Neural recordings of extraocular muscle motoneurons do not show evidence for selective innervation of muscle compartments

Abstract

Purpose : Selective innervation of extraocular muscle (EOM) compartments may explain the observation made via MRI that certain horizontal recti compartments may contribute to specific vertical eye movements such as vertical vergence and that not all compartments of the cyclovertical EOMs contribute to all vertical eye movements. We investigated the discharge characteristics of EOM motoneurons (MN) during vertical vergence and vertical smooth-pursuit for evidence of selective innervation of EOM compartments. Our hypothesis was that selective innervation of compartments would manifest as a sub-population of horizontal MN that are modulated during vertical vergence and a sub-population of cyclovertical MNs that are modulated during vertical smooth-pursuit but not vertical vergence.

Methods : We recorded from all EOM MN populations in the abducens, oculomotor and trochlear nuclei as two non-human primates performed vertical vergence and vertical smooth-pursuit. The relationship between MN firing rate and horizontal/vertical eye parameters of the innervated eye during each task was determined using multiple linear regression analysis by fitting the data to the equation FR= K_v*(vert. eye pos.) + K_h*(horiz. eye pos.) + R_v*(vert. eye vel.) + R_h*(horiz. eye vel.) + B. Position (K_h, K_v) and velocity sensitivities (R_h, R_v) were considered significant if the 95% confidence interval did not include zero.

Results : We did not find different subpopulation of EOM MNs with different responses during vertical eye movement tasks where some EOMs compartments have been previously found to contract and relax differentially. Thus 28 of 30 abducens MN recorded showed no significant modulation in relation to vertical eye position during vertical vergence and all 30 cells did not modulate during vertical smooth-pursuit. All 149 cyclovertical MN in our sample discharged in relation to vertical eye position during vertical smooth-pursuit (Mean K_v = 4.7 spk/s/°). 147 out of the 149 cyclovertical MN (35/35 IO, 27/27 SO, 41/41 SR, and 44/46 IR) modulated during vertical vergence with mean K_v of 6.2 spk/s/°. Analysis of medial rectus MNs is ongoing.

Conclusions : Our data suggests that the EOM compartments are not selectively innervated and the observed differential contractility of EOM compartments is due to other mechanisms.

This abstract was presented at the 2022 ARVO Annual Meeting, held in Denver, CO, May 1-4, 2022, and virtually.