Neural Control of Vertical Vergence and Extraocular Muscles Compartmentalization

Date

2022-08-08

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Abstract

Purpose: Vertical vergence is an important eye movement used to adjust the vertical position of each eye to achieve and maintain binocular fusion. This dissertation investigated the neural circuitry that controls vertical vergence by determining the contribution of each cyclovertical extraocular muscle (EOM) to its generation using both behavior and neurophysiological approaches. We also tested for evidence for selective innervation of EOM compartments to explain MRI observations of horizontal recti compartments contributing to specific vertical eye movements and that not all compartments of the cyclovertical EOMs contribute to all vertical eye movements. Methods: Horizontal and vertical position of both eyes were recorded as two awake behaving non-human primates performed a dichoptic asymmetric vertical vergence task. We (1) measured and compared vertical fusion amplitude and vertical vergence at different horizontal gaze directions, (2) recorded single-unit activity of cyclovertical motoneurons and analyzed the relationship between their firing rate and vertical eye position during vertical vergence and (3) recorded the single-unit activity of horizontal motoneurons during vertical vergence and vertical smooth-pursuit to complement cyclovertical motoneuron recordings and test for compartmental innervation. Results: (1) Vertical fusion amplitude and vertical vergence differed at different orbital eye positions, but was idiosyncratic between the eyes and between animals. (2) The firing activity of neurons in all four cyclovertical motoneuron populations (n=149) correlated with vertical eye position during vertical vergence indicating the involvement of all cyclovertical EOMs. Moreover, we identified paradoxical behavior in that almost half of the cyclovertical motoneurons modulated with movement of either eye. (3) Only 2/56 of the tested horizontal motoneurons modulated their activity with vertical eye position, and 147/149 of the tested cyclovertical motoneurons modulated their activity during vertical vergence, indicating an absence of evidence for compartmental innervation. Conclusion: All cyclovertical EOMs contribute to the generation of vertical vergence, but their relative contribution may differ and also vary amongst different subjects. Paradoxical behavior suggests the existence of eye specific premotor control for vertical vergence, and so show some similarities to horizontal vergence control. The EOM compartments are not selectively innervated, and the observed differential behavior is likely not driven by oculomotor control.

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Keywords

Vertical vergence, Extraocular muscles, Extraocular muscle compartmentalization, Binocular coordination, Motoneuron

Citation

Portions of this document appear in: Adade, Samuel, and Vallabh E. Das. "Vertical vergence in nonhuman primates depends on horizontal gaze position." Strabismus 27, no. 3 (2019): 172-181.