The muscles of the globe can be divided into two groups: the involuntary intrinsic muscles and the voluntary extrinsic muscles. The intrinsic muscles—the ciliary muscle, the iris sphincter, and the iris dilator—are located within the eye; these muscles control the movement of internal ocular structures. The extrinsic mus- cles—the six extraocular muscles—attach to the sclera and control movement of the globe.

This chapter begins with a brief review of the microscopic and macroscopic anatomy of striated muscle, then discusses eye movements and describes the characteristics and actions of each extraocular muscle. (The smooth intrinsic muscles are discussed in Chapter 3.)

M I C R O S C O P I C A N A T O M Y O F S T R I A T E D M U S C L E

Striated muscle is surrounded by a connective tissue sheath known as the epimysium; continuous with this sheath is a connective tissue network, the perimysium, which infiltrates the muscle and divides it into bundles. The individual muscle fiber within the bundle is surrounded by a delicate connective tissue enclosure, the endomysium (Figure 10-1). The individual muscle fiber is comparable to a cell; however, each fiber is multinucleated, with the nuclei arranged at the periphery of the fiber. The plasma cell membrane surrounding each muscle fiber, the sarcolemma, forms a series of invaginations into the cell, the transverse tubules (T tubules), which allow ions to spread quickly through the cell in response to an action potential. The cell cytoplasm, sarcoplasm, contains normal cellular structures and special muscle fibers, the myofibrils.

Myofibrils comprise two types, thick and thin. The thick myofibrils are composed of hundreds of myosin subunits. Each subunit is a long, slender filament with two globular heads attached by arms at one end. These filaments lie next to each other and form the “backbone” of the myofibril, with the heads projecting outward in a spiral (Figure 10-2, A). The thin myofibrils are formed by the protein actin arranged in a double-helical filament, with a molecular complex of troponin and tropomyosin lying within the grooves of the double helix (Figure 10-2, B).

The alternating light and dark bands characteristic of striated muscle are produced by the manner in which

these two types of myofibrils are arranged. The light band is the I (isotropic) band, and the dark band is the A (anisotropic) band. These names describe the birefringence to polarized light exhibited by the two areas.1

The I band contains two sets of actin filaments connected to each other at the Z line, a dark stripe bisecting the I band. Only actin myofibrils are found in the I band. The A band contains both myosin and actin; the central lighter zone of the A band—the H zone—­contains only myosin. Overlapping actin and myosin filaments form the outer darker edges of the A band (Figure 10-3). The M line bisects the H zone and contains proteins that interconnect the myosin fibrils.

A sarcomere extends from Z line to Z line and is the contractile unit of striated muscle. With muscle contraction, a change in configuration occurs; the H zone width decreases as the actin filaments slide past the myosin filaments. The sarcomere is shortened; as this occurs along the muscle, muscle length is decreased. The length of the actin and myosin filaments remain constant as does the A band, the I band, and the H zone shorten.

SLIDING RATCHET MODEL OF MUSCLE CONTRACTION

The process of muscle contraction and sarcomere shortening is explained by the sliding ratchet model2-4 (­ Figure 10-4). The initiation of a muscle contraction occurs when a nerve impulse causes the release of acetylcholine into the neuromuscular junction. The sarcolemma depolarizes and an action potential passes along the surface and is carried into the muscle fiber through the system of T-tubules. Ionic channels are opened and calcium ions are released from the sarcoplasmic reticulum into sarcoplasm. Ca2+ binds to the troponin-tropomyosin complex, resulting in a configurational change, allowing an active site on the actin protein to be available for binding with a myosin head. Coincidentally, adenosine triphosphate (ATP) attached to the myosin head is broken down and released, allowing a cross-bridge to bind with the active actin site. Once this bond is formed, the head tilts toward the shaft of the myosin filament, pulling the actin filament along with it.

Epimysium

Perimysium

Endomysium

FIGURE 10-1

Connective tissue network of striated muscle.

The junction between the actin and myosin is broken by the attachment of a new ATP molecule to the myosin head. The head then rights itself, and the cross-bridge is ready to bind with the next actin site along the chain. This ratchet type of movement occurs along the length of the fiber, moving the filaments past one another with the overall effect of shortening the sarcomere and the entire muscle.

Clinical Comment: Myasthenia

Gravis

MYASTHENIA GRAVIS  is a chronic autoimmune neuromuscular­ disease caused by a defect in transmission of the nerve impulse to muscle fibers. Antibodies are formed that either block or destroy the acetylcholine receptors at the neuromuscular junction. Muscle weakness and fatigue worsens throughout the day and is particularly evident with repetitive movements. Often the first clinical symptom is ptosis; sometimes during a vision examination,­ the upper lid begins to droop and by the end of the examination­ is quite evident. Ocular myasthenia gravis is limited to eye and lid muscles, resulting in diplopia and ptosis.

STRUCTURE OF THE EXTRAOCULAR MUSCLES

The extraocular muscles have a denser blood supply, and their connective tissue sheaths are more delicate and richer in elastic fibers than is skeletal muscle.5 Fewer muscle fibers are included in a motor unit in extraocular muscle than are found in skeletal muscle elsewhere. Striated muscle of the leg can contain several hundred muscle fibers per motor unit6; in the extraocular muscles, each axon innervates 3 to 10 fibers.7 This dense innervation provides for precise fine motor control of the extraocular muscles resulting in high velocity ocular movements,

A

B

FIGURE 10-2

Myosin and actin myofibrils. A, Myosin fibril is composed of two-headed filaments, with heads arranged in a spiral. B, Actin myofibril is composed of double-helix filament to which troponin-tropomyosin complex is attached.

A

FIGURE 10-3

A, Arrangement of thick and thin filaments in sarcomere.

B, Photomicrograph of striated muscle, with parts of sarcomere indicated. (B from Krause WJ, Cutts JH: Concise text of histology, Baltimore, 1981, Williams & Wilkins.)

necessary in saccades, (up to 1000 degrees per second) and very accurate pursuits (velocities of 100 degrees per second) and fixations.8 Singly innervated fibers have the classic end plate (en plaque) seen in skeletal muscle; multiply innervated fibers have a neuromuscular junction resembling a bunch of grapes (en grappe).9,10

The extraocular muscles have a range of fiber sizes, with the fibers closer to the surface generally having smaller diameters (5 to 15 μm) and those deeper within

Myosin

ADP + P

ATP

ADP + P

Z-LINE

FIGURE 10-4

Sliding ratchet model of muscle contraction.

the muscle generally having larger diameters (10 to 40 μm).11-14 They can be divided into groups based on characteristics such as location, size, morphology, neuromuscular junction type, or various biochemical properties­ .5,12,13,15,16 The fibers range from typical twitch fibers at one end of the spectrum to typical slow fibers at the other end, with gradations in between.

It would seem that the fast-twitch fibers should produce quick saccadic movements and the slow fibers should produce slower pursuit movements and provide muscle tone. However, all fibers apparently are active at all times and share some level of involvement in all ocular movements.12,14,16,17 Extraocular muscles are among the fastest and most fatigue-resistant of striated muscle.18

Muscle spindles and Golgi tendon organs of typical striated muscle have been identified in human extraocular muscle, although it is unclear whether these structures provide any useful proprioceptive information relative to the extraocular muscles.19,20 Afferent information regarding extraocular muscle proprioception is thought to be mediated by a receptor that is unique to extraocular muscle, the myotendinous cylinder (palisade ending).16,21

E Y E M O V E M E N T S

FICK’S AXES

Before a discussion of the individual muscles and the resultant eye movements caused by their contraction, it is necessary to define certain terms. All eye movement can be described as rotations around one or more axes. According to Fick, these axes divide the globe into quadrants and intersect at the center of rotation, a fixed nonmoving point22 and the approximate geometric center of the eye. For convenience, it is assumed that the eye rotates around this fixed point, located 13.5 mm behind the cornea; this point varies in ametropia, is slightly more posterior in myopia, and is slightly more anterior in hyperopia.5 The x-axis is the horizontal or transverse axis and runs from nasal to temporal. The y-axis is the sagittal axis running from the anterior pole to the posterior pole. The z-axis is the vertical axis and runs from superior to inferior (Figure 10-5). When the front of the eye moves up, the back moves down. When the front of the eye moves right, the back of the eye moves left. The anterior pole of the globe is the reference point used in the description of any eye movement. Eye movements are described and based on the movement of the muscle insertion towards its origin.

DUCTIONS

Movements involving just one eye are called ductions (Figure 10-6). Rotations around the vertical axis move the anterior pole of the globe medially—adduction—or lat- erally—abduction. Rotations around the horizontal axis movetheanteriorpoleoftheglobeup—elevation (supra- duction)—or down—depression (infraduction).

Torsions or cyclorotations are rotations around the sagittal axis and are described in relation to a point at the 12-o’clock position on the superior limbus. Intorsion (incyclorotation) is the rotation of that point nasally,

Z-axis

Y-axis

X-axis

FIGURE 10-5

Fick axes: x-axis is horizontal; y-axis is sagittal; and z-axis is vertical.

pathologic conditions.25 Others have documented torsion in normal eye movements and with head tilt.26-29

VERGENCES AND VERSIONS

Movements involving both eyes are either vergences or versions, depending on the relative directions of movement. In vergence movements, the eyes move in opposite left-right directions; these are disjunctive movements. In convergence each eye is adducted, and in divergence each eye is abducted. Version movements are conjugate movements and occur when the eyes move in the same direction. Dextroversion is right gaze, and levoversion is left gaze. In supraversion both eyes are elevated, and in infraversion both eyes are depressed. Table 10-1 lists terms for monocular and binocular eye movements and some combination movements.

POSITIONS OF GAZE

The primary position of gaze is defined as the position of the eye with the head erect, the eye located at the intersection of the sagittal plane of the head and the horizontal plane passing through the centers of rotation of both eyes, and the eye focused for infinity.17 Secondary positions of gaze are rotations around either the vertical axis or the horizontal axis; tertiary positions are rotations around both the vertical and the horizontal axes.

FIGURE 10-6

Movements of the eye in duction. Anterior pole is point of ­reference. L, Lateral; M, medial.

and extorsion (excyclorotation) is the rotation of that point temporally. Torsional movements may occur in an attempt to keep the horizontal retinal raphe parallel to the horizon.23 With a head tilt of 30 degrees, the ipsilateral eye is intorted approximately 7 degrees, and the contralateral eye is extorted approximately 8 degrees.24

Torsional movements have been questioned by some investigators who believe that true torsion occurs only in

M A C R O S C O P I C

A N A T O M Y O F T H E

E X T R A O C U L A R M U S C L E S

The six extraocular muscles are medial rectus, lateral rectus, superior rectus, inferior rectus, superior oblique, and inferior oblique (Figure 10-7). From longest to shortest, the rectus muscles are the superior, the medial, the lateral, and the inferior.30

ORIGIN OF THE RECTUS MUSCLES

The four rectus muscles have their origin on the common tendinous ring (annulus of Zinn). This oval band of connective tissue is continuous with the periorbita and is located at the apex of the orbit anterior to the optic foramen and the medial part of the superior orbital fissure. The upper and lower areas are thickened bands and sometimes are referred to as the upper and lower tendons or limbs. The medial and lateral rectus muscles take their origin from both parts of the tendinous ring. The superior rectus is attached to the upper limb, and the inferior rectus is joined to the lower ­(Figure 10-8). The medial rectus and the superior rectus also attach to the dural sheath of the optic nerve.30

Clinical Comment: Retrobulbar

Optic Neuritis

RETROBULBAR OPTIC NEURITIS  is an inflammation affecting the sheaths of the optic nerve. Generally, there are no observable fundus changes in this condition, but pain with extreme eye movement can be one of the early presenting signs.1,30 The optic nerve sheath is supplied with a dense sensory nerve network and because of the close association of muscle sheath and optic nerve sheath, eye movement can cause stretching of the optic nerve sheath, resulting in a sensation of pain.31

The area enclosed by the tendinous ring is called the oculomotor foramen, and several blood vessels and nerves pass through the foramen, having entered the orbit either through the optic canal or the superior orbital fissure (see Figure 10-8). The optic nerve and ophthalmic artery enter the oculomotor foramen from the optic canal; the superior and inferior divisions of the oculomotor nerve, the abducens nerve, and the nasociliary nerve enter the oculomotor foramen from the superior orbital fissure (see Figure 10-8). These structures lie within the muscle cone, the area enclosed by the four rectus muscles and the connective tissue joining them. Thus the motor nerve to each rectus muscle can enter the surface of the muscle that lies within the muscle cone.

Trochlea

Superior oblique muscle

Superior rectus muscle

Medial rectus muscle

Lateral rectus muscle

Inferior rectus muscle

Inferior oblique muscle

FIGURE 10-7

Globe in orbit as viewed from lateral side.

In 1887, Motais described a common muscle sheath between the rectus muscles enclosing the space within the muscle cone.5 More recently, dissections by ­Koornneef32 revealed no definitive, continuous muscle sheath between the rectus muscles in the retrobulbar region.

The lacrimal and frontal nerves and the superior ophthalmic vein lie above the common ring tendon, and the inferior ophthalmic vein lies below. They are outside the muscle cone (see Figure 8-15).