Paradoxical responses of cyclovertical motoneurons during asymmetrical vertical vergence

Abstract

Purpose : A majority of lateral and medial rectus motoneurons paradoxically discharge in relation to movement of both eyes during asymmetric horizontal vergence even though they only innervate the ipsilateral eye muscles. Here we describe activity of cyclovertical motoneurons during asymmetrical vertical vergence in non-human primates.

Methods : Binocular eye movements were recorded as two non-human primates performed a vertical vergence task in which only one eye moved (asymmetrical vertical vergence). Single cell activity of motoneurons in the oculomotor and trochlear nuclei were recorded. Oculomotor motoneuron subdivisions were differentiated by their increase in activity with eye movement in a preferred direction and also by using microstimulation techniques. We categorized each motoneuron as either monocular or binocular using an ocular selectivity index derived from their position sensitivity to movement of the innervated and non-innervated eyes [OSI = (K_inn - K_non-inn)/(K_inn + K_non-inn)].

Results : 32/49 cyclovertical motoneurons (6 superior rectus (SR)), 10 inferior rectus (IR), 4 inferior oblique (IO) and 12 superior oblique (SO) showed activity that modulated with movement of only the innervated eye and were classified as monocular (Mean OSI = 0.61±0.17). However, 17/49 motoneurons (3 SR, 5 IR, 5 IO and 4 SO) modulated with movement of both innervated and non-innervated eyes and were classified as binocular (mean OSI = 0.14±0.10). Position sensitivity of monocular cells was 5.5 spk/s/° (IR), 8.9 spk/s/° (SO), 7.1 spk/s/° (SR) and 6.8 spk/s/° (IO). Activity of these cells modulated very weakly in correlation with the non-innervated eye (1.4 spk/s/°). For binocular motoneurons mean sensitivity with respect to the innervated and non-innervated eyes were not significantly different (K_inn=6.8 spk/s/°; K_non-inn=5.7 spk/s/°; p>0.05).

Conclusions : Motoneurons innervate only one muscle and it is therefore paradoxical that 35% of cyclovertical motoneurons encode movement of both eyes, challenging the concept of a “final common pathway”. Our data on cyclovertical motoneurons are remarkably similar to the data on horizontal motoneuron responses during asymmetric horizontal vergence. Note that an equivalent way of describing the data would be to report unequal conjugate and vergence sensitivities for the cyclovertical motoneuron population and the existence of a premotor control center for vertical vergence.

This is a 2020 ARVO Annual Meeting abstract.