Palisade endings in extraocular eye muscles revealed by SNAP‐25 immunoreactivity

Abstract

Palisade endings form a cuff of nerve terminals around the tip of muscle fibres. They are found only in extraocular muscles, but no definite evidence for their role in eye movements has been established. Palisade endings have been reported in all species so far investigated except the rat. In this study we demonstrate that antibodies against SNAP-25, the synaptosomal associated protein of 25 kDa, reliably visualize the complete motor, sensory and autonomic innervation of the extraocular muscles in human, monkey and rat. The SNAP-25 antibody can be combined with other immunofluorescence procedures, and is used here to study properties of palisade endings. With SNAP-25 immunolabelling putative palisade endings are identified in the rat for the first time. They are not well branched, but fulfil several criteria of palisade endings, being associated with non-twitch fibres as shown by double labelling with 'myosin heavy chain slow-twitch' antibodies. The putative palisade endings of the rat lack alpha-bungarotoxin binding, which implies that these synapses are sensory. If palisade endings are sensory then they could function as an eye muscle proprioceptor. They seem to be a general feature of all vertebrate eye muscles, unlike the other two extraocular proprioceptors, muscle spindles and Golgi tendon organs, the presence of which varies widely between species.

A central mesencephalic reticular formation projection to medial rectus motoneurons supplying singly and multiply innervated extraocular muscle fibers

“…Palisade endings were assumed to be sensory structures, compensating for a general lack of conventional proprioceptive receptors (muscle spindles) in the extraocular musculature (Billig, Buisseret-Delmas, & Buisseret, 1997; Donaldson, 2000; Ruskell, Kjellevold Haugen, Bruenech, & van der Werf, 2005; Steinbach, 1987; Weir, Knox, & Dutton, 2000). However, palisade endings also show features that correlate with a motor function: for example, they contain vesicles and are immunoreactive for cholinergic markers (Blumer et al, 2009; Eberhorn et al, 2005; Konakci et al, 2005a, 2005b; Lukas et al, 2000). Furthermore, injections of anterograde tracer into the extraocular motor nuclei label palisade endings, indicating the source of these features lies in the MIF motoneuron pools (Lienbacher, Mustari, Ying, Büttner-Ennever, & Horn, 2011; Zimmermann, May, Pastor, Streicher, & Blumer, 2011; Zimmermann et al, 2013).…”

Evidence that the extraocular motor nuclei innervate monkey palisade endings

“…Several studies support a sensory role of this EOM specific organ [1,2,6,8,9,20]. Specifically, fine structure studies demonstrated that all palisade endings, with the exception of rat's [9] and rabbit's [5], established contacts with the tendon [1,3,4,12,19,21]. In Golgi tendon organs, analogous nerve contacts are sensory [23].…”

Palisade Endings of Extraocular Muscles Develop Postnatally Following Different Time Courses

“…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.…”

“…[7][8][9] Palisade endings are regularly present in the EOMs of frontal-eyed species (human, monkey, cat, dog, and ferret) but infrequent in lateral-eyed species (i.e., they are present in ungulates [pig, cow, horse, and sheep] and rabbit), but absent in most rodents. [10][11][12] Palisade endings are located at the myotendinous junction and formed by nerve fibers that come in from the muscle and extend into the tendon. There, axons make a u-shaped turn, branch, and establish terminal varicosities at the tendon level and around single muscle fiber tips.…”