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

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Coordinated eye movements are used to direct the eyes to targets of interest and to maintain this relationship in the face of external perturbations. This system has been used as a model to study motor control because of our capacity to measure eye movements precisely, the simplicity of its anatomy (only six extraocular muscles per eye), a relatively constant load during eye movements and because the central anatomical connections controlling eye movements are well established. Despite these points, the etiology of eye movement disorders, such as strabismus, is not well understood (Leigh and Zee, 2015). To address this problem better, it is critical that we fully understand the anatomy of both the oculomotor plant and the circuits directing it. One challenge to achieving this understanding is the complexity of the extraocular muscles. The fibers in these muscles are highly specialized, with a wide range of biochemical and morphological fiber subtypes present in each extraocular muscle. Furthermore, they are differentially arranged in two layers (Spencer and Porter, 2006).
Mammalian extraocular muscle innervation patterns are idiosyncratic compared with most skeletal muscles because there are two different patterns by which their fibers receive axonal input from motoneurons. The most common extraocular muscle fiber class is the singly innervated fiber (SIF). Each SIF is contacted by a large‐diameter, heavily myelinated axon that forms a single en plaque endplate, which is typical in most skeletal muscles. These endplates form a band across the middle one‐third of the muscle (Büttner‐Ennever et al., 2001; Namba et al., 1968a). Excitation of the SIF axons by electrical or pharmacological means produces an all‐or‐nothing response in the muscle fiber, resulting in a twitch (Bach‐y‐Rita and Ito, 1966; Bach‐y‐Rita et al., 1977; Bondi and Chiarandini, 1983; Chiarandini, 1976; Chiarandini and Davidowitz, 1979; Jacoby et al., 1989). Based on these properties and their histochemical and ultrastructural features, SIFs are categorized as fast‐twitch, relatively fatigueable, large‐diameter fibers (Spencer and Porter, 2006). The second, less common class is the multiply innervated fiber (MIF). In this case, a thin axon supplies the target fiber with numerous, small boutonal terminals organized in an en passant and, occasionally, an en grappe manner. These boutons are distributed along the length of each muscle fiber from origin to insertion (Büttner‐Ennever and Horn, 2002; Büttner‐Ennever et al., 2001; Eberhorn et al., 2006; Namba et al., 1968a). Excitation of MIF axons is believed to produce a slow, graded response in the muscle fiber (Nelson et al., 1986). Given their physiological, histochemical, and ultrastructural features, MIFs are categorized as nontwitch, highly fatigue‐resistant, small‐diameter fibers (Bach‐y‐Rita and Ito, 1966; Bach‐y‐Rita et al., 1977; Bondi and Chiarandini, 1983; Chiarandini, 1976; Chiarandini and Davidowitz, 1979; Jacoby et al., 1989; Spencer and Porter, 2006). This type of fiber is rare in mammals, but has been reported for other small muscles, including the stapedius, tensor tympani, vocalis, and pharyngeal muscles (for reviews see Morgan and Proske, 1984; Schiaffino and Regioni, 2011).
Büttner‐Ennever and Akert (1981) and Porter et al. (1983) used retrograde tracers to label separate, muscle‐specific pools of motoneurons in the monkey oculomotor nucleus (III) and noted that, in some cases, more than one pool was labeled for a specific muscle. More recently, Büttner‐Ennever and colleagues (2001) used tracer injections into the distal portion of the muscle to limit tracer uptake to the axons supplying MIFs. They found that MIF motoneuronal populations in monkeys were anatomically segregated from the SIF motoneuronal populations. Specifically, MIF motoneurons are smaller cells peripheral to the cytoarchitectonically defined extraocular motor nuclei, whereas SIF motoneurons are larger cells residing within them (Büttner‐Ennever and Horn, 2002; Büttner‐Ennever et al., 2001; Wasicky et al., 2004).
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