Investigation of Selective Innervation of Extraocular Muscle Compartments

PURPOSE: Recent magnetic resonance imaging studies have suggested that extraocular muscles (EOM) are further divided into transverse compartments that behave differentially and often unexpectedly during eye movements. Selective innervation of EOM compartments may explain the observation that certain horizontal recti compartments contribute to specific vertical eye movements and that some cyclovertical EOM compartments do not contribute to vertical vergence. We investigated the discharge characteristics of extraocular motoneurons during these eye movement tasks where EOM compartments behaved differentially for evidence of selective innervation. METHODS: We recorded from all six extraocular motoneuron populations in the abducens, oculomotor, and trochlear nuclei as two non-human primates performed vertical vergence and vertical smooth-pursuit. The relationship between motoneuron firing rate, horizontal and vertical eye parameters of the innervated eye during each task was determined using multiple linear regression. RESULTS: All 26 medial rectus motoneurons recorded showed no significant modulation during vertical smooth-pursuit and vertical vergence. Twenty-eight of 30 abducens motoneurons showed no significant modulation during vertical vergence, and all 30 cells did not modulate during vertical smooth-pursuit. For the cyclovertical motoneurons, 147 of the 149 cells (44/46 inferior rectus, 27/27 superior oblique, 41/41 superior rectus and 35/35 inferior oblique) modulated significantly during vertical vergence. CONCLUSIONS: Extraocular motoneuron activity during vertical vergence and vertical smooth-pursuit does not support the theory that EOM compartments are selectively innervated. The observed differential behavior of EOM compartments is likely not driven by oculomotor control and could be due to passive change in EOM cross-sectional area.