Examination of feline extraocular motoneuron pools as a function of muscle fiber innervation type and muscle layer

Abstract

This study explores two points related to the pattern of innervation of the extraocular muscles. First, species differences exist in the location of the motoneurons supplying multiply innervated fibers (MIFs) and singly innervated fibers (SIFs) in eye muscles. MIF motoneurons are located outside the extraocular nuclei in primates, but are intermixed with SIF motoneurons within rat extraocular nuclei. To test whether this difference is related to visual capacity and frontal placement of eyes, we injected retrograde tracers into the medial rectus muscle of the cat, a highly visual nonprimate with frontally placed eyes. Distal injections labeled smaller MIF motoneurons located ventrolaterally and rostrally within the oculomotor nucleus (III). More central injections also labeled a separate population of larger cells located dorsally in III. Thus, the cat shares with the nocturnal rat the feature of having MIF motoneurons located within the bounds of III. On the other hand, just as with monkeys, cats show segregation of the MIF and SIF medial rectus motoneuron pools, albeit in a different pattern. Second, extraocular muscles are divided into two layers; the inner, global layer inserts into the sclera, and the outer, orbital layer inserts into the connective tissue pulley. To test whether these layers are supplied by anatomically discrete motoneuron pools, we injected tracer into the orbital layer of the cat lateral rectus muscle. No evidence of either morphological or distributional differences was found, suggesting that the functional differences in these layers may be due mainly to their orbital anatomy, not their innervation. J. Comp. Neurol. 000:000–000, 2016.

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

“…In primates, SIF motoneurons are large cells found within the extraocular motor nuclei, while MIF motoneurons are small cells found just outside the nuclear borders (Wasicky et al, ; Erichsen et al, ; Bohlen et al, ). In cat, medial rectus SIF and MIF motoneurons are both found within III, albeit in anatomically separate subgroups, and MIF motoneurons are smaller (Bohlen et al, ). In rats, the MIF and SIF motoneurons are intermixed within III, but partially separate in VI (Eberhorn et al, ).…”

“…On the other hand, the rat study indicates that there is considerable overlap in the somatic sizes of the histochemically defined MIF and SIF motoneuron populations like that seen here (Eberhorn et al, ). Previous studies used injections of the muscle insertion to specifically label MIF motoneurons, due to the fact the axons supplying MIFs extend to the insertion and produce palisades (Büttner‐Ennever et al, ; Wasicky et al, ; Bohlen et al, ). We did not approach this question by injecting the muscle insertions due to the fact that mouse MIFs lack palisade endings (Blumer et al, ), which results in the location of the MIF and SIF terminals being much closer together.…”

“…Furthermore, MIF motoneurons are smaller than SIF motoneurons (Büttner‐Ennever et al, ; Erichsen et al, ). In cats, the motoneurons supplying the MR lie in two pools within III, one of which contains smaller cells and preferentially supplies MIFs (Bohlen et al, ). Eberhorn et al, () extended the primate findings by showing that SIF and MIF motoneurons differ histochemically.…”

Palisade Endings of Extraocular Muscles Develop Postnatally Following Different Time Courses

“…7,9 MIFs exhibit a nontwitch form of contraction and in frontal-eyed species, the cell bodies of MIF motoneurons lie separated in the EOM motor nuclei, although the specific pattern of arrangement is different across species. 13,14 Their location at the muscle-tendon junction has placed palisade endings for many years as candidates for providing eye position signals. 7,9,11,15 Their sensory role has been put into question when molecular analyses and neuronal tracing studies have demonstrated that palisade endings are cholinergic and originate from the EOM motor nuclei, most likely from MIF motoneurons.…”

Neuroanatomie des okulomotorischen Systems

“…Extraokuläre Muskelfasern lassen sich prinzipiell in 2 Gruppen aufteilen, einfach innervierte, schnelle und mehrfach innervierte, langsame Muskelfasern [6]. Diese beiden Gruppen werden durch unterschiedliche Motoneurone versorgt [6][7][8][9][10]. Die einfach innervierten, schnellen Muskelfasern sind die klassisch bekannten Muskelfasern, bei denen man davon ausgeht, dass sie alle Augenbewegungen ausführen.…”