FIGURE 10-8

Orbital apex with globe removed. The origin of the rectus­ ­muscles at the anulus of Zinn. Motor innervation of the ­extraocular muscles and the relationship between superior orbital fissure and common tendinous ring is shown.

INSERTIONS OF THE RECTUS MUSCLES: SPIRAL OF TILLAUX

The four rectus muscles insert into the globe anterior to the equator. A line connecting the rectus muscle insertions forms a spiral, as described by Tillaux. This spiral starts at the medial rectus, the insertion that is closest to the limbus, and proceeds to the inferior rectus, the lateral rectus, and finally the superior rectus, the insertion farthest from the limbus5 (Figure 10-9). In a recent study, variations were found from person to person in specific measurements, but the spiral of Tillaux was always observed.33 The tendons of insertion pierce Tenon’s capsule and merge with scleral fibers. A sleeve of the capsule covers the tendon for a short distance, and the muscle can slide freely within this sleeve.5,13 Connective tissue extends from the insertions joining them to each other.

MEDIAL RECTUS MUSCLE

The medial rectus muscle is the largest of the extraocular muscles, with its size probably resulting from the frequency of its use in convergence.30 Its origin is from both the upper and the lower parts of the common ring tendon and from the sheath of the optic nerve. The medial rectus muscle parallels the medial orbital wall until it passes through a connective tissue pulley just posterior to the equator of the globe; at this point it follows the curve of the globe to its insertion.34 The insertion of the medial rectus is about 5.5 mm from the limbus, and the tendon is approximately 3.7 mm long5 (Table 10-2). The insertion line lies vertically such that the horizontal plane of the eye approximately bisects it (Figure 10-10, A).

Superior rectus

Inferior rectus

FIGURE 10-9

Insertions of rectus muscles forming spiral of Tillaux.

Table 10-2  Rectus Muscle Tendon of Insertion

Measurements*

*All measurements in millimeters (mm).

Modified from Eggers HM: Functional anatomy of the extraocular muscles. In Tasman W, Jaeger EA, editors: Duane’s foundations of clinical ophthalmology, Philadelphia, 1994, Lippincott.

The superior oblique muscle, ophthalmic artery, and nasociliary nerve lie above the medial rectus. Fascial expansions from the sheath of the muscle run to the medial wall of the orbit and form the well-developed medial check ligament (see Figure 8-18). The medial rectus is innervated by the inferior division of cranial nerve III, the oculomotor nerve, which enters the muscle on its lateral surface.

LATERAL RECTUS MUSCLE

The lateral rectus muscle has its origin on both limbs of the common tendinous ring and the spina recti lateralis, a prominence on the greater wing of the sphenoid bone. The lateral rectus muscle parallels the lateral orbital wall until it passes through a connective tissue pulley just posterior to the equator of the globe; at this point it follows the curve of the globe to its insertion.34,35

The insertion parallels that of the medial rectus and is approximately 6.9 mm from the limbus, and the length of the tendon is approximately 8.8 mm.5

The lacrimal artery and nerve run along the superior border of the lateral rectus muscle. The ciliary ganglion, the abducens nerve, and the ophthalmic artery lie medial to the lateral rectus between it and the optic nerve. Fascial expansions from the muscle sheath attach to the lateral wall of the orbit and form the lateral check ligament (see Figure 8-18). The lateral rectus is innervated by cranial nerve VI, the abducens nerve, which enters on the medial side of the muscle.

SUPERIOR RECTUS MUSCLE

The superior rectus muscle has its origin on the superior part of the common tendinous ring and the sheath of the optic nerve.30 The muscle passes forward beneath the levator muscle; the sheaths enclosing these two muscles are connected to each other, allowing coordination of eye movement with eyelid position and resulting in elevation of the eyelid with upward gaze. An additional band of this tissue connects to the superior conjunctival fornix. The superior rectus muscle parallels the roof of the orbit until it passes through a connective tissue pulley just posterior to the equator of the globe; at this point it follows the curve of the globe to its insertion.34,35

The insertion of the superior rectus is approximately 7.7 mm from the limbus5 and is curved slightly, with the convex side forward. The line of the insertion is oblique, with the nasal side closer to the limbus than the temporal side (see Figure 10-10, B). The tendon length is approximately 5.8 mm.5 A line drawn from the origin to the insertion along the muscle will form an angle of approximately 23 degrees with the sagittal axis.

The frontal nerve runs above the superior rectus and levator muscles, and the nasociliary nerve and the ophthalmic artery lie below. The tendon of insertion for the superior oblique muscle runs below the anterior part of the superior rectus muscle (see Figure 10-7).

The superior rectus is innervated by the superior division of the oculomotor nerve, which enters the muscle on its inferior face. Branches pass either through the muscle or around it to innervate the levator.

INFERIOR RECTUS MUSCLE

The inferior rectus muscle has its origin on the lower limb of the tendinous ring; its insertion is about 6.5 mm from the limbus in an arc, convex side forward, with the nasal side nearer the limbus; the tendon length is approximately 5.5 mm.5 The inferior rectus approximately parallels the superior rectus, making an angle of 23 degrees with the sagittal axis.

The inferior rectus muscle parallels the orbital floor until it passes through a connective tissue pulley just posterior to the equator of the globe; at this point it follows the curve of the globe to its insertion,34 which is parallel to the insertions of the superior rectus (see Figure 10-10, C).

Below the inferior rectus lies the floor of the orbit and above it is the inferior division of the oculomotor nerve. Anteriorly, the inferior oblique muscle comes between the inferior rectus and the orbital floor (see Figure 10-7). The sheaths of these two inferior muscles unite to contribute to the suspensory ligament of Lockwood (see Figure 8-17). The capsulopalpebral fascia, an anterior extension from the sheath of the inferior rectus muscle and the suspensory ligament, inserts into the inferior edge of the tarsal plate, allowing coordination of eye movements with eyelid position and ensuring lowering of the lid on downward gaze.36 The inferior rectus is innervated by the inferior division of cranial nerve III, the oculomotor nerve, which enters the muscle on its superior surface.

SUPERIOR OBLIQUE MUSCLE

The superior oblique muscle has its origin on the lesser wing of the sphenoid bone, medial to the optic canal near the frontoethmoid suture.17 The muscle courses forward and passes through the trochlea, a U-shaped piece of cartilage attached to the orbital plate of the frontal bone (see Figure 10-7). The tendon of insertion actually begins approximately 1 cm posterior to the trochlea. Normally, no connective adhesions exist between these two structures, allowing the tendon to slide easily through the trochlea.1

The superior oblique muscle is the longest and thinnest of the extraocular muscles because of its long (2.5 cm) tendon of insertion.30 The tendon of insertion changes direction as it passes through the trochlea to run in a posterior direction and lies inferior to the superior rectus muscle. The insertion of the superior oblique muscle attaches in the superoposterior lateral aspect of the globe37 and is fan shaped, concave forward, and oblique (see Figure 10-10, B).

The trochlea is considered the physiologic or effective origin of the superior oblique muscle in determining muscle action because it acts as a pulley and changes the direction of muscle pull. In considering the action of the superior oblique, a line is drawn from the trochlea to the insertion rather than from the anatomic origin to the insertion. A line drawn from the physiologic origin to the insertion makes an angle of approximately 55 degrees with the sagittal axis.37 The superior oblique muscle lies above the medial rectus, with the nasociliary nerve and the ophthalmic artery lying between them. Innervation is by the trochlear

Table 10-3  Extraocular Muscle Innervation

nerve, cranial nerve IV, which enters the posterior area of the muscle.

INFERIOR OBLIQUE MUSCLE

The inferior oblique muscle has its origin on the maxillary bone just posterior to the inferior medial orbital rim and lateral to the nasolacrimal canal.38 The inferior oblique is the only extraocular muscle to have its anatomic origin in the anterior orbit. The muscle runs from the medial corner of the orbit to the lateral aspect of the globe, its length approximately paralleling the tendon of insertion of the superior oblique muscle.

The insertion of the inferior oblique is on the posterior portion of the globe on the lateral side, mostly inferior, lying just outer to the macular area (see Figure­ 10-10, D).1,30 The insertion is curved concave downward, the tendon of insertion is quite short, just 1 mm in length. The muscle makes an angle of approximately 51 degrees with the sagittal axis.34 Above the inferior oblique are the inferior rectus and globe, and below it lies the floor of the orbit. The inferior oblique is innervated by the inferior division of the oculomotor nerve, which enters the muscle on its upper surface.

Table 10-3 lists the motor innervation of the extraocular muscles.

FIBERS OF THE EXTRAOCULAR MUSCLES

The fibers of the extraocular muscles have a layered organization. The global layer is adjacent to the globe and consists of fibers of various diameters.39 This group of fibers extends the full length of the muscle and is attached at the origin and insertion through welldefined tendons.18,40 The global layer inserts into the sclera and causes movement of the globe.41 The outer orbital layer is adjacent to orbital bone, consists of smaller-diameter fibers, and is more vascularized than the global layer.39,42 These fibers end before the muscle tendon and have insertions into the muscle sheath. The orbital layer of the oblique muscles may encircle

the global layer.18,39,40 The orbital layer inserts into connective tissue muscle pulleys that can influence the rotational axis of the muscle.18,41

The orbital layer fibers make up 40% to 60% of the fibers within an extraocular muscle.40

Fibers of extraocular muscles can be divided into types having some of the usual characteristics of striated muscle. All of these types are involved in all muscle contractions. Orbital fibers with a high number of mitochondria and that are singly innervated have small myofibrils, allowing for rapid access of Ca2+ to contractile fibers. These are generally fast twitch and fatigue resistant fibers resulting in rapid contraction.18 Orbital fibers that are multiply innervated have several nerve terminals along the length of a single fiber, and they include both fast twitch and slowly contracting fibers.18

Among the global fibers that are singly innervated, the red fibers (having high amount of myoglobulin) may be fast twitch and fatigue resistant; the white fibers (lesser amount of myoglobulin) are fast twitch and may be fatigable.18 Global fibers that are multiply innervated are associated with the myotendinous cylinder or palisade endings; they are large myofibrils and appear to be slow and tonic.18

ORBITAL CONNECTIVE TISSUE STRUCTURES

Connective tissue sleeves or pulleys can be identified using detailed magnetic resonance imaging (MRI); the pulleys that couple the rectus muscles to the orbital walls and Tenon’s capsule were the first to be visualized­ .34,35,43-45 Pulleys along the inferior oblique and superior oblique muscle paths have subsequently been identified.18,40 Although not as prominent as the pulley of the superior oblique muscle, and only consisting of soft tissue,40 the pulleys encircle each extraocular muscle like a sleeve and can affect the mechanisms of muscle positioning. Smooth muscle-connective tissue struts attach the pulleys to the periorbita of the orbital wall and may help to refine coordination of binocular eye movements.35,41,44,46 The smooth muscle of the pulley is richly innervated by sympathetic and parasympathetic nerves, suggesting both excitatory and inhibitory capabilities.18,46 The smooth muscle either regulates the stiffness of the connective tissue or moves the pulleys to alter the pulling direction.41 The pulleys reduce sideslip of the extraocular muscles during globe rotation and help to determine the effective direction of pull.43 Pulley displacement can clinically mimic muscle dysfunction, and orbital imaging may be needed to distinguish it accurately from a palsy. The pulley for the medial rectus is the most fully developed.47

Dense connective tissue septa between the extra­ ocular muscle sheaths and between the sheaths and the orbital bones form a highly organized network that contributes to the framework supporting the globe within the orbit. The horizontal rectus muscles are anchored to the periorbita at the anterior orbital walls through the medial and lateral check ligaments. The medial check ligament is attached to the bones of the medial orbital wall, and the lateral check ligament is attached to the lateral tubercle on the zygomatic bone of the lateral wall; both ligaments are posterior to the orbital septum. The medial check ligament is better developed than the lateral.32 Traditionally, these ligaments were described as “brakes” that limit the extent of movement of the globe; that is, in abduction the medial check ligament stops lateral movement of the globe when extension of the medial rectus muscle starts to exert pull on the relatively inelastic ligament.

The connective tissue septa that connect muscle to muscle and periodically connect individual muscles to the orbital walls along a significant portion of the muscle length have been identified in dissection ­studies.45,48,49 These intermuscular septa include those joining (1) ­lateral rectus, inferior rectus, and medial rectus; (2) medial rectus and superior rectus; (3) lateral rectus and superior rectus; (4) medial rectus to superior oblique and to orbital roof and floor; (5) medial rectus to periorbita of ethmoid; (6) superior oblique to frontoethmoid angle; (7) inferior rectus to orbital floor;

(8) lateral rectus to lateral wall; (9) levator to adjacent periorbita32; and (10) superior oblique to orbital roof45 (Figure 10-11).

The presence and orientation of these septa vary from front to back. Figure 10-12 shows a representation of the septa at midorbit. The considerable amount of attachment between muscle and bone helps to stabilize the muscle path and can limit eye movement.18,45

I S O L A T E D A G O N I S T M O D E L

One of the earliest models developed to explain eye movement is the isolated agonist model described by Duane.50 This straightforward model has been used widely in the clinical evaluation of extraocular muscles and can be used to describe the movement around the axes that occurs with contraction of each muscle. However, it is important to remember that during eye movements, all six extraocular muscles are in some state of contraction or relaxation, and it is strictly hypothetical to discuss the movement of the eye as if only one muscle contracts. In each of these descriptions the eye begins in primary position.