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.

Figure 1

Electron micrograph showing unmyelinated nerve fibres scattered throughout the cross-sectional area of the inferior branch of the third cranial nerve.

Figure 2

Histogram illustrating the spectrum of nerve fibre diameters in the inferior branch of the third cranial nerve. A trimodal distribution was apparent in all branches. The first peak encompasses the majority of all unmyelinated nerves fibres (≤1 μm).

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.

Figure 4

Illustration showing the three varieties of nerve termination observed in distal tendon. (a) The most frequently occurring terminal, the myotendinous cylinder. (b) Terminals unconfined or partially confined by a capsule. (c) Dispersed terminals from a non-recurrent nerve fibre (redrawn from Bruenech and Ruskell).

Figure 5

Electron micrograph showing both a myelinated nerve fibre and neural elements terminating in tendon, distal to the contractile material.

Figure 6

Micrograph showing a transverse section through the equatorial region of a muscle spindle. The spindle holds both intrafusal chain fibres and anomalous fibres with extrafusal features. The latter type is present both within the lumen and embedded in the capsule wall.