Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys

Abstract

Eye muscle fibers can be divided into two categories: nontwitch, multiply innervated muscle fibers (MIFs), and twitch, singly innervated muscle fibers (SIFs). We investigated the location of motoneurons supplying SIFs and MIFs in the six extraocular muscles of monkeys. Injections of retrograde tracers into eye muscles were placed either centrally, within the central SIF endplate zone; in an intermediate zone, outside the SIF endplate zone, targeting MIF endplates along the length of muscle fiber; or distally, into the myotendinous junction containing palisade endings. Central injections labeled large motoneurons within the abducens, trochlear or oculomotor nucleus, and smaller motoneurons lying mainly around the periphery of the motor nuclei. Intermediate injections labeled some large motoneurons within the motor nuclei but also labeled many peripheral motoneurons. Distal injections labeled small and medium-large peripheral neurons strongly and almost exclusively. The peripheral neurons labeled from the lateral rectus muscle surround the medial half of the abducens nucleus: from superior oblique, they form a cap over the dorsal trochlear nucleus; from inferior oblique and superior rectus, they are scattered bilaterally around the midline, between the oculomotor nucleus; from both medial and inferior rectus, they lie mainly in the C-group, on the dorsomedial border of oculomotor nucleus. In the medial rectus distal injections, a "C-group extension" extended up to the Edinger-Westphal nucleus and labeled dendrites within the supraoculomotor area. We conclude that large motoneurons within the motor nuclei innervate twitch fibers, whereas smaller motoneurons around the periphery innervate nontwitch, MIF fibers. The peripheral subgroups also contain medium-large neurons which may be associated with the palisade endings of global MIFs. The role of MIFs in eye movements is unclear, but the concept of a final common pathway must now be reconsidered.

Morphology, Intrinsic Membrane Properties, and Rotation-Evoked Responses of Trochlear Motoneurons in the Turtle

“…However, whether the size principle operates in the ocular motor system remains unclear. Many studies have found the correlation between measures of ocular motoneuron size and recruitment order to be weak or nonexistent (Delgado-Garcia et al 1986;Fuchs et al 1988;Pastor and Gonzalez-Forero 2003;Pastor et al 1991). Yet a relatively strong correlation is observed in the data shown in Fig.…”

“…In these studies, synaptic responses were evoked by electrical stimulation of afferent pathways when they were examined at all. As a rule, studies of the VOR employing natural stimulation have been restricted to extracellular recording (Blanks et al 1978;Delgado-Garcia et al 1986;Fuchs et al 1988;Pastor and Gonzalez-Forero 2003;Pastor et al 1991).…”

“…In these studies, synaptic responses were evoked by electrical stimulation of afferent pathways when they were examined at all. As a rule, studies of the VOR employing natural stimulation have been restricted to extracellular recording (Blanks et al 1978;Delgado-Garcia et al 1986;Fuchs et al 1988; Pastor and Gonzalez-Forero 2003; Pastor et al 1991).Our laboratory is studying vestibuloocular physiology using an in vitro preparation consisting of the intact brain stem of the pond turtle with attached temporal bones (Ariel et al 2004;Fan et al 1997;Jones and Ariel 2006). Because of the extraordinary resistance to hypoxia exhibited by the turtle, the brain can be isolated in this fashion, facilitating the use of intracellular recording techniques.…”

Recruitment Order of Cat Abducens Motoneurons and Internuclear Neurons

“…We describe a homogeneous response in recruitment properties of abducens neurons to TeNT applications, whereas on the basis of muscle histochemistry Porter 1981, 1988) and retrograde tracing (Büttner-Ennever et al 2001) at least two types of motoneurons-twitch and nontwitch-could exist. More recently, transneuronal rabies virus tracing, in primates, suggests differences in the afferent inputs to those two likely types of motoneurons (Büttner-Ennever et al 2002).…”

Ocular motor nerve palsies: implications for diagnosis and mechanisms of repair

“…Disparity between the repair of saccade speed and the persistence of defective ranges of abduction may be due to the selective nature of the nerve fibres damaged or the tempo of their regeneration and remyelination. Large motoneurons within the abducens nucleus innervate singly innervated, twitch muscle fibres, whereas smaller motoneurons around its periphery innervate multiply innervated, non-twitch muscle fibres (Buttner-Ennever et al, 2001. Normal speed but restricted duction might be explained by either predominant damage to nerve fibres from non-twitch nerve fibres motoneurons just outside the abducens nucleus, or by better repair of nerve fibres from twitch motoneurons within the nucleus.…”