculomotor nuclei. These studies provide compelling evidence that a disturbance of binocular vision during a sensitive period early in life, whatever the cause, results in a cascade of abnormalities through numerous brain areas involved in visual functions and eye movements.