The Extraocular Muscles

Gross anatomy

There are six EOM in each orbit whose function is to move the eyes: four rectus muscles, superior, medial, inferior, and lateral; and two oblique muscles, inferior and superior ( Fig. 7.3 ). In addition there is a seventh skeletal muscle in each orbit, the levator palpebrae superioris, which inserts into the upper eyelid and functions in elevating the palpebral fissure. While its cranial nerve innervation is similar to the EOM, functionally and metabolically it is distinct, and will not be discussed further in this chapter.

The four rectus muscles take their origin in part from the bones at the apex of the orbit, but also from the tendinous annulus. They course anteriorly to insert into the sclera anterior to the equator of the globe, a key factor when considering their functional effects on eye movements. Classically this insertion is described as external to the ora serrata; however, recent studies demonstrate that insertions of the rectus muscles range from 2.25 mm posterior to 2.25 mm anterior to the ora serrata, with 90 percent of the insertions within 1 mm. Generally considered to be tendinous at the insertion site, the medial and lateral rectus muscles in humans may contain myofibers that extend directly to the sclera, an important consideration for incisional strabismus surgery. The insertions of the four rectus muscles increase in distance from the corneal limbus circumferentially, with the medial rectus closest and the superior rectus furthest. The distances were originally determined on cadaveric material; however, recent analyses on living adult patients during strabismus surgery show that the average distances from the corneal limbus to the rectus muscle insertions have large inter-individual variations. In part, this explains the disparate measurements seen in the literature. One typical study measured the distances from the limbus to muscle insertion as 6.2 ± 0.6 mm for the medial rectus, 7.0 ± 0.6 mm, for the inferior rectus, 7.7 ± 0.7 mm for the lateral rectus, and 8.5 ± 0.7 mm for the superior rectus. Distances can vary up to 4 mm, even between the same muscles in both eyes of one patient, and does not correlate with primary position of the eye or surgical success for strabismus patients. Thus, there is a significant amount of variation in rectus muscle insertions, and this variability has important consequences for incisional surgery of the EOM.

The superior and inferior oblique muscles have distinct paths compared to the rectus muscles. The superior oblique takes its origin from the dense connective tissue periosteum lining the orbit just superior and medial to the attachment of the tendinous annulus, and courses anteriorly along the border between the orbital roof and the medial orbital wall. Approximately 10–15 mm posterior to the orbital margin it becomes tendinous and enters the trochlea, a cartilaginous and dense connective tissue structure attached to the orbital periosteum. Emerging from the trochlea, the superior oblique muscle passes posteriorly at a 51° angle to the axis of the eye in primary position and inserts into the sclera. The trochlea thus serves as the “de facto” origin, creating the vector of force that moves the globe. The insertion of the superior oblique is on the superior pole deep to the superior rectus muscle, but in contrast to the rectus muscles, posterior to the equator of the globe ( Fig. 7.3 ). The inferior oblique muscle is the only EOM that does not take its origin from the apex of the orbit; instead originating from the anteromedial orbital floor. The inferior oblique muscle courses posteriorly and inferior to the inferior rectus and inserts into the sclera posterior to the equator of the globe.

The shape, size, and orientation of the EOM from origin to insertion form the basis for the eye movements that result from their contraction ( Table 7.1 ). While the effect of contraction of each EOM will be described separately, it is important to remember that they work in a coordinated fashion, maintaining significant tension or “tonus” even when the eye is in primary position and thus presumably “at rest”.

Horizontal movements are controlled by the medial and lateral rectus muscles, agonist–antagonist pairs with opposing primary functions; the medial rectus adducts the eye, while the lateral rectus abducts the eye. Vertical movements are more complex. The superior and inferior rectus muscles have a more complex effect on the direction of eye movements because the bony orbits are not parallel to each other ( Fig. 7.2 ). In primary gaze, both the superior and inferior recti are angled laterally at approximately 22.5° from the sagittal plane. The primary action of the superior rectus muscle is elevation, but it also adducts and intorts the eye ( Table 7.1 , Fig. 7.4 ). Intorsion is where the superior pole of the eye rotates medially. Thus, if the superior rectus muscle was acting alone, the direction of gaze would be superior and medial, that is, up and in towards the nose. The inferior rectus is parallel to the superior rectus, but inserts on the inferior surface of the globe. Thus, it primarily depresses the eye, but also adducts and extorts ( Fig. 7.4 ); extorsion is rotation of the superior pole of the eye laterally.

Due to its insertion posterior to the equator of the globe, as well as the vector of force directed by the position of the trochlea in the superior and medial orbit, the superior oblique mainly intorts the eye ( Table 7.1 , Fig. 7.4 ). It also depresses and abducts. Thus, working unilaterally, gaze would be directed down and out. As the inferior oblique muscle parallels the superior oblique, but inserts on the inferior surface of the globe, its primary function is extorsion of the eye ( Table 7.1 , Fig. 7.4 ); it also elevates and abducts. In order for accurate positioning of the visual world on the fovea, activity of all the EOM must be tightly coordinated.

Cranial motor nerve innervation

The optic foramen is found within the lesser wing of the sphenoid bone at the orbital apex, through which runs the optic nerve (cranial nerve II, CNII) and ophthalmic artery. Between the greater and lesser wings of the sphenoid is the superior orbital fissure. The structures entering the orbit through this fissure are divided by the tendinous annulus (formerly the annulus of Zinn). Structures that enter the orbit superior to the annulus are the lacrimal and frontal nerves, both sensory branches of the ophthalmic division of the trigeminal nerve (CNV); the trochlear nerve (CNIV), motor nerve to the superior oblique muscle; and the superior ophthalmic veins ( Fig. 7.5 ). Once through the annulus, structures enter what is referred to as the muscle cone, and are surrounded by the EOM and their connective tissue ensheathments. Within the annulus, the superior orbital fissure admits the superior and inferior divisions of the oculomotor nerve (CNIII) the motor nerve to the inferior rectus, inferior oblique, medial rectus, superior rectus and levator palpebrae superioris muscles; the nasociliary nerve which is a sensory branch of the ophthalmic division of the trigeminal nerve (CNV), and the abducens nerve (CNVI), the motor nerve to the lateral rectus muscle. On the floor of the orbit is the inferior orbital fissure, which admits the zygomatic nerve, a sensory nerve innervating the lateral mid-face; communications of the inferior ophthalmic vein with the pterygoid plexus of veins inferiorly; and the lacrimal rami, carrying parasympathetic innervation from the facial nerve (CNVII) to the lacrimal gland.

Once inside the bony orbit, the motor nerve branches of CNIII, CNIV and CNVI course anteriorly towards the muscles they innervate. The superior division of CNIII innervates the superior rectus muscle and continues superiorly to innervate the levator palpebrae superioris. The inferior division of CNIII innervates the medial and inferior rectus muscles, and the latter branch continues inferiorly to innervate the inferior oblique. All nerve branches enter the muscles on their deep surfaces within the muscle cone. CNVI also enters the lateral rectus muscle on its deep surface. Of the motor nerves, only the trochlear nerve, CNIV, enters the orbit outside the tendinous annulus innervating the superior oblique muscle on its superior or lateral surface ( Fig. 7.5 ). All motor nerves that innervate the EOM enter the body of the muscles at their posterior third ( Fig. 7.5 ).

Neuromuscular junctions (NMJ) are the specialized sites of communication between a nerve and the myofibers it innervates. In non-cranial skeletal muscle, NMJs usually form in the middle one-third of each myofiber. The NMJs formed by the cranial motor nerves with individual EOM myofibers display some distinct differences compared to those in non-cranial skeletal muscle. Similar to body muscles, the EOM have singly innervated myofibers with NMJs referred to as “en plaque” endings ( Fig. 7.6 ). However, the “en plaque” NMJs in EOM are smaller and less complicated structurally than those in non-cranial skeletal muscles. In addition, the EOM have multiply innervated myofibers with neuromuscular junctions referred to as “en grappe” endings ( Fig. 7.6 ). These are a linear array of small synaptic contacts often found towards the ends of individual myofibers, but can be continuous along the length of individual myofibers. The “en grappe” NMJ contacts are structurally simple. Thus, in EOM a single myofiber can have an “en plaque” NMJ somewhere along the middle one-third and also have multiple “en grappe” endings along the tapered ends ( Fig. 7.6 ). Some myofibers in EOM that express the slow tonic myosin heavy chain isoform (MYH14) have “en grappe” endings along their entire myofiber length and do not have an “en plaque” ending.

The acetylcholine receptor found within NMJs is composed of 5 subunits, similar to skeletal muscle generally. In developing non-cranial muscle there are two alpha, 1 beta, 1 gamma, and 1 delta subunits (α2βγδ), and in the adult the γ subunit is replaced with the epsilon (ε) subunit. In contrast, in adult EOM the majority of the “en grappe” endings express the “immature” gamma subunit, rather than the epsilon subunit of mature endings. Both the “en plaque” and “en grappe” endings in the EOM can co-express both the epsilon and gamma subunits; this appears to be unique to EOM. Due to the nature of EOM myofiber length, as discussed in a following section, NMJs can be seen throughout the origin-to-insertional length of EOM in most species where this has been examined. This is in contrast to most limb skeletal muscles, which have a motor endplate zone, an NMJ band that is fairly contained within a defined area in the midbelly region of the muscle.

It has generally been assumed that the multiply innervated myofibers are innervated by a single motor neuron, but polyneuronally innervated myofibers are also present. This means that more than one motor neuron can innervate a single myofiber. This has important implications for EOM physiology and will be discussed in that section.

Orbital connective tissue

A complex framework of connective tissue exists throughout the orbit, and this network has a clear structural organization and constant pattern ( Fig. 7.7 ). These connective tissue septa contain nerves, vessels and smooth muscle, and are postulated to play a role in supporting eye movements. Recent studies have confirmed and extended these initial detailed analyses of orbital connective tissue septa to include thickenings around individual EOM called orbital pulleys ( Fig. 7.7 ). These connective and smooth muscle septa and bands constrain the paths of the EOM, changing the vector of force as the EOM contract and stabilize muscle position during movement.