Neural Innervation of Cyclovertical Extraocular Muscles During Asymmetric Vertical Vergence.

Purpose: Vertical vergence is a critical involuntary eye movement used to make relatively small and slow adjustments of the vertical position of each eye to achieve and maintain binocular fusion for daily activity. Little is known about the mechanisms driving vertical vergence, beginning with the contribution of specific extraocular muscle (EOM) groups and extending to its neural control. Here, we describe activity of cyclovertical extraocular motoneurons during vertical vergence in non-human primates to determine their role in generating this movement. Methods: In two non-human primates, we recorded and analyzed single-unit activity of motoneurons (n = 149) that innervate the four cyclovertical EOMs during conjugate vertical smooth pursuit and an asymmetrical vertical vergence task in which one eye is stationary and the other eye moves vertically. Results: Firing activity of all neurons within the four cyclovertical motoneuron subgroups (inferior rectus, superior rectus, inferior oblique, and superior oblique) correlated with vertical position of the innervated eye during the vertical vergence task. Analysis of position sensitivities suggested that cyclovertical motoneurons contribute differently during vertical vergence compared to vertical smooth pursuit. During asymmetric vertical vergence, 67 of the 149 cyclovertical motoneurons supplying the stationary eye modulated their activity. Conclusions: Neural innervation patterns suggest that contraction and relaxation of all cyclovertical EOMs result in vertical vergence. The differences in activity between vertical vergence and conjugate pursuit and the presence of matched and unmatched neurons are parallel to observations of motoneuron activity during horizontal asymmetric vergence and add to the literature showing the complex relationship between EOM innervation and oculomotor plant behavior.