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Chapter 68 – Anatomy and Physiology of the Extraocular Muscles and Surrounding Tissues

Part 6 – STRABISMUS

 

Gary R. Diamond

 

Section 1 – Basic science

 

 

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Chapter 68 – Anatomy and Physiology of the Extraocular Muscles and Surrounding Tissues

 

BRIAN N. CAMPOLATTARO

FREDERICK M. WANG

 

EMBRYOLOGY

The extraocular muscles are of mesodermal origin, development beginning at 3–4 weeks’ gestation.[1] The muscles originate from three separate foci of primordial cells, one for the muscles innervated by the oculomotor nerve, one for the superior oblique muscle, and one for the lateral rectus muscle. All of the extraocular muscles develop in situ; they do not begin development at their origins and sprout toward their respective insertions. The extraocular muscles receive input from their respective cranial nerves as early as 1 month of gestation.[2]

The tissues that surround the extraocular muscles also develop early in gestation. Formation of the trochlea begins at 6 weeks’ gestation, and early fascial coverings can be detected around the extraocular muscles by 3 months’ gestation.[3] Tissues destined to become intermuscular septa and orbital fat differentiate in the fourth and fifth months of gestation, respectively. All of the extraocular muscle and their surrounding tissues are present and in their final anatomical positions by 6 months’ gestation, merely enlarging throughout the remainder of gestation.

GROSS ANATOMY OF THE EXTRAOCULAR MUSCLES

The alignment of the eye is determined by the extraocular muscles and their surrounding tissues. Primary position is defined as the position when the eye and head are both directed straight ahead. The primary position of the eye is approximately 23° nasal to the position of the orbits (the medial orbital walls are approximately parallel to each other); this relationship explains and determines both the cardinal positions of gaze and the fact that all vertical extraocular muscles have vertical, rotational, and horizontal (i.e., primary, secondary, and tertiary) actions on the globe when the globe is in primary position ( Fig. 68-1 ). (Remember, the horizontal rectus muscles do have vertical actions on the globe, but not in primary position, where the primary, secondary, and tertiary actions of the extraocular muscles are defined.)

Origin of the Extraocular Muscles

Five of the six extraocular muscles (the inferior oblique excepted) originate at the orbital apex. The superior, inferior, medial, and lateral rectus muscles arise from the annulus of Zinn, an oval, fibrous ring at the orbital apex. The superior oblique muscle arises just above the annulus of Zinn. The following structures pass through the annulus of Zinn ( Fig. 68-2 ):

• The superior and inferior divisions

• The oculomotor nerve

• The abducens nerve

• The optic nerve

• The nasociliary nerve

• The ophthalmic artery

 

 

Figure 68-1 The extrinsic muscles of the right eyeball in the primary position, seen from above. The muscles are shown partially transparent.

The sixth extraocular muscle, the inferior oblique, originates from the maxillary bone, adjacent to the lacrimal fossa, posterior to the orbital rim.

Insertion of the Extraocular Muscles

The rectus muscles insert into the sclera via their tendons anterior to the equator of the globe. Although the rectus insertions may vary slightly, the spatial formation created by connecting their insertion is called the spiral of Tillaux ( Fig. 68-3 ).[4] Note that the medial rectus tendon inserts closest to the limbus, followed by the inferior, lateral, and superior recti in that order.

 

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Figure 68-2 The annulus of Zinn and surrounding structures.

 

 

Figure 68-3 Spiral of Tillaux. The structure of the rectus muscle insertions.

Also note that the tendinous insertion line of the superior and inferior recti migrates posteriorly from the nasal to the temporal edge of the tendon. The sclera is thinnest (approximately 0.3?mm thick) just posterior to the tendinous rectus insertions. Because the distance between the rectus insertions is less than the width of each rectus insertion, a thorough knowledge of the

 

 

Figure 68-4 Posterior view of the eye with Tenon’s capsule removed. (Adapted with permission from Parks MM. Extraocular muscles. In: Duane TD. Clinical ophthalmology. Philadelphia: Harper & Row; 1982:1–12.)

anatomy of the region is essential to ensure proper surgery on the correct muscles during strabismus surgery.

The oblique muscles insert into the sclera posterior to the equator of the globe ( Fig. 68-4 ). The superior oblique tendon inserts into the posterior, superolateral sclera in a broad, fan-shaped fashion under the superior rectus muscle. The tendon insertion extends from the temporal pole of the superior rectus muscle to near the optic nerve. The insertion may be up to 18?mm wide and extend near the superotemporal vortex vein. The tendon insertion is functionally separated into two parts, the anterior one third and the posterior two thirds. The anterior one third of the tendon functions almost exclusively to incyclotort the globe. The posterior two thirds of the tendon functions to depress and abduct the globe. This distinction allows surgical treatment of cyclovertical strabismus through manipulation of the anterior tendon fibers, such as by the Harada-Ito procedure.[5]

The inferior oblique muscle, which has almost no tendon at its insertion, inserts into the posterior, inferolateral sclera. The insertion lies in close proximity to both the macula and the inferotemporal vortex vein. In general, the point of insertion of the oblique muscles is more variable than that of the rectus muscles.[6]

Course of the Extraocular Muscles

The extraocular muscles are belt-shaped structures with their thickest section residing posterior to the globe. The path of the extraocular muscles from their origin to their insertion determines their effects on eye movement, and a thorough knowledge of the relationship of the muscles with each other as they course to their insertions is requisite for successful orbital and strabismus surgery.

The medial rectus muscle leaves the nasal edge of the annulus of Zinn and courses anteriorly along the medial wall of the orbit to insert on the nasal anterior sclera. The proximity of the muscle to the medial orbital wall means that the medial rectus

 

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Figure 68-5 The actions of the right superior rectus muscle. A, Primary position. B, Adduction. C, Abduction.

can sustain inadvertent damage during standard or endoscopic ethmoid sinus surgery. The medial rectus is the only rectus muscle that does not have a fascial attachment to an oblique muscle; thus, the medial rectus muscle is at greatest risk for slippage or loss during orbital or strabismus surgery.

The lateral rectus muscle leaves the temporal edge of the annulus of Zinn and courses anteriorly in the lateral orbit to insert on the temporal anterior sclera. The inferior border of the lateral rectus passes just superior to the insertion of the inferior oblique muscle, and fascial connections between the two muscles here (8–9?mm from the insertion of the lateral rectus) allow the surgeon to retrieve the lateral rectus at this location if inadvertent muscle detachment occurs.[7]

The superior rectus muscle leaves the superior edge of the annulus of Zinn and courses anteriorly, laterally, and superiorly in the superior orbit to insert on the anterior globe. In the primary position, the muscle forms an angle of 23° with the visual axis ( Fig. 68-1 ). This angle determines the secondary and tertiary actions of the superior rectus muscle in the primary position. In primary position, the superior rectus functions to elevate, incyclotort, and adduct the globe. If the globe is abducted 23°, the visual axis and the muscle axis align and the sole action (in theory) of the superior rectus is elevation of the globe.

The cardinal positions of gaze refer to positions of the globe that minimize the angle between the axis of the extraocular muscle being evaluated and the visual axis. Minimizing this angle minimizes the secondary and tertiary actions of the muscle on the globe.

Nomenclature defines secondary and tertiary actions of the extraocular muscles in the primary position. In reality, if the globe is abducted more than 23°, the actions of the superior rectus muscle on the globe are elevation, abduction, and excyclotorsion ( Fig. 68-5 ).

The superior rectus muscle courses between the tendon of the superior oblique muscle and the levator palpebrae muscle prior to its insertion, and fascial attachments from the superior rectus extend to both muscles. Failure to remove these connections to the levator muscle during superior rectus muscle recession or resection may lead to subsequent eyelid-fissure widening or narrowing, respectively.

The inferior rectus muscle leaves the inferior edge of the annulus of Zinn and courses anteriorly, laterally, and downward along the orbital floor to insert on the anterior globe. In the primary position, the muscle forms an angle of 23° with the visual axis. In primary position, the inferior rectus muscle functions to depress, excyclotort, and adduct the globe. If the globe is abducted 23°, the only action of the inferior rectus is depression of the globe.

The inferior rectus muscle courses between the globe and the inferior oblique muscle prior to its insertion, and fascial attachments exist between the inferior rectus, the inferior oblique, and the lower lid retractors. Failure to dissect these connections during inferior rectus recession or resection may lead to eyelid-fissure widening or narrowing, respectively. Some clinicians suggest that late overcorrections after inferior rectus recession may be caused by reattachment of these connections postoperatively even if dissection is performed.[8] If inadvertent disinsertion of the inferior rectus muscle occurs, this fascial network may allow retrieval of the muscle in the region of Lockwood’s ligament.[9] These fascial relationships are described in detail later in this chapter.

The superior oblique muscle leaves the orbital apex at its anatomical origin above the annulus of Zinn and courses anteriorly along the superomedial wall of the orbit. The superior oblique muscle becomes tendinous as it passes through the trochlea, where its direction is altered. Connective tissue attachments exist between the trochlea and the superior oblique tendon.[10] The trochlea becomes the functional origin of the superior oblique tendon, and the tendon exits the trochlea inferiorly, posteriorly, and laterally to insert on the posterior globe. In the primary position, the superior oblique tendon forms an angle of 51° with the visual axis. In primary position, the superior oblique muscle functions to incyclotort, depress, and abduct the globe. If the globe is abducted 39°, the major action of the superior oblique muscle is incyclotorsion of the globe. If the globe is adducted 51°, the major action of the superior oblique muscle is depression of the globe. (The globe can move up to 50° in each direction from the primary position, but head movement usually occurs after it moves 15–20° from the primary position.)

The superior oblique tendon courses between the globe and the superior rectus muscle prior to its insertion, and fascial attachments exist between the tendon and the superior rectus muscle.

 

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TABLE 68-1 — CHARACTERISTICS OF EXTRAOCULAR MUSCLES

Muscle

Origin

Insertion

Muscle Length (mm)

Tendon Length (mm)

Width of Insertion (mm)

Direction of Pull From 1° Position (°)

Action: i. Primary ii. Secondary iii. Tertiary

Innervation (Cranial Nerve)

Medial rectus

Annulus of Zinn

5.5?mm behind nasal limbus

41

3.5

10.3

90

i. Adduction

Inferior III

Lateral rectus

Annulus of Zinn

6.9?mm behind temporal limbus

41

8

9.2

90

i. Abduction

VI

Superior rectus

Annulus of Zinn

7.7?mm behind superior limbus

42

5

10.6

23

i. Elevation

ii. Incyclotorsion

iii. Adduction

Superior III

Inferior rectus

Annulus of Zinn

6.5?mm behind inferior limbus

40

6

9.8

23

i. Depression

ii. Excyclotorsion

iii. Adduction

Inferior III

Superior oblique

Frontoethmoidal suture above annulus of Zinn

Posterior, lateral, superior quadrant

32

26

10.8

51

i. Incyclotorsion

ii. Depression

iii. Abduction

IV

Inferior oblique

Posterior to lacrimal fossa

Posterior, lateral, inferior quadrant

35

1

9.6

51

i. Excyclotorsion

ii. Elevation

iii. Abduction

Inferior III

 

 

The inferior oblique muscle leaves the lacrimal fossa and courses posteriorly, laterally, and temporally; it passes beneath the inferior rectus muscle to its insertion, which is adjacent to the inferior border of the lateral rectus. Fascial attachments exist between the inferior oblique muscle and the inferior and lateral rectus muscles. In the primary position, the inferior oblique muscle forms an angle of 51° with the visual axis. In primary position, the inferior oblique functions to excyclotort, elevate, and abduct the globe. If the globe is abducted 39°, the major action of the inferior oblique muscle is excyclotorsion of the globe. If the globe is adducted 51°, the major action of the muscle is elevation of the globe.

Other pertinent information about the extraocular muscles is listed in Table 68-1 .

Innervation

The third cranial (oculomotor) nerve innervates multiple extraocular muscles after separating near the orbital apex into a superior and an inferior division. The superior division innervates the levator palpebrae and superior rectus muscles, and the inferior division innervates the medial rectus, inferior rectus, and inferior oblique muscles. The fourth cranial (trochlear) nerve innervates the superior oblique muscle. The sixth cranial (abducens) nerve innervates the lateral rectus muscle.

All rectus muscles are innervated from the intraconal surface of the muscle belly at approximately the junction of the middle and posterior third of each muscle. The inferior oblique muscle receives its innervation just lateral to the inferior rectus muscle. Inadvertent trauma to the nerve at this location may cause ipsilateral mydriasis because the parasympathetic fibers responsible for pupillary constriction also travel with the nerve to the inferior oblique muscle. The superior oblique muscle is innervated from its orbital surface, in several branches, near the middle of the muscle. Because the fibers of the fourth cranial nerve pass outside the muscle cone, the superior oblique muscle is not usually affected by retrobulbar anesthesia.

Blood Supply

The ophthalmic artery sends muscular branches to most of the extraocular muscles. The medial muscular branch supplies the medial rectus, inferior rectus, and inferior oblique muscles. The lateral muscular branch supplies the superior rectus, lateral rectus, and superior oblique muscles as well as the levator palpebrae muscle. Also, the lacrimal artery supplies the lateral rectus muscle and the infraorbital artery supplies the inferior rectus and inferior oblique muscles. The blood vessels that supply the oblique muscles do not carry any circulation to the anterior segment. The blood vessels that supply the rectus muscles are termed anterior ciliary arteries; these anterior ciliary arteries also supply the anterior segment of the eye. Usually, each rectus muscle contains two anterior ciliary arteries, with the exception of the lateral rectus muscle, which contains one such artery, but variations have been reported. These branches travel on the anterior surface of the rectus muscles and then pierce the sclera just anterior to the tendinous rectus insertions. They anastomose with conjunctival vessels at the limbus before connecting with the major arterial circle of the iris. The long posterior ciliary arteries also supply the anterior segment of the eye with blood via the major arterial circle of the iris. These long posterior ciliary arteries allow collateral blood flow after rectus muscle surgery.

Surgical manipulation of the rectus muscles permanently disrupts the anterior ciliary arteries. If surgery is performed on multiple rectus muscles simultaneously, anterior segment ischemia may result.[11] Usually, anterior segment circulation is most dependent on arteries from vertical rectus muscles and least dependent on arteries from the lateral rectus muscle, although exceptions have been reported.[12] Other risk factors for the development of anterior segment ischemia include sickle cell anemia, lupus erythematosus, hyperviscosity syndromes, arteriosclerosis, and advanced age. Anterior segment ischemia can lead to pain, uveitis, or even phthisis bulbi. Dissection of the anterior ciliary arteries from the rectus muscles prior to muscle surgery allows sparing of these vessels, minimizing the risk of anterior segment ischemia.[13]

The superior and inferior orbital veins supply venous drainage for the extraocular muscles.

Microscopic Anatomy

Extraocular muscle is unique because of its combination of different forms of muscle cells. Although five types have been reported, these can be represented by two main groups of muscle cells.

 

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Fibrillenstruktur fibers are similar to the muscle fibers of skeletal muscle—they are singly innervated with large myelinated axons, motor end plates that resemble en plaque nerve endings, and many glycolytic enzymes that allow anaerobic metabolism. Their firing rate is proportional to conducted action potentials.[14] These characteristics allow a rapid, all-or-none response to a single nerve stimulus, which is necessary for rapid eye movements such as saccades. Within each extraocular muscle, these relatively large fibers reside on the global side.

The second group of muscle cells form Felderstruktur fibers. These fibers are unique to extraocular muscle—they are multiply innervated via small axons and multiple en grappe nerve endings and have a high concentration of mitochondria for aerobic metabolism. Their firing rate is proportional to the nerve impulse rate, not to conducted action potentials. [15] These characteristics allow a graded response to repetitive nerve stimuli, which is necessary for slow, precise eye movements, such as smooth pursuit, or for a tonic response necessary for gaze fixation. Within each extraocular muscle, these relatively small fibers reside on the orbital side. Because these fibers with high mitochondrial content are more physiologically “active” and consume more oxygen than Fibrillenstruktur fibers, capillaries are most prevalent on the orbital surface of the muscle.

Both groups demonstrate a high ratio of nerve fibers to eye muscle fibers compared with true skeletal muscle (approximately 1:50 to 1:100 in true skeletal muscle), especially Felderstruktur fibers (1:4). [16]

Unlike the situation in skeletal muscle, individual muscle cells, both Fibrillenstruktur and Felderstruktur types, are surrounded by connective tissue. This complex of mucopolysaccharide, collagen, and elastin harbors blood supply and nerve input to the muscle.[17]

Muscle spindles that detect length changes of extraocular muscles (proprioception) do exist, although they are less well developed than muscle spindles in skeletal muscle. They are most prevalent at the muscle-tendon interface.[18] Their importance in eye position and extraocular muscle activity, however, is unclear.

THE ORBITAL INFRASTRUCTURE AND ANATOMY

Within the orbit, there exists a delicate fibrous infrastructure that suspends the globe, compartmentalizes the cushioning fat pads, and directs the traversing muscles, nerves, and vessels ( Fig. 68-6 ). [19] [20] [21] Tenon’s capsule is a fibroelastic membrane that begins 1?mm from the limbus, where it is fused with the conjunctiva; it then caps the globe posteriorly to the optic nerve.[19] Its inner surface is smooth, which allows free gliding of the adjacent structures within it. Its equatorial region is penetrated by the extraocular muscles. The rectus muscles penetrate Tenon’s capsule just posterior to the equator (approximately 10?mm posterior to the extraocular muscle insertions), and the oblique muscles penetrate Tenon’s capsule just anterior to the equator. Tenon’s capsule is arbitrarily divided into anterior and posterior segments at the sites of rectus penetration.

Tenon’s capsule thickens in the equatorial region, where it is penetrated by the extraocular muscles.[20] At the site of penetration, a sleeve is formed around the penetrating extraocular muscle with increasing cross-linked collagen and elastin. This sleeve has significant fibroelastic attachments to the periorbita and adjacent sleeves ( Figs. 68-7 and 68-8 , A). These sleeves create compliant pulleys that redirect the extraocular muscles and act as functional origins.[20] [22] [23] The sleeve-like pulleys are centered at and just posterior to the equator of the globe with total anteroposterior extents of 13–19?mm, although it is likely that only the middle 5–8?mm of this extent is mechanically stiff. The pulley sleeves contain collagen, elastin, and innervated smooth muscle. Whether or not the smooth muscle dynamically changes pulley function is not known at present. [22] The sleeves extend both

 

 

Figure 68-6 Muscle cone. (Adapted with permission from Parks MM. Extraocular muscles. In: Duane TD, ed. Clinical ophthalmology. Philadelphia: Harper & Row; 1982:1–12.)

 

 

Figure 68-7 The structure of the orbital connective tissues. (Adapted with permission from Slack Incorporated. Demer JL, Miller JM, Poukens V, et al. Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest Ophthalmol Vis Sci. 1995;36:1125–36.)

 

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Figure 68-8 Coronal 10?mm thick sections of a whole right orbit. A, Near equator of the globe demonstrating collagen (blue) pulley sleeves around medial (arrowhead) and inferior rectus muscles. Note the attachments (arrow) of the inferior rectus to the inferior oblique forming Lockwood’s ligament. Sub-Tenon’s space is marked (asterisk). B, Near globe–optic nerve (ON) junction demonstrating posterior sling of lateral rectus extending from the periorbita (arrowhead) and superior rectus sling (arrow) around the global surface of the lateral rectus (double arrow). Masson’s trichome stain. (By kind courtesy of Dr JL Demer, Jules Stein Eye Institute, UCLA.)

anteriorly and posteriorly from the site of maximal pulley effect to form slings that stabilize the extraocular muscle paths through fibroelastic attachments to periorbita and surrounding slings ( Figs. 68-7 and 68-8 , B).

Rectus muscles travel through their thick pulleys by sliding inside thin collagenous sheets that probably telescope within the pulley sleeves to permit passage of the entire muscle. At the sites of horizontal recti penetration of Tenon’s capsule, pulley formation and periorbital attachments are most highly developed. The equatorial attachments suspend the globe in the orbit from Tenon’s capsule in a drumhead-like fashion.[20]

Tenon’s capsule thins posteriorly, which allows free movement of the penetrating optic nerve and vessels with globe movement. The rectus muscles form a muscle cone within the orbit, with the apex at their origins at the annulus of Zinn and the base at their penetration of Tenon’s capsule ( Fig. 68-9 ). Posterior Tenon’s capsule lines the base of the cone forming the barrier between intraconal fat and sclera. Each muscle is surrounded by a thin fibrous muscle capsule throughout its extent. The capsules are attached by a thin continuous membrane that forms the intermuscular septum. Posterior to the globe, the intermuscular septum separates the extraconal and intraconal fat pads. The muscle capsules create a smooth avascular surface for easy gliding of the extraocular muscles. The intermuscular septum fuses with Tenon’s capsule 3?mm from the limbus.

Fat cushions the orbital structures both inside and outside the muscle cone. [19] [20] [21] Fat is contained in an intricate fibrous septal network (reticulum), which defines the cushions, and is isolated from the globe by Tenon’s capsule. Extraconal fat extends forward 10?mm from the limbus, being limited in its anterior extent by the close apposition and fine areolar connections between Tenon’s capsule and conjunctiva.

 

 

Figure 68-9 Sagittal section of orbital tissues through the vertical recti. (Adapted with permission from Parks MM. Extraocular muscles. In: Duane TD, ed. Clinical ophthalmology. Philadelphia: Harper & Row; 1982:1–12.)

The trochlea is a cartilaginous saddle attached to periorbita of the frontal bone in the superior nasal orbit ( Fig. 68-10 ).[24] The superior oblique tendon passes through the trochlea, changing direction in the fashion of a simple pulley. This cartilaginous saddle is 5.5?mm long, 4?mm wide, and 4?mm deep with a 2?mm groove along its long axis. Within the cartilaginous saddle and separated from it by a bursa-like space is a fibrillovascular sheath. The tendon of the superior oblique runs within this sheath. Movement of the tendon through the trochlea occurs by telescoping of the tendon fibers, the more internal fibers moving farther than the peripheral ones ( Fig. 68-11 ). The tendon penetrates Tenon’s capsule 2?mm nasally and 5?mm posteriorly to the nasal insertion of the superior rectus, where its capsule becomes continuous with the anterior intermuscular septum to the superior rectus. The superior oblique tendon has no special “sheath.” This concept arose because the technique for capturing the superior oblique tendon frequently resulted in its being enveloped with a combination of Tenon’s and intermuscular septum, which gave the appearance of a sheath.

The inferior oblique arises from the orbital plate of the maxilla, traveling through the extraconal fat cushion until it penetrates Tenon’s capsule at the nasal border of the inferior rectus. It crosses beneath the inferior rectus, at which point extensions from the muscle capsules of the two muscles become continuous to form the “suspensory ligament of Lockwood.”[25] This particular structure may have no unique suspensory or ligamentous function. [26] It is instead one part of the continuous fibrous infrastructure. After crossing beneath the inferior rectus, the posterior lateral surface of the inferior oblique abuts Tenon’s capsule near the muscle’s insertion. The surface capsule of the inferior oblique is continuous with the intermuscular septum of the lateral rectus.

 

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Figure 68-10 Components of the trochlea. (Adapted with permission from Helveston EM, Merriam WW, Ellis RD, et al. The trochlea: a study of the anatomy and physiology. Ophthalmology. 1989;89:124–33.)

Fibrous septa arise from the orbital surface of the capsule of the inferior rectus 15?mm from the limbus and extend forward to form the capsulopalpebral head of the inferior rectus ( Fig. 68-12 ).[25] [27] The fibroelastic tissue of the capsulopalpebral head divides above and below the inferior oblique while fusing with its capsule. Anterior to the inferior oblique, the fibers of the two portions of the capsulopalpebral head come together to form Lockwood’s ligament. The capsulopalpebral head divides, sending fibers inferiorly through orbital fat to attach to the orbital septum; the bulk of the fibers continue anteriorly. This anterior extension proceeds forward as the capsulopalpebral fascia, being joined by smooth muscle fibers, the “inferior tarsal muscle.” This fibromuscular band extends forward and attaches in slips to the tarsus on its anterior, basal, and posterior surfaces. Some fibers also extend through the preseptal orbicularis oculi muscle toward the skin, probably contributing to the lower eyelid crease.

CLINICAL CORRELATES

A thorough knowledge of and careful respect for the orbital infrastructure are the keys to successful strabismus and orbital surgery. Violating Tenon’s capsule disrupts the globe’s free movement by allowing adherence of fat to the globe, which restricts excursions.[28] Tenon’s capsule is most often violated during strabismus surgery by either of the following:

• Making fornix incisions more than 9?mm posterior to the limbus that expose the extraconal fat cushion, or

• Penetrating posterior Tenon’s capsule to expose the intraconal fat cushion while working on the segment of the inferior oblique that is apposed to Tenon’s capsule.

The muscle pulleys redirect the rectus muscles and limit the effect of transposition surgery.[23] The system of sleeves and slings limits the sideslip of the muscles that occurs during transposition procedures, thereby lessening the effective change in pulling direction that would occur if such structures were not

 

 

Figure 68-11 Movement of the insertion of the superior oblique. The eye is shown in 50° adduction. From elevation A to primary position B is 8?mm and from primary position B to downgaze C is 8?mm. (Adapted with permission from Helveston EM, Merriam WW, Ellis RD, et al. The trochlea: a study of the anatomy and physiology. Ophthalmology. 1989;89:124–33.)

present. Whether or not there are entities of pulley dysfunction that produce incomitant strabismus remains to be elucidated.

Maintaining the integrity of the muscle capsules during surgery eliminates bleeding and preserves free-sliding upper surfaces. The intermuscular septal connections, especially between the obliques and their adjacent recti, help prevent surgical “loss” of the muscles through their pulleys at the sites of penetration of Tenon’s capsule. Once the muscle slips through Tenon’s pulley, it is difficult to find it within the orbital fat; the process of finding it may violate various tissue planes with attendant complications. The intermuscular septal connections and check ligaments attached to Tenon’s capsule should be carefully severed when resecting or transposing muscles. This prevents the relocation of adjacent muscles and fat compartments. For example, if the attachments between the lateral rectus and inferior oblique are not severed, the inferior oblique is moved anteriorly during a resection of the lateral rectus. Severing of the intermuscular septal connections is not necessary for rectus recessions.[29]

Recession of the inferior rectus results in a posterior displacement of the capsulopalpebral head, which causes lowering of the lower lid. The capsulopalpebral septa, therefore, should be carefully severed during inferior rectus recession surgery. With moderate or large recessions of the inferior rectus, it is best to replace these septa at their normal distance from the limbus in order to minimize the lowering of the lower lid.[27]

Disruption of the reticulum of the fat cushions may result from various surgical procedures but most commonly occurs with orbital floor fracture. Resultant incarceration of orbital

 

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Figure 68-12 Anatomy of the lower eyelid retractors. (Adapted with permission from Hawes MJ, Dortzbach RK. The microscopic anatomy of the lower eyelid retractors. Arch Ophthalmol. 1982;100:1313–18.)

septa, scarring, and contracture produce incomitance of gaze through restrictive adhesions or traction transmitted to the muscle capsules, which change extraocular muscle direction and function.[30] Disorders of the trochlea may be responsible for certain inflammatory and traumatic Brown syndromes.[24]

EXTRAOCULAR MUSCLE PHYSIOLOGY

For globe movement, extraocular muscles must generate a force that overcomes the stiffness of passive tissues and the resting tension of the antagonist extraocular muscles. The contractile force produced by an eye muscle depends on its innervation and its length.

Length-tension curves summarize these forces for each extraocular muscle ( Fig. 68-13 ).[31] For example, in primary position the medial rectus muscle has a resting tension of approximately 15?g. This resting tension balances the tension of the lateral rectus muscle and the resistance of the surrounding tissues. With medial rectus contraction, tension of the muscle increases and the muscle shortens. However, the continued force available for muscle contraction decreases as a muscle shortens (due partly to changes in sarcomere length), with the result that continued contraction leads to higher tension but smaller force within the medial rectus muscle for further contraction. At the same time, the lateral rectus muscle is being stretched. Although, first, innervation to the lateral rectus is decreased during this adduction and, second, initial stretching places the lateral rectus muscle at its lowest resting tension, further stretching increases the tension in the lateral rectus muscle. Continued stretching leads to continued increases in the tension of the lateral rectus muscle and decreases in the force of contraction remaining in the medial rectus muscle until the opposing forces balance and a new eye position and resting tension are achieved. The resting tension of the medial rectus at this new eye position is less than the maximal tension within the muscle during the saccade to the new eye position. These forces are affected by paralysis, scar formation, abnormal innervation, and muscle contracture.

In the past, the length-tension curve provided the sole explanation for globe movement and for the resultant eye position

 

 

Figure 68-13 The length-tension curve of the left medial rectus muscle. (From Collins C, O’Mear DM, Scott AB. Muscle tension during unrestrained human eye movement. J Physiol. 1975;245:351–69.)

after strabismus surgery. More recent evidence demonstrates that sarcomere reorganization occurs after extraocular muscle recession, resection, or paralysis, and these changes may be partly responsible for the resultant eye position after strabismus surgery. [32]

In normal, tonically innervated muscle, sarcomeres are of a precise length to maximize their contractility. Recession of extraocular muscle causes temporary “slack” of each sarcomere in that muscle. An analogy to decreasing the length of each sarcomere during muscle recession is to push the two sides of an accordion together, with each fold representing one sarcomere ( Fig. 68-14 ). In time (8–12 weeks), each sarcomere reorganizes to its original length for maximal contractility. Now, however, the total number of sarcomeres in the muscle is decreased from preoperative levels. Similarly, muscle resection creates a temporary “stretch” of each sarcomere in that muscle (because tendon has been removed in the resection process and the remaining muscle must now reach from origin to insertion), and sarcomeric reorganization to its original length causes an increase in the total number of sarcomeres in the resected muscle.[33] How an increase or decrease in the number of sarcomeres per muscle ultimately affects extraocular muscle function, however, remains to be elucidated.

Principles and Terms

For convenience, it is assumed that the eye rotates about a fixed point 13.5?mm behind the cornea, the center of rotation, on the visual axis. The three axes that pass through this fixed point can describe all globe rotations and are termed the axes of Fick.[34] These axes are the x-axis, which is horizontally orientated for vertical globe movement, the z-axis, which is vertically orientated for horizontal globe movement, and the y-axis, which is orientated on the visual axis for rotational globe movement. Listing’s equatorial plane also passes through the center of rotation and includes the x- and z-axes ( Fig. 68-15 ).[35]

Donder’s law states that the orientation of the eye is determined solely by the horizontal and vertical coordinates plotted

 

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Figure 68-14 Sarcomere reorganization of the left medial rectus muscle. (A, Recession. B, Resection.

 

 

Figure 68-15 The axes of Fick and Listing’s plane.

on the axes of Fick; preceding eye movements have no effect on subsequent orientation. [36] This law does not apply to smooth pursuit movements or eye movements in the presence of head tilt.

Listing’s law specifies the orientation of the globe as a function of gaze direction and states that all positions of gaze can be achieved by rotations around axes that lie on Listing’s plane. On Listing’s plane, an oblique (O-) axis is present between the z- and x-axes of Fick, which allows oblique eye rotation. Listing’s law does not apply in the presence of head tilt because countertorsion is elicited ( Fig. 68-16 ).

 

 

Figure 68-16 Demonstration of Listing’s law. All positions of gaze can be achieved by rotations around axes that lie on Listing’s plane. Note pseudotorsion of the cornea during rotation around the oblique axes.

Central Innervational Patterns

Individual muscle fibers fire at a rate dependent on both eye position and velocity of movement regardless of the type of eye movement.[37] Each extraocular muscle fiber, classified simply as a “fast-saccadic” type or “slow-tonic” type, is innervated by a neuron with a particular electric threshold at which it becomes active. In the spinal cord, a “size order of nerve recruitment” exists for motor neurons; the concept seems to apply to extraocular muscle innervation as well.[38] This means that smaller neurons with smaller axons (which in the simplified concept of extraocular

 

558

 

 

 

Agonist-Antagonist Pairs (in the Same Eye)

Medial rectus–lateral rectus

 

Superior rectus–inferior rectus

 

Superior oblique–inferior oblique

 

 

 

 

 

 

 

Paired Agonists (in Separate Eyes)

Left medial rectus–right lateral rectus

 

Left lateral rectus–right medial rectus

 

Left superior rectus–right inferior oblique

 

Left inferior rectus–right superior oblique

 

Left superior oblique–right inferior rectus

 

Left inferior oblique–right superior rectus

 

 

 

 

muscle types innervate “tonic” muscle fibers) are more easily recruited by field potentials; this concept of a low recruitment threshold for neurons that innervate tonic muscle fibers provides an efficient method of stimulating continuous extraocular muscle activity for pursuit or gaze fixation.[39] For saccades, a larger field potential is required to recruit the larger neurons with larger axons (which innervate fast muscle fibers). Thus, with increasing stimulation of a nucleus, the motor units are automatically recruited in sequence of size. In reality, the muscle units probably become active in the sequence of their recruitment threshold regardless of the type of extraocular movement elicited.

Hering and Sherrington Laws

Eye movements during monocular viewing conditions are termed ductions. During a duction, contraction of one extraocular muscle results in simultaneous relaxation of its antagonist in the same eye. Agonist-antagonist pairs are listed in Box 68-1 . This relationship between agonist-antagonist pairs in one eye is termed Sherrington’s law of reciprocal innervation, which describes the inhibition of innervation to the antagonist as innervation to the agonist increases. Electromyogram recordings of agonist-antagonist pairs, such as the medial rectus and lateral rectus muscles during horizontal gaze, demonstrate Sherrington’s law.[40] In Duane’s retraction syndrome, Sherrington’s law is violated because of cocontraction of the medial rectus and lateral rectus muscles during adduction.[41]

Eye movements during binocular viewing conditions are termed versions. During a version, contraction of one extraocular muscle results in simultaneous contraction of an agonist in the contralateral eye. These paired agonists are called yoke muscles and receive equal and simultaneous innervation during versions ( Box 68-2 ). This equal and simultaneous innervation to the yoke muscles during versions is called Hering’s law of motor correspondence.[42] Hering’s law is often violated during saccadic eye movements, when dynamic overshoot and slightly different innervational signals to the yoke muscles may occur.[43] Hering’s law explains the findings of primary and secondary deviations in the setting of paralytic strabismus. Innervation to the yoke muscles is always determined by the fixing eye. When the normal eye fixates, the resultant strabismus is termed the primary deviation. When the paretic eye fixates, the resultant strabismus is termed the secondary deviation and is often the larger of the two deviations.

 

 

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