Anatomy and Physiology of Eye Movements
Kenneth W. Wright
OCULAR POSITION
Within the orbit, the eye is suspended by six extraocular muscles (four rectus muscles and two oblique muscles), suspensory liga- ments, and surrounding orbital fat (Fig. 2-1). A tug-of-war exists between the rectus and oblique muscles. The four rectus muscles insert anterior to the equator, and pull the eye posteri- orly, while the two oblique muscles insert posterior to the equator providing anterior counterforces. Posterior orbital fat also pushes the eye forward. If rectus muscle tension increases, the eye will be pulled back causing enophthalmos and lid fissure narrowing. Simultaneous cocontraction of the horizontal rectus muscles in Duane’s syndrome, for example, can cause signifi- cant lid fissure narrowing and enophthalmos. In contrast, decreased rectus muscle tone causes proptosis and lid fissure widening. Conditions such as muscle palsies or a detached rectus muscle allow the eye to move forward and result in lid fissure widening. Rectus muscle tightening procedures such as resections tend to cause lid fissure narrowing whereas loosen- ing procedures such as rectus recessions induce lid fissure widening. When the eye is looking straight ahead with the visual axis parallel to the sagittal plane of the head, the eye is in primary position.The vertical rectus muscles follow the orbits and diverge from the central sagittal plane of the head by 23°.
Thus, the visual axis in primary position is 23° nasal to the muscle axis of the vertical rectus muscles (Fig. 2-2). This dis- crepancy between the vertical rectus muscle axis and the visual axis of the eye explains the secondary and tertiary functions of the vertical rectus muscles (see muscle functions, following).
2
24
Superior oblique m.
Levator palpebrae
Superior rectus m.
Intraconal fat
Lateral rectus m.
Inferior rectus m.
Inferior oblique m.
Extraconal fat Müller's m.
Lockwood's lig.
FIGURE 2-1. Side view of extraocular muscles. Note that the rectus muscles pull the eye posteriorly while the oblique muscles pull the eye anteriorly.
FIGURE 2-2. Diagram shows visual axis versus muscle/orbital axis. Note that the visual axes parallel the central sagittal plane, while the orbital axis of each eye diverges 23° from the visual axis.
25
The term position of rest refers to the position of the eyes when all the extraocular muscles are relaxed or paralyzed. Normally, the position of rest is divergent (i.e., exotropic), with the visual axis in line with the orbital axis. The eyes of a patient under general anesthesia are usually deviated in a divergent position.
OCULAR MOVEMENTS
Ductions
The term ductions is used to describe monocular eye move- ments without regard for the movement of the fellow eye (Fig.
2-3). Ductions result from an extraocular muscle contraction 26 handbook of pediatric strabismus and amblyopia
A
B
C
D
E
F
G
FIGURE 2-3A–G. Diagram of ductions, which are monocular eye movements.
that pulls the scleral insertion site toward the muscle’s origin while the opposing extraocular muscle simultaneously relaxes.
The contracting muscle is referred to as the agonist and the relaxing muscle as the antagonist. An upward movement of an eye is referred to as supraduction or sursumduction, a down- ward movement is termed infraduction or dorsumduction, a nasal-ward movement is termed adduction, and a temporal movement is termed abduction. Torsional rotations (twisting movements) are known as cycloductions, with incycloduction (intorsion) referring to a nasal rotation of the 12 o’clock position of the cornea and excycloduction (extorsion) referring to a tem- poral rotation of the 12 o’clock position.
Muscle Action Versus Field of Action
The terms “muscle action” and the “field of action” are often confused. Muscle action refers to the effect of muscle contrac- tion on the rotation of the eye when the eye starts in primary position. Table 2-1 lists the muscle actions of each extraocular muscle. Horizontal rectus muscles have but one action: hori- zontal rotation of the eye. Vertical rectus and oblique muscles,
TABLE 2-1. Extraocular Muscles.
Approximate Action
muscle Anatomic Tendon Arc of from
length insertion length contact primary
Muscle (mm) Origin (mm) (mm) (mm) position
Medial 40 Annulus 5.5 4 6 Adduction
rectus of Zinn
Lateral 40 Annulus 7.0 8 10 Abduction
rectus of Zinn
Superior 40 Annulus 8.0 6 6.5 Elevation
rectus of Zinn Adduction
Intorsion
Inferior 40 Annulus 6.5 7 7 Depression
rectus of Zinn Adduction
Extorsion Superior 32 Orbit apex From 26 12 Intorsion
oblique above temporal Depression
annulus pole of Abduction
of Zinn superior rectus to within 6.5 mm of optic nerve
Inferior 37 Lacrimal Macular 1 15 Extorsion
oblique fossa area Elevation
Abduction
however, have three actions: vertical, horizontal, and torsional.
The most robust action is termed the primary action, followed by the less obvious secondary and tertiary actions. It is impor- tant to remember the classic descriptions of primary, secondary and tertiary muscle actions as they relate to the eye when it is in primary position.
In contrast, the field of action of a muscle is the position of gaze when an individual muscle is the primary mover of the eye.
Granted, virtually all eye movements are the result of combined contraction and relaxation of multiple muscles, but there are eight positions of gaze where one muscle provides the dominant force (Fig. 2-4). For example, when one looks up, the brain recruits both the superior rectus and the inferior oblique muscles. Looking up and nasal, however, is the primary func- tion of the inferior oblique muscle, so this is the field of action of the inferior oblique muscle. A muscle’s function is best eval- uated by having the patient look into the field of action of the 28 handbook of pediatric strabismus and amblyopia
FIGURE 2-4. Diagram of the field of action of the extraocular muscles.
Arrowspoint to the quadrant where the specified muscle is the major mover of the eye. SR, superior rectus; IR, inferior oblique; MR, medial rectus; SO, superior oblique; IO, inferior oblique; IR, inferior rectus; LR, lateral rectus.
muscle. Thus, even though the secondary action of the inferior oblique muscle is abduction, evaluate inferior oblique function by having the patient look “up and nasal.” A patient with an inferior oblique palsy will show limitation of eye movement up and nasal. Note, for straight upgaze, the superior rectus muscle is the major elevator, and for straight down-gaze the inferior rectus is the major depressor, with the oblique muscles con- tributing little.
Smooth Pursuit Versus Saccadic Eye Movements
There are two basic forms of eye movements: smooth pursuit and saccadic. Smooth pursuit eye movements are generated in the occipital parietal temporal cortex, with the right cortex con- trolling movements to the right and the left cortex controlling movements to the left. In humans, smooth pursuit first occurs at 4 to 6 weeks of age. These are slow accurate eye movements requiring visual feedback from central foveal fixation. Smooth pursuit eye movements can follow visual targets moving at velocities up to 30° per second (30°/s). Clinically, accurate smooth pursuit indicates central fixation and in preverbal chil- dren is an indication of good vision.
Saccadic movementsare rapid eye movements with veloc- ities usually ranging from 200° to 700°/s, but saccades have been recorded up to 1000°/s. The peak velocity increases as the ampli- tude of the movement increases, and this relationship is termed the main sequence. Saccades are movements used to keep up with targets moving too fast for smooth pursuit and for quick refixation from one target to another. Saccadic eye movements develop before smooth pursuits, occurring as early as 1 week of age. Saccadic eye movements are generated in the frontal lobes and are under contralateral control; that is, right frontal lobe stimulation will result in a saccadic eye movement to the left.
Saccadic movements can be voluntarily initiated, but they are not voluntarily controlled, and there is no significant visual feedback to adjust the amount of movement. It is thought that the amplitude of a saccadic movement is preprogrammed based on the degree of retinal eccentricity of the target; this is why saccadic movements are termed ballistic, analogous to the bal- listic trajectory of a cannon ball. The neuronal signal that initi- ates a saccade consists of a burst of high-frequency discharge or pulseto the agonist and inhibition of the antagonist. Because all neurons available are activated for eye movements greater than
5°, the magnitude of a saccade is determined by the duration of the pulse. At the end of a saccade, tonic neuronal firing of the agonist and antagonist muscles occurs to hold the eye position referred to as the step. Vision during a saccadic eye movement is suspended or suppressed. Some have used the term saccadic omission for the process of cortical suppression.1A tremendous force is required to produce a saccadic eye movement; therefore, the presence of saccadic eye movements indicates “good” muscle function. Only rectus muscles generate saccadic eye move- ments. When evaluating a patient with limited ductions, look for the presence of a normal saccadic eye movement into the field of limited ductions. If there is a brisk saccade in the direction of the limitation, this indicates good muscle function and suggests the limited movement is caused by restriction, not a muscle paresis.
Optokinetic nystagmus (OKN) can be generated by a slowly rotating drum with stripes and used to evaluate smooth pursuit and saccadic eye movements. As the drum rotates toward the patient’s right, there is a smooth pursuit eye movement to the right to follow the stripe. As the end of the stripe passes, there is a fast saccadic movement to the left to refixate on the next stripe. At target velocities less than 30°/s, smooth pursuit keeps pace with the target. At velocities between 30° and 100°/s, smooth pursuit movements progressively lag behind the target.
At velocities greater than 100°/s, OKN is not evoked. OKN can be used to evaluate saccadic and smooth pursuit eye move- ments. Look at the fast phase of OKN to evaluate saccadic move- ments and the slow phase to evaluate smooth pursuit.
ANATOMY OF THE EYE MUSCLES
Rectus Muscles
The four rectus muscles originate at the orbital apex at the annulus of Zinn and course anteriorly to insert on the anterior aspect of the globe. The “straight” course of the rectus muscles gives rise to the term rectus. The rectus muscle insertions form a progressive spiral termed the spiral of Tillaux around the corneal limbus. The medial rectus muscle is the closest to the limbus (5.5 mm), then the inferior rectus (at 6.5 mm), the lateral rectus (at 7.0 mm), and the superior rectus is the furthest from the limbus (8.0 mm). The muscle–scleral insertion line has 30 handbook of pediatric strabismus and amblyopia
a horseshoe configuration with the rounded apex pointing toward the cornea (Fig. 2-5). One can remember this as the horse- shoes are always galloping toward the cornea. The scleral thick- ness behind the rectus insertions is the thinnest of the eye, being only 0.3 mm thick. Hooking a rectus muscle requires passing the hook several millimeters behind the central muscle inser- tion to clear the posterior aspect of the horseshoe insertion. The widths of the insertions are all approximately 10 mm, and the distance between insertions or intermuscle spacing is only 6 to 8 mm. Because of the proximity of the rectus muscle insertions, it is easier than you might think to hook the wrong muscle during strabismus surgery. An important number to remember is the rectus muscle length, which is 40 mm for all rectus muscles and is also the length of the orbit. Rectus muscles are innervated from the intraconal side of the muscle belly at the junction of the anterior two-thirds and posterior one-third of the muscle.
FIGURE 2-5. Diagram of distance of the rectus muscle insertions from the limbus (in millimeters, mm). Note that the medial rectus muscle inserts closest to the limbus and the distances increase, going counter- clockwise from the medial rectus toward the superior rectus, which inserts furthest from the limbus.
HORIZONTALRECTUSMUSCLES
The horizontal rectus muscles consist of the medial and lateral rectus muscles. In primary position, each muscle has one action:
the medial rectus is an adductor and the lateral rectus is an abductor (Fig. 2-6). When the eye elevates or depresses away from primary position, however, the horizontal rectus muscles take on secondary vertical functions. When the eye is “up,” the horizontal rectus muscles take on a secondary action of supra- duction, and when the eye is “down,” the secondary action is infraduction (Fig. 2-7). In addition, if one surgically transposes a horizontal rectus muscle insertion up, the muscle becomes an elevator in addition to the horizontal function. Supraplacing the horizontal rectus insertions during strabismus surgery will induce a hyperdeviation whereas infraplacement induces a hypodeviation. Vertically displacing the medial and lateral rectus muscle insertion is an excellent way to correct small ver- tical deviations when performing a recession/resection proce- dure. In Duane’s syndrome, the common finding of upshoot and downshoot is probably caused by the secondary elevator and depressor actions of the cocontracting horizontal rectus 32 handbook of pediatric strabismus and amblyopia
FIGURE 2-6. Diagram of simple function of the medial rectus (MR) and lateral rectus (LR) muscle with the eye in primary position.
A
B
C
FIGURE 2-7A–C. Diagram of secondary actions of the medial rectus when the eye rotates up or down. These secondary actions also relate to the lateral rectus. (A) Globe rotated superiorly; now the medial rectus acts as an elevator in addition to its adduction or horizontal function. (B) In the center part of the figure, the medial rectus is a pure adductor. (C) Globe rotated down; in this position, the medial rectus acts as a depres- sor and an adductor.
muscles. Remember, the secondary vertical functions of the horizontal rectus muscles occur only when the eye is rotated vertically off primary position.
MEDIALRECTUSMUSCLE
The medial rectus muscle is innervated by the lower division of the oculomotor nerve (third cranial nerve) and, in primary posi- tion, is a pure adductor. The medial rectus is uniquely diminu- tive. It has the shortest arc of scleral contact (6 mm) and the shortest tendon length of the rectus muscles (4 mm). The infe- rior oblique muscle actually has the shortest tendon (1 mm) of the extraocular muscles, but it is not a rectus muscle. (Be careful; this could be the basis of a trick question.) Of the extraocular muscles, the medial rectus inserts closest to the limbus and is therefore susceptible to insult during anterior segment surgical procedures. Inadvertent removal of the medial rectus muscle is a well-known complication of pterygium removal. The medial rectus is also unique, as it is the only rectus muscle without fascial connections to an adjacent oblique muscle. This lack of oblique muscle connection makes the medial rectus the most difficult to surgically retrieve if lost.
Once disinserted, the medial rectus is free to retract completely off the globe into the orbital fat, making retrieval extremely dif- ficult and, in some cases, almost impossible.
LATERALRECTUSMUSCLE
The lateral rectus muscle is innervated by the sixth cranial nerve and is a pure abductor. In direct contrast to the medial rectus muscle, the lateral rectus has the longest tendon (8 mm) and the longest arc of scleral contact (10 mm) of the rectus muscles. Be careful, the “longest” cited above refers to only rectus muscles, as the superior oblique tendon has the longest arc of contact and tendon length of all the extraocular muscles. (This could be the source of another trick question.) The long arc of contact occurs because the lateral rectus muscle initially has a divergent course following the lateral wall of the orbit. Then, in the anterior orbit, it turns nasally, wrapping around the globe to its scleral inser- tion point (see Fig. 2-6). This temporal to nasal wrap around the globe accounts for the long arc of contact. The inferior border of the lateral rectus muscle courses above the inferior oblique insertion, and there are connective tissue bands connecting the lateral rectus muscle to the inferior oblique muscle.13This is an important anatomic relationship, because a lost lateral rectus 34 handbook of pediatric strabismus and amblyopia
muscle will come to rest at the insertion of the inferior oblique muscle. The surgeon can often find a lost lateral rectus muscle by tracing the inferior oblique muscle back to its insertion.
VERTICALRECTUSMUSCLES
The superior and inferior rectus muscles are the vertical rectus muscles and are the major elevators and depressors of the eye, respectively. The vertical rectus muscles have secondary and tertiary actions because, in primary position, the muscle axis is 23° temporal to the visual axis of the eye (Figs. 2-2, 2-8A).
TEMPORAL NASAL
VISUAL AXIS
MUSCLE AXIS 23°
A
B
VISUAL &
MUSCLE AXIS
C
MUSCLE AXIS VISUAL AXIS
FIGURE 2-8A–C. Functions of the vertical rectus muscles with the eye in various positions of gaze. (A) The eye is in primary position with the visual axis 23° nasal to the muscle axis. (B) The eye is abducted 23° from the primary position, and the visual axis is in line with the muscle axis.
(C) The eye is abducted more than 23° from the primary position, and the visual axis is now temporal to the muscle axis.
Their secondary action is adduction, and it occurs because the vertical rectus muscles pull the front of the eye nasal to the visual axis. Tertiary actions are torsional, consisting of intor- sion for the superior rectus muscle and extorsion for the inferior rectus muscle. These secondary and tertiary muscle actions are dependent on eye position. If the eye is abducted 23°, for example, the muscle and visual axes will be in line, and the vertical rectus muscles lose their secondary and tertiary actions, leaving only their vertical actions (Fig. 2-8B). In this position of 23° abduction, the superior rectus acts purely as an elevator, and the inferior rectus purely as a depressor. With further abduction past 23°, the secondary and tertiary actions of the vertical rectus muscles return, but they are different.
The secondary action for both vertical rectus muscles becomes abduction, and the tertiary functions reverse, becoming extor- sion for the superior rectus and intorsion for the inferior rectus muscle (Fig. 2-8C).
SUPERIORRECTUSMUSCLE
The upper division of the oculomotor nerve innervates the superior rectus muscle. It is the major elevator of the eye, and its actions include supraduction (primary), adduction (secondary), and intorsion (tertiary). The superior rectus muscle overlies the superior oblique tendon and has connec- tive tissue connections to the superior oblique tendon below and the levator palpebrae muscle above (Fig. 2-9). This anato- mic relationship to the levator palpebrae is important because a large superior rectus recession can cause upper lid retrac- tion and lid fissure widening. On the other hand, a superior rectus resection pulls the upper lid down, resulting in lid fissure narrowing. Lid fissure changes associated with superior rectus surgery can be minimized by surgically removing the fascial connections between the levator and the superior rectus muscles.
INFERIORRECTUSMUSCLE
The inferior rectus muscle is innervated by the lower division of the oculomotor nerve and is the principal depressor of the eye. Actions of the inferior rectus muscle include infraduction (primary), adduction (secondary), and extorsion (tertiary). The inferior rectus is sandwiched between the inferior oblique below 36 handbook of pediatric strabismus and amblyopia
and the sclera above (Fig. 2-10). The fascial connection between the inferior rectus muscle, the inferior oblique muscle, and the lower lid retractors (capsulopalpebral fascia) is termed Lock- wood’s ligament (Fig. 2-11).17 These fascial connections are responsible for the eyelid changes that often occur after inferior rectus surgery. An inferior rectus recession results in lower lid retraction with lid fissure widening, and a resection causes lid advancement with lid fissure narrowing. If the inferior rectus is inadvertently disinserted or lost during surgery, these connec- tions will hold the inferior rectus to the inferior oblique and keep it from retracting posteriorly. The surgeon who is in search of a lost inferior rectus muscle can usually find it lying between the inferior oblique and sclera.
FIGURE 2-9. Diagram of the eye and orbit from a top view looking down on the superior rectus (SR) muscle. Note that the superior rectus muscle overlies the superior oblique (SO). T, temporal; N, nasal.
FIGURE 2-10. Diagram of the eye and orbit viewed from below. Note that the inferior oblique (IO) underlies the inferior rectus (IR) muscle.
Conjunctiva Tarsus
Orbicularis m.
ITM CPF Orbital septum
Fornix
Tenon's capsule
Inf. rectus m.
Inf. oblique m.
Lockwood's lig.
CPH
38
OBLIQUEMUSCLES
Like the vertical rectus muscles, the oblique muscles have primary, secondary and tertiary actions. In the case of the oblique muscles, this is because the functional muscle axis is approximately 50° nasal to the visual axis, and the insertion extends posterior to the equator of the eye (Figs. 2-12, 2-13). By
FIGURE 2-11. Diagram of the relationship between the inferior rectus, inferior oblique, lower lid retractors, and Lockwood’s ligament. The infe- rior tarsal muscle (ITM) courses from the posterior border of the tarsus toward the inferior oblique muscle. It then passes between the inferior oblique muscle and the inferior rectus muscle to insert at the capsu- lopalpebral head (CPH). The CPH extends posteriorly to connect the infe- rior oblique to the inferior rectus muscle. The capsulopalpebral fascia (CPF) is the anterior extension of the CPH and courses from the inferior oblique anteriorly to the tarsus along with the ITM. “Lockwood’s liga- ment” (Lockwood’s lig.) consists of these fascial attachments that con- nect the lower lid, inferior rectus, and inferior oblique muscles.
FIGURE 2-12. Diagram of the superior oblique (SO) muscle and tendon.
The functional muscle axis extends from the trochlea to the superior oblique insertion. The muscle axis is 54° nasal to the visual axis.
comparing Figures 2-12 and 2-13, one can see that the oblique muscles have an almost identical functional course with both muscle axes at approximately 50°. The posterior muscle–scleral insertion gives the oblique muscles their seemingly paradoxical vertical functions, with the superior oblique being a depressor and the inferior oblique an elevator. The oblique muscles have no anterior ciliary blood supply, and they do not contribute to the anterior segment circulation. Remember that the “oblique muscles always course below the corresponding vertical rectus muscle” (Fig. 2-14).
SUPERIOROBLIQUEMUSCLE
The primary action of the superior oblique muscle is intorsion, but it also acts as a depressor (secondary) and an abductor (tertiary). Depression and abduction occur as the back of the eye is pulled up and in toward the trochlea. The superior oblique 40 handbook of pediatric strabismus and amblyopia
FIGURE 2-13. Diagram of the inferior oblique (IO) from a view from below. The inferior oblique muscle axis is 51° nasal to the visual axis.
muscle originates at the orbital apex just above the annulus of Zinn and gradually becomes tendon at the trochlea (see Fig.
2-12). After passing through the trochlea, the superior oblique tendon reverses course and turns in a posterior temporal direc- tion to pass under the superior rectus muscle to insert on sclera along the temporal border of the superior rectus muscle (Fig.
2-14). Even though the anatomic origin is at the apex of the orbit, the functional origin of the superior oblique is at the trochlea.
This tendon is the longest tendon of the extraocular muscles, 26 mm in length. The tendon insertion fans out broadly under the superior rectus muscle, extending from the temporal pole of the superior rectus muscle to 6.5 mm from the optic nerve.13 Fascial attachments connect the superior oblique tendon to the superior rectus muscle above and to the sclera below.13 The tendon insertion can be functionally divided into two basic parts: the anterior one-third and the posterior two-thirds.
Posterior fibers are responsible for depression and abduction whereas tendon fibers anterior to the equator are devoted to intorsion. This distinction between anterior and posterior superior oblique tendon fibers is important because one can
FIGURE 2-14. Diagram of posterior anatomy of the eye and muscles.
Note the proximity of the inferior oblique to the macula and vortex veins (vv). The posterior aspect of the superior oblique insertion is in proxim- ity to the superior temporal vortex vein and is approximately 6 to 8 mm from the optic nerve.
manipulate these functions surgically to correct specific motil- ity disorders. The Harada–Ito procedure, for example, involves tightening the anterior fibers of the superior oblique tendon.
Because the anterior tendon fibers intort the eye, the Harada–Ito procedure can be used to treat extorsion associated with supe- rior oblique palsy.
The trochlear nerve innervates the superior oblique muscle at its midpoint from outside the muscle cone. The superior oblique muscle is, in fact, the only eye muscle innervated on the outer surface of the muscle belly. This unique innervation explains why a retrobulbar anesthetic block results in akinesia of all the eye muscles except the superior oblique muscle.
TROCHLEA
The trochlea (Latin for pulley) is a cartilaginous U-shaped struc- ture attached to the periosteum that overlies the trochlear fossa of the frontal bone in the superior nasal quadrant of the orbit. It has been taught that the superior oblique tendon moves through the trochlea much like a rope through a pulley. Anatomic studies have shown, however, that tendon movement is not that simple. Within the trochlea is a connective tissue capsule with connective tissue bands that unite the superior oblique tendon to the surrounding trochlea (Fig. 2-15).46 Some of the tendon slackening distal to the trochlea may come from a telescoping elongation of the central tendon (Fig. 2-16).19This telescoping elongation of the tendon appears to be caused by movement of the central tendon fibers that have scant interfiber connections.
Thus, the mechanism for tendon movement is complex, with at least two mechanisms: (1) tendon movement through the trochlea (pulley and a rope) and (2) tendon elongation (telescoping).
INFERIOROBLIQUEMUSCLE
It is the principal extortor of the eye; however, other actions include elevation (secondary) and abduction (tertiary). The infe- rior oblique muscle originates at the lacrimal fossa located at the anterior aspect of the inferior nasal quadrant of the orbit (see Fig. 2-13). Starting at the lacrimal fossa, the inferior oblique muscle courses posteriorly and temporally underneath the infe- rior rectus muscle to its scleral insertion, which is adjacent to the inferior border of the lateral rectus muscle (see Fig. 2-14).
The inferior oblique muscle has fascial connections to the lower 42 handbook of pediatric strabismus and amblyopia
A
B
FIGURE 2-15A–B. Histology of the trochlea. (A) Low-magnification cross section of midtrochlea. H&E stain. Note horseshoe shape of cartilaginous tissue and the fibrous connective tissue ring that surrounds the superior oblique muscle. At this cross section, the superior oblique is two-thirds muscle and one-third tendon. (B) High-magnification cross section of superior oblique muscle in midtrochlea shows fibrous connective tissue ring connecting to muscle via fine fascial septae.
44 handbook of pediatric strabismus and amblyopia
C
D
FIGURE 2-15C–D. (C) Low-magnification cross section of superior oblique tendon exiting the trochlea. Note small area of cartilage and larger ring of fibrous connective tissue that surrounds the superior oblique tendon as the tendon capsule. At this section, the superior oblique is one- third muscle and two-thirds tendon. (D) High magnification of the supe- rior oblique tendon exiting the trochlea. Note the superior oblique tendon capsule consists of circumferential onionskin layers of fibrous connective tissue. The tendon capsule is attached to the superior oblique tendon capsule by circumferential connective tissue fibers. (From Wright et al., Ref. 46, with permission.)
border of the lateral rectus muscle and to the overlying inferior rectus muscle via Lockwood’s ligament (see Fig. 2-11). When the inferior oblique muscle contracts, it pulls the back of the eye down and in toward the insertion at the lacrimal fossa. This action produces elevation, abduction, and extorsion (Fig. 2-14).
Important structures near the inferior oblique insertion include the macula and inferior temporal vortex vein (Fig. 2-14).
The inferior oblique muscle has only 1 mm of tendon at its insertion.
The inferior oblique muscle is innervated by the inferior branch of the third nerve at a point just lateral to the inferior rectus muscle. Innervation occurs at the posterior aspect of the inferior oblique muscle belly, and the nerve is accompanied by blood vessels forming a neurovascular bundle. This neurovas- cular bundle is surrounded by an inelastic capsule of collagen tissue that protects the inferior oblique nerve from damage caused by stretching.39The neurovascular bundle with its inser- tion into the posterior aspect of the muscle is an important structure in regard to inferior oblique surgery. Anterior transpo- sition of the inferior oblique muscle is an effective surgical FIGURE 2-16. Diagram of anatomy of the trochlea. Note the central fibers of the tendon expand and retract more than the peripheral tendon fibers. (From Ref. 19, with permission.)
procedure used to treat inferior oblique muscle overaction;
however, the complication of postoperative limited elevation has been reported.5,25,26,47This complication is caused by anteri- orizing the posterior muscle fibers at, or anterior to, the inferior rectus muscle insertion, because this tightens the inelastic neu- rovascular bundle.38The tight neurovascular bundle acts as the functional origin of the inferior oblique muscle and changes the action of the inferior oblique muscle from an elevator to a depressor (Fig. 2-17A).16 This author has coined the term J-deformity for this acute bend of the anteriorized inferior oblique.47When the patient looks up, the inferior oblique muscle contracts along with the superior rectus muscle, but the anteri- 46 handbook of pediatric strabismus and amblyopia
Maxillary bone Inferior oblique
muscle
Neurofibrovascular bundle
Inferior rectus muscle
FIGURE 2-17A,B. (A) Diagram of inferior oblique muscle anteriorization with “J-deformity.” The J-deformity is caused by anterior placement of the posterior inferior oblique muscle fibers to the level of the inferior rectus muscle insertion. Because the neurovascular bundle of the inferior oblique muscle inserts in the posterior muscle belly, anteriorization of the posterior muscle fibers produces a tight neurovascular bundle; this causes limited elevation of the eye as active contraction of the anterior- ized inferior oblique muscle pulls against the tight neurovascular bundle.16
orized inferior oblique muscle now depresses the eye and limits elevation; this is an active leash caused by inferior oblique con- traction, and forced ductions on patients with this complication of limited elevation often show only slight restriction to supra- duction. The complication of limited elevation can be avoided while maintaining excellent results by anterior transposition of the anterior muscle fibers at, or a millimeter or two behind, the inferior rectus insertion. Be sure to keep the posterior fibers back, behind the anterior fibers. Placing the posterior muscle fibers several millimeters posterior to the inferior rectus inser- tion and in line with the inferior rectus muscle prevents the J-deformity (Fig. 2-17B).16,47
Vortex vein
Inferior oblique muscle
Inferior rectus muscle
FIGURE 2-17A,B. (B) Diagram of the “graded anteriorization” technique described by Guemes and Wright that is effective in reducing inferior oblique overaction but avoids the postoperative complication of limited elevation.16The new inferior oblique muscle insertion is shown being placed 1 mm behind the inferior rectus muscle insertion, and the poste- rior muscle fibers are placed an additional 4 to 5 mm further posterior, and parallel to the inferior rectus muscle axis. Note that the posterior placement of the posterior muscle fibers avoids the J-deformity. By keeping the posterior muscle fibers posterior to the anterior fibers and avoiding the J-deformity, the neurovascular bundle remains loose, pre- venting postoperative limitation of elevation.
EXTRAOCULAR MUSCLE HISTOLOGY
As are other skeletal muscles, extraocular muscles are made up of striated fibers that, on electron microscopy, show the typical banding pattern of sarcomeres with overlapping threads of actin and myosin. Also resembling other muscles, the strength of an extraocular muscle contraction is dependent on the number of motor units activated (recruitment) and the frequency of muscle fiber stimulation. Extraocular muscles, however, do show some interesting anatomic and physiological differences from other skeletal muscles. The fibers are variable in size, are considerably smaller, and contract more than 10 times faster than other skeletal muscle. Extraocular muscle fibers are innervated at a high nerve fiber to muscle fiber ratio (almost 1:1), whereas other skeletal muscle can have up to 100 muscle fibers for every nerve fiber. This rich innervation, teamed with a fast muscle reaction time, contributes to the precision, accuracy, and control of eye movements.
Another distinction of extraocular muscles is the presence of two distinct muscle fiber types: fast muscle fibers and slow muscle fibers. The fast, or twitch, fibers are single innervated fibers (SIF), innervated by a large motor neuron with “en plaque”
neuromuscular junctions and are typical of mammalian skele- tal muscle. The SIF can be classified into three types: red, intermediate, and white. Red SIF have the highest density of mitochondria and are the most fatigue resistant, while the white SIF have fewer mitochondria and are less resistant to fatigue.
Intermediate and white fibers provide the high transient force needed for the extremely fast saccadic eye movements.
Slow, or tonic muscle fibers, are multiple innervated fibers (MIF) innervated by small-diameter motor nerves with “en grappe” neuromuscular endings characteristic of avian and amphibian muscles. MIF are thought to participate in smooth pursuit movements and static muscle tone to hold and maintain eye position, and SIF probably also play a supportive role in tonic control of eye position and pursuit eye movements. The exact functions of the variety of specific muscle fiber types are unknown, and it is likely that various fibers have overlapping functions.28
Within extraocular muscle tissue are neuromuscular spindles that are concentrated at the muscle–tendon junction.
Neuromuscular spindles are thought to be sensory organs pro- viding information on muscle tone to the brain.9The exact role 48 handbook of pediatric strabismus and amblyopia
of the muscle spindles is unknown, but they may provide pro- prioceptive feedback to motor centers in the brain regarding muscle tone and eye position. Muscle spindles may explain why many adult patients experience transient spatial disorientation after strabismus surgery on the dominant eye.
ARCHITECTURE OF THE EXTRAOCULAR MUSCLES AND PULLEYS
Extraocular muscles have two distinct muscle layers seen on transverse sections (cross section). There is a peripheral layer closest to the orbital wall called the orbital layer (OL) and an inner layer closest to the eye globe called the global layer (GL).33,37OL muscle fibers contain small-diameter fibers with many mitochondria and abundant vessels, staining dark red by Masson’s trichrome. The GL, in contrast, contains larger fibers with variable numbers of mitochondria and fewer vessels; it stains bright red by Masson’s trichrome. Approximately 90% of GL muscle fibers are fast-twitch SIF, with one-third of the SIF being fatigue-resistant red SIF; 80% of OL muscle fibers are twitch-generating SIF and 20% are MIF.33In humans, OL muscle fibers do not appear to run the entire course of the muscle and do not insert in sclera, as there is a gradual decline in the OL in the anterior aspect of the muscle.11,28
Elastic fibers connect the OL to a fibromuscular pulley sleeve that surrounds each extraocular muscle close to the muscle insertion (see Muscle Pulleys, following) (Fig. 2-18).11 There are also muscle-to-muscle-fiber junctions (myomyous junctions) within the OL. GL fibers, on the other hand, are con- tinuous from their origin in the orbital apex to their insertion by tendon into sclera.28Most GL fibers act in saccadic eye move- ments and function only in the field of action of the muscle whereas OL fibers are active throughout the oculomotor range, providing continuous muscle tone to the pulley system.7Collins hypothesized that OL muscle fibers might have a role in maintaining fixation whereas GL muscle fibers participate in dynamic eye movements.7An alternative hypothesis proposed by Demer is that OL muscle fibers actively control pulley posi- tion, thereby influencing the rotational force vectors during eye movements.11,28
A
FIGURE 2-18A–C. Masson’s trichrome stain of 10-m-thick transverse section of medial rectus at the level of the pulley ring of a 17-month-old human. (A) Low power shows the overall architecture of the pulley (P) that surrounds the medial rectus muscle. Fibers in the orbital layer (OL) (arrowheads) insert in the pulley, shown at high power in (B). The OL muscle layer takes the form of a C-shape and is on the left, delineated by the large arrows; the global layer (GL) fibers are to the right. OL on the leftis shown on the bottom.
50
B
C
FIGURE 2-18A–C. (B) High-power magnification shows the insertion of the OL into the pulley (taken from the upper left box on A). (C) High- power magnification of the GL and pulley relationship. The GL does not insert into the surrounding pulley (taken from the middle right box on A).11,28
EXTRAOCULAR MUSCLE FASCIA
A smooth white connective tissue, Tenon’s capsule, underlies the conjunctiva and envelops the globe and extraocular muscles.
This delicate membrane partitions the orbital contents, iso- lating the globe and extraocular muscles from the surrounding orbital fat. Another fascial structure interconnected with Tenon’s capsule is the muscle sleeve or extraocular muscle pulley, which suspends the extraocular muscles.
Muscle Pulley (Muscle Sleeve)
Each of the rectus muscles passes through a pulley system con- sisting of a sleeve or ring of collagen, elastic, and smooth muscle fibers. Previously, this structure was termed muscle sleeve. The medial rectus muscle pulley has the most fibroelastic tissue and smooth muscle. Muscle pulleys connect to the orbital layer (OL) of the rectus muscle, to the orbital wall, to adjacent extraocular muscles, and to Tenon’s capsule.10The pulley or sleeve extends for approximately 10 mm from the equator of the globe anteri- orly to approximately 6 mm from the muscle insertion. During strabismus surgery, one can see these bands as they connect the surrounding muscle sleeve or pulley to the OL of the rectus muscle. Similar to the trochlea and superior oblique tendon, the pulleys guide the rectus muscles to their insertion point. In con- trast to the superior oblique muscle, which changes direction after passing through the trochlea, rectus muscle pulleys keep the muscle in line with their anatomic origin. Demer has sug- gested that in secondary gaze positions the extraocular muscle path is “discretely inflected by the pulley.”6Demer et al. also hypothesized that OL muscle fibers insert into the pulley system and actively influence pulley position and the mechan- ics of ocular rotation.11,28
Tenon’s Capsule
Tenon’s capsule is a collagen-elastic tissue that is a continuous membrane surrounding the eye and extraocular muscles.22This membrane separates surrounding orbital fat from the globe and extraocular muscles. The elastic nature of Tenon’s capsule allows free rotation of the globe and unrestricted muscle relax- ation and contraction. For clinical and surgical purposes, it is useful to subdivide it into the following categories:
52 handbook of pediatric strabismus and amblyopia
1. Intermuscular septum 2. Anterior Tenon’s capsule 3. Posterior Tenon’s capsule 4. Check ligaments
5. Muscle sleeve (see Pulley System, earlier)
INTERMUSCULARSEPTUM
This thin tissue lies sandwiched between the conjunctiva and sclera, spanning between the rectus muscles (Fig. 2-19).30,40 During strabismus surgery, intermuscular septum can be iden- tified as the white membrane on each side of the rectus muscles.
When elevated with muscle hooks, the intermuscular septum takes on the appearance of the wings of a manta ray (Fig. 2-20).45 The intermuscular septum can be safely incised during strabis- mus surgery, as it is not a barrier to orbital fat.
ANTERIORTENON’SCAPSULE
This tissue is the subconjunctival membrane anterior to the muscle insertions. It proceeds forward with the intermuscular septum and fuses with the conjunctiva at 2 to 3 mm posterior to the corneal limbus (Figs. 2-18, 2-20). When suturing a muscle during strabismus surgery, it is important to dissect anterior Tenon’s capsule off the tendon insertion to avoid the complica-
Reflected conjunctiva
Anterior Tenon's Capsule SR
MR LR
IMS
IMS
FIGURE 2-19. Anterior ocular fascia. Intermuscular septum (IMS) is the connective tissue that spans between the rectus muscles underneath the conjunctiva. Anterior Tenon’s is that tissue anterior to the rectus muscle insertions; it fuses with the conjunctiva 3 mm posterior to the limbus.
54 handbook of pediatric strabismus and amblyopia
A
B
FIGURE 2-20A,B. (A) Lateral rectus muscle with intermuscular septum and check ligaments. Check ligaments overlie the rectus muscle and connect the muscle to the overlying conjunctiva. Intermuscular septum is seen on either side of the lateral rectus muscle, spanning between the superior and inferior rectus muscles. (B) Photograph shows the Jameson hook under the lateral rectus muscle and Desmarres retractor pulling the conjunctiva posteriorly. (Figure published with permission of J.B. Lippincott Co. from Wright KW. Color Atlas of Ophthalmic Surgery: Strabismus. Philadelphia:
Lippincott, 1991.)
tion of a slipped muscle (Fig. 2-21). If anterior Tenon’s capsule is left on the tendon, the surgeon may inadvertently suture and secure anterior Tenon’s capsule, missing all or part of the tendon. The unsuspecting surgeon then disinserts the unsutured tendon and allows the muscle to slip posteriorly while anterior Tenon’s capsule is placed at the intended recession site.31 A slipped muscle is a frequent cause of unexpected overcorrection after recession procedures, as it often goes unrecognized at the time of surgery. Remember that some slipped muscles involve only part of the muscle and can present as a mild overcorrection with relatively good muscle function.48
POSTERIORTENON’SCAPSULE
This tissue lines the posterior globe and functions to separate orbital fat from the sclera (Fig. 2-22). Just anterior to the equator of the eye, the four rectus muscles penetrate Tenon’s capsule and become surrounded by intra- and extraconal orbital fat. At this juncture, Tenon’s capsule unites with the capsule of the rectus muscle to form a muscle pulley or muscle sleeve (see Muscle Pulley, earlier). The muscle sleeve is an important surgical
Anterior Tenon's capsule
Anterior ciliary artery
Medial rectus muscle
FIGURE 2-21. Anterior Tenon’s capsule is the white tissue retracted anteriorly with a small Steven’s hook (bottom left hook). During strabis- mus surgery, it is important to remove the anterior Tenon’s capsule to visualize the muscle tendon for suturing. Note the anterior ciliary vessels on the tendon insertion.
landmark when looking for a slipped or lost rectus muscle. A lost muscle is a rectus muscle that has become completely detached from the globe because of trauma or a surgical mistake.32,48Once lost, the muscle will slip posteriorly within the muscle sleeve to be surrounded by intra- and extraorbital fat. To find a lost muscle, first find the muscle sleeve located between the intra- and extraconal fat; then, carefully follow the sleeve to retrieve the muscle. When looking for a lost medial rectus muscle, avoid the tendency to follow the sclera posteriorly, as this leads to the optic nerve. An important complication of attempted retrieval of a lost medial rectus muscle is inadvertent transection of the optic nerve that is enshrouded in postoperative scar tissue.
Together, posterior Tenon’s capsule, anterior Tenon’s capsule, and the muscle sleeve are very important structures as they are the barrier that keeps orbital fat from the globe and extraocular muscles. If posterior Tenon’s capsule or muscle sleeve is traumatically or surgically violated, fat adherence can occur because orbital fat prolapses through the torn Tenon’s capsule and scars to the sclera or an extraocular muscle (Fig.
2-23). The scarring of orbital fat produces a restrictive scar, which extends from the periosteum to the eyeball. As the scar 56 handbook of pediatric strabismus and amblyopia
Medial rectus muscle
Posterior Tenon's capsule
Intraconal fat
Extraconal fat Muscle sleeve (pulley)
Anterior Tenon's capsule
Conjunctiva
Fused anterior Tenon's and conjunctiva
FIGURE 2-22. Drawing of a rectus muscle showing fascial relationships.
Note that the muscle penetrates posterior Tenon’s capsule; the capsule at this point forms a muscle sleeve or muscle pulley. Intraconal and extra- conal fat are isolated from the globe by Tenon’s capsule.
contracts over weeks to several months, the scar pulls the eye, producing a restrictive strabismus associated with limitation of eye movements. Fat adherence can occur as a complication of almost any extraocular surgery (e.g., strabismus surgery, retina surgery) or periocular trauma.31,49Extreme care must be taken when operating in the area of orbital fat, which starts 10 mm posterior to the limbus. Once fat adherence occurs, it is almost impossible to correct. Surgically induced fat adherence can usually be avoided if the surgeon carefully dissects close to muscle belly or sclera, thus preserving the integrity of the over- lying posterior Tenon’s capsule and muscle sleeve.
CHECKLIGAMENTS
These are fine falciform webs that overlie the rectus muscles and join the muscle capsule with overlying bulbar conjunctiva
A
B
FIGURE 2-23A,B. Diagram modified after Parks and published in Oph- thalmologyby Wright (1986)49 shows the pathophysiology of the fat adherence syndrome. (A) Normal anatomy with orbital bone, periorbita, extraconal fat, muscle, and intermuscular septum. Note that the fat is isolated from muscle and sclera by intact Tenon’s capsule and intermus- cular septum. (B) Violation of Tenon’s capsule with fat adherence to the globe and muscle (to right).
at the muscle tendon (see Fig. 2-20). More posteriorly, check lig- aments are probably the bands that connect the OL muscle fibers to the surrounding muscle sleeve (muscle pulley). In the case of the superior and inferior rectus muscles, check ligaments also connect to the levator muscle and lower lid retractors, respec- tively. A recession or resection of vertical rectus muscles requires removal of these ligaments to avoid lid fissure changes after surgery.
VASCULAR SUPPLY TO THE ANTERIOR SEGMENT
The anterior segment and iris are supplied by the anterior ciliary arteries, conjunctival vessel, and the long posterior ciliary arteries (Fig. 2-24). Approximately 50% of the anterior segment circulation comes from the long posterior ciliary arteries and 58 handbook of pediatric strabismus and amblyopia
FIGURE 2-24. Diagram of circulation of the anterior segment with the rectus muscle supplying the anterior ciliary arteries (aa); the deep long posterior arteries are also shown. (Figure published with permission of J.B. Lippincott Co. from Wright KW. Color Atlas of Ophthalmic Surgery:
Strabismus. Philadelphia: Lippincott, 1991.47)
50% from the anterior ciliary arteries.44The conjunctival vessels also contribute to anterior segment circulation.14 Anterior ciliary arteries and the conjunctival vessels merge at the limbus to form the episcleral limbal plexus.27 These vessels in turn connect with the major arterial circle of the iris, which is also fed by the two long posterior ciliary arteries. The superior rectus, inferior rectus, and medial rectus muscles have at least two ante- rior ciliary arteries and are major contributors to the anterior segment circulation.18The lateral rectus has a single anterior ciliary artery and, of the four recti muscles, the lateral rectus probably provides the least in the way of anterior segment cir- culation.20,41The oblique muscles do not have anterior ciliary arteries, and they do not contribute to the anterior segment circulation.
Iris angiograms can be used to assess anterior segment circulation in blue-eyed patients. Removal of a vertical rectus muscle will cause hypoperfusion in that area that relates to the vascular input.18It is interesting that this hypoperfusion lasts only 1 to 2 months because its collateral circulation and vasodi- latation will replenish the hypoperfused area.45 Additionally, infants and children do not typically show hypoperfusion even when multiple rectus muscles are removed. Removal of a rectus muscle during strabismus surgery will permanently interfere with vascular supply of the anterior ciliary arteries unless the surgery is performed specifically to maintain anterior segment circulation. Surgeries have been devised that attempt to main- tain anterior segment circulation despite manipulations of the muscle position.24,45Iris angiograms can be used to document anterior segment blood flow from the anterior ciliary arteries in nonhuman primates. A muscle-to-sclera plication developed by this author (Wright plication) is designed to tighten a rectus muscle but spare the anterior ciliary arteries. Instead of resect- ing the muscle, as is done in the standard muscle tightening pro- cedure, the Wright plication folds the muscle, suturing muscle to sclera without disrupting the anterior ciliary vessels. Figure 2-25 shows an iris angiogram after inferior rectus muscle plica- tion and surgical removal of the other three rectus muscles in a nonhuman primate. The iris angiogram demonstrates intact per- fusion from the inferior rectus muscle and hypoperfusion supe- riorly because the arteries of the other three rectus muscles had been sacrificed on surgical removal.
Anterior segment ischemia can be a consequence of strabismus surgery, most often after a three- or four-muscle
