How does the structure of extraocular muscles and their nerves affect their function?

Abstract

The sensory and motor control of human extraocular muscles (EOMs) have been subjected to considerable speculation in ophthalmic literature, often related to infranuclear structures such as the unique complement of muscle fibres and their associated sensory organs. The intrafusal fibres do not resemble their somatic counterparts and their peculiar morphology has raised questions about their proprioceptive capacity. No Golgi tendon organs have so far been observed and the myotendinous nerve endings, previously assumed to convey sensory information, have recently been argued to merely represent constituents of the efferent innervation serving the multiply innervated muscles fibres. These observations raise questions about the overall capacity to monitor the activity created by the generous efferent nerve supply observed in these muscles. Furthermore, the argued independent activity of muscular layers and compartments suggest that the required feedback must be highly structured and more specific than previously assumed. Yet, uncertainty about the source of such information remains. The purpose of this paper is to provide a short review of neuromuscular properties of human extraocular muscles. Their functional implications and the most reputable sources of proprioception will also be discussed. The promoted views are based on pertinent literature and previous research undertaken by the authors.

Neuroanatomical Structures in Human Extraocular Muscles and Their Potential Implication in the Development of Oculomotor Disorders

“…Recent studies on sensory information from extraocular muscles have suggested that proprioception participates in space localization and that individuals with strabismus may have deficits in this particular function. 7,[20][21][22][23]…”

A Subset of Palisade Endings Only in the Medial and Inferior Rectus Muscle in Monkey Contain Calretinin

“…The amount and even the presence of proprioceptors vary not only between different species, 1 , 3 , 14 , 15 but even between the eye muscles themselves. 16 – 18 In addition, the extraocular muscles contain a unique type of nerve ending, the palisade endings, that could fulfill such a proprioceptive function. A sensory role is supported by the location of palisade endings at the myotendinous junction with mainly neurotendinous contacts 19 and their resemblance to immature Golgi tendon organs.…”

One-to-one innervation of vocal muscles allows precise control of birdsong

“…We quantified the mean IN (INmean) of syringeal muscles in male zebra finches by counting i) the number of muscle fibers and ii) the number of axons in the supplying ipsilateral nerve single superfast syringeal muscle fiber. Such one-to-one innervation has to our knowledge only been reported for monkey extraocular muscle [24] and one motor neuron of the mouse interscutularis muscle [25] and provides the nXIIts motor pool with the highest control resolution possible in the vertebrate nervous system. 100 500 Hz stimulations.…”

“…However, instead we observe extremely small MUs (13 -17% of all MUs are innervated one-to-one), which strongly suggests an additional selection for small MUs. MU innervation numbers below 10 are on the extremely low end of MU sizes in 220 vertebrates, and have so far only been reported for laryngeal [19,47], extraocular [20,24] and ear muscles [25]. Interestingly, all those muscles belong to the craniofacial lineage [27] suggesting that their developmental origin might predispose them or even provide unique access to low MU sizes.…”