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How Does the Structure of Extraocular Muscles and Their Nerves

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How Does the Structure of Extraocular Muscles and Their Nerves Eye (2015) 29, 177–183 & 2015 Macmillan Publishers Limited All rights reserved 0950-222X/15 www.nature.com/eye 1 2 How does the JR Bruenech and IB Kjellevold Haugen CAMBRIDGE OPHTHALMOLOGICAL SYMPOSIUM structure of extraocular muscles and their nerves affect their function? Abstract understanding the sensorimotor control of eye movements, yet uncertainty associated with both The sensory and motor control of human afferent and efferent modalities persists. The extraocular muscles (EOMs) have been distribution and complement of sensory organs is subjected to considerable speculation in unique compared with conventional somatic ophthalmic literature, often related to muscles,1 and large interspecies variations have infranuclear structures such as the unique been observed.2 This has created controversy complement of muscle fibres and their about the role of proprioception and has associated sensory organs. The intrafusal fibres challenged the notion that it participates in the do not resemble their somatic counterparts development of binocular vision, ocular and their peculiar morphology has raised alignment, and adaptive processes.3 Furthermore, questions about their proprioceptive capacity. recent observations suggest that EOMs are No Golgi tendon organs have so far been compartmentalised, not only into global and observed and the myotendinous nerve 1 orbital layers,4,5 butalsointosuperiorand Biomedical Research Unit, endings, previously assumed to convey Faculty of Health Sciences, inferior compartments of horizontal rectus sensory information, have recently been Buskerud and Vestfold muscles.6–9 This implies a broader division of argued to merely represent constituents of the University College, Campus labour between muscle segments than previously efferent innervation serving the multiply Kongsberg, Kongsberg, assumed, which in turn should require a highly Norway innervated muscles fibres. These observations structured and specific neural feedback. Whether raise questions about the overall capacity to 2 this feedback is provided by proprioception or Institute for Biomedical monitor the activity created by the generous Sciences, Oslo, Norway other mechanisms is still unresolved. This paper efferent nerve supply observed in these aims to review current concepts of motor and muscles. Furthermore, the argued independent Correspondence: sensory innervation of human EOMs, and activity of muscular layers and compartments JR Bruenech, Biomedical comment on their functional implications. suggest that the required feedback must be Research Unit, Faculty of References will be made to pertinent literature Health Sciences, Buskerud highly structured and more specific than and previous research undertaken by the authors. and Vestfold University previously assumed. Yet, uncertainty about the College, Campus source of such information remains. The Kongsberg, PO 235, purpose of this paper is to provide a short 3603 Kongsberg, Norway review of neuromuscular properties of human Efferent innervation Tel: +4732869615; Fax: +4732890671. extraocular muscles. Their functional Analyses of the innervation of human EOMs E-mail: jan.richard.bruenech@ implications and the most reputable sources of have revealed that there is a clear correlation hbv.no proprioception will also be discussed. The between nerve fibre diameters and the distinct promoted views are based on pertinent Received: 30 September morphology of the muscle fibres they serve.10 literature and previous research undertaken by 2014 However, many of the small nerve fibres seem the authors. Accepted in revised form: to have been missed in earlier studies using 11 October 2014 Eye (2015) 29, 177–183; doi:10.1038/eye.2014.269; low-resolution techniques.11,12 In a more recent Published online: 14 published online 14 November 2014 study13 unmyelinated nerve fibres were found November 2014 to be numerous (Figure 1), constituting Introduction The work was presented at 10.2–19.3% (mean 16.1%) of the nerve fibre the Cambridge Detailed knowledge of the characteristics of population in cranial nerves obtained from Ophthalmological extraocular muscles (EOMs) is vital for seven human subjects (Figure 2). The ratio Symposium Properties of human extraocular muscles JR Bruenech and I-BK Haugen 178 Figure 1 Electron micrograph showing unmyelinated nerve fibres scattered throughout the cross-sectional area of the inferior branch of the third cranial nerve. between myelinated and unmyelinated fibres was fairly uniform in all examined nerve branches, with exception of the branch serving the levator palpebrae muscle, known to lack multiply innervated fibres (MIFs). Adjustments were made for autonomic nerve fibres, based on results from preceding observations of superior cervical ganglionectomy in monkey.14 Quantifications of the corresponding muscle fibre population indicated that MIFs, which constituted 18–23% of all fibres, have a more generous efferent supply than previously assumed. The numerical data indicated motor units as small as 1 : 1. This was supported by the absence of bifurcations, when selected nerve fibres were traced in serial sections down Figure 2 Histogram illustrating the spectrum of nerve fibre to their distal ‘en grappe’ terminations. This neural diameters in the inferior branch of the third cranial nerve. A trimodal distribution was apparent in all branches. The first arrangement, the modest amounts of sarcoplasm among peak encompasses the majority of all unmyelinated nerves fibres myofibrils (Figure 3) and the absence of MIFs in the (r1 mm). levator palpebrae muscle, supports the consensus that they provide the fine-tuned tonic activity needed in regarded as the principal proprioceptors in human 15,16 ocular alignment and eye fixation. The consent has EOMs for many years. The notion that these unique, been strengthened through more recent studies using so-called palisade endings have a sensory function was tracer injections in non-human primates, indicating that supported through clinical studies, where transient peripheral motor neurones innervating non-twitch MIFs disruption of the assumed proprioceptive pathway receive inputs from premotor neurones involved in caused binocular vision anomalies.21 Structural 17,18 smooth pursuit, convergence, and gaze holding. It is irregularities observed in nerve endings from strabismus therefore of special interest that many of the MIFs, which patients provided additional support and indicated that seem to have a one-to-one relationship with their efferent these receptors were implicated in the pathogenesis of unmyelinated nerve fibres, also have nerve terminals at oculomotor disorders.22 In a study by Bruenech and their distal end (described below). Ruskell,23 three varieties of nerve endings were described in the EOMs of six adult and five infant humans. The most frequently occurring structure consisted of a single Afferent innervation recurrent myelinated nerve fibre that branched and terminated in between the muscular processes at the Myotendinous nerve endings distal end of the muscle fibres (Figure 4a). Varicosities Myotendinous nerve terminals, first reported by Dogiel19 containing vesicles and mitochondria occurred at regular and later described in detail by Richmond et al,20 were intervals. The capsule, enveloping the myotendinous Eye Properties of human extraocular muscles JR Bruenech and I-BK Haugen 179 Figure 3 Electron micrograph showing a multiply innervated muscle fibre with small amounts of sarcoplasmic reticulum, surrounded by singly innervated muscle fibres. An unmyelinated, pre-terminal nerve fibre is in close vicinity of the muscle fibre. compartments, was thin and composed of fibroblast-like motor nuclei of EOMs.32,33 Even though it cannot be cells rather than extensions of perineurium of the nerve precluded that myotendinous nerve endings have a fibre as seen in muscle spindles. These features were sensory function,2,34 the notion that muscle spindles collectively referred to as myotendinous cylinders represents the only structures with proprioceptive (MTCs) because of their resemblance to distal nerve potency seem to gain growing support.35 terminals previously observed in monkey,24 later also found in proximal tendons.25 In some cases the capsule Muscle spindles was incomplete or absent, allowing nerve endings to be dispersed in tendon and occasionally terminate on more Muscle spindles in human EOMs differ morphologically than one muscle fibre (Figure 4b). In other cases, the from conventional somatic spindles in several ways.1,35–37 nerve fibre terminated in pure tendon in a more distal They also differ from spindles in EOMs of other location (Figures 4c and 5). All three varieties were found mammals.3 Their numbers may have been overestimated in both global and orbital muscle layers, but their in previous studies because encapsulated spindle-like distribution was patchy and scarce. It is of interest that structures, with unmodified intrafusal fibres lacking the lowest number of these structures, assumed to be sensory neuronal contacts, are also present in human sensory, was found in muscle samples from strabismus EOMs.37–39 These anomalous fibres found in so-called patients (unpublished). No Golgi tendon organs or other false spindles, are also observed in true spindles. putative receptors were observed, suggesting that MTCs Bruenech and Ruskell37 reported that 25.7% of the represent the only proprioceptive source in the intrafusal fibres in 40 spindles were anomalous, lacking myotendinous region of human EOMs.23 However, equatorial modifications and sensory
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