Extraocular Muscles

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Diagnostic Intervention

Description/Overview

Introduction

Extraocular muscles are the most specialized skeletal muscles in the human body. These are broadly divided into voluntary and involuntary muscles. The voluntary muscles include seven extraocular muscles that control the movements of the eye and eyelids, and are important for binocular single vision. These include four recti muscles, two oblique muscles, and levator palpebrae superioris. The four recti include the superior, inferior, medial, and lateral rectus. The two oblique muscles include the superior oblique and inferior oblique. These six muscles are responsible for the movement of eyes into different gazes. The levator palpebrae superioris is responsible for eyelid elevation. The involuntary muscle group include superior tarsal muscle (Muller's muscle), inferior tarsal muscle and orbitalis. Understanding the principles of extraocular muscle movements plays a key role in the diagnosis of various strabismus pathologies.[1]

Embrology

The orbit and the extraocular muscles are embryologically derived from the mesoderm and the neural crest cells. The extraocular muscles per se are derived from the mesoderm, and the connective tissue surrounding the muscles is derived from the neural crest cells.[2] The extraocular muscles are thought to arise from two different subsets of mesenchymal cells including the paraxial and prechordal head mesoderm.[3] The lateral rectus and superior oblique arise from the unsegmented paraxial head mesoderm, whereas the superior, inferior, medial rectus and the inferior oblique are thought to arise from the prechordal head mesoderm.[4]

Blood Supply

Arterial Supply

The extraocular muscles (EOM) receive their major blood supply from the ophthalmic artery's medial and lateral muscular branches. The medial muscular branch supplies the medial rectus, inferior rectus, and inferior oblique.[5] The lateral muscular branch supplies the lateral rectus, superior rectus and oblique, and the levator palpebrae superioris. The superior, inferior, and medial rectus muscles receive blood supply via two anterior ciliary arteries that communicate with the anterior circle of the ciliary body. The lateral recti muscle receives blood supply from a single branch of the lacrimal artery. The inferior rectus and inferior oblique also receive partial blood supply from the infraorbital artery, a branch of the maxillary artery.[6]

Venular Supply

Venous drainage occurs through the vortex veins into the superior and inferior orbital veins. Vortex veins are located along the lateral and medial aspects of the superior and inferior rectus muscles. These vortex veins then drain into the orbital venous system.[7]

Applied Aspects

There is a risk of iatrogenic damage to the vortex veins during surgery on IR or SR. The blood supply of EOM also supplies most of the anterior segment. Thus, procedures involving damage to vascular supply should be limited to a maximum of two rectus muscles at a time given the increased risk of anterior segment ischemia.[8]

Nerve Supply

The chief nerve supply of the extraocular muscles is received from the third, fourth, and sixth nerves. The third (Oculomotor) nerve supplies multiple extraocular muscles, while the fourth (Trochlear) and the sixth (Abducent) nerve supply individual extraocular muscles.[9] Details of the nerve supply of different extraocular muscles are mentioned in Table 1.

Nerve Supply of Extraocular Muscles
S.No Nerve Supply Extraocular Muscles Supplied
1 Oculomotor nerve – Superior division Superior rectus, Levator palpebrae superioris
2 Oculomotor nerve – Inferior division Medial rectus, Inferior rectus, Inferior oblique
3 Trochlear nerve Superior oblique
4 Abducens nerve Lateral rectus

Origin of Extraocular Muscles

Figure 1- Schematic diagram showing the course and anatomical relation of the extraocular muscles in the eye.

The rectus muscles originate from the annulus of Zinn, which is a common tendinous ring lying in the back of the orbit.[10] The superior rectus originates from the upper part of the annulus of Zinn, which is attached to the dura mater of the optic nerve.[11] The levator palpebrae superioris arises medial and superior to the origin of the superior rectus muscle. The other recti muscles, i.e., the medial, inferior, and lateral recti, also arise from the annulus of Zinn. Each of the recti muscles courses anteriorly along the orbit’s walls and gets inserted into the sclera at varying distances, as shown in Figure 1. The four recti muscles form the muscle cone within the orbit.[12] The apex of the muscle cone is at the annulus of Zinn, the point of origin of the recti muscles. The cone widens as the muscles progress anteriorly, forming its base at the points of muscle penetration into the tenon’s sheath. Each muscle is enclosed by the fibrous capsule, which is attached by a thin continuous membrane called an “intermuscular septum”. The intermuscular septum divides the orbital fat pad into intraconal and extraconal fat.[13]

Figure 2- Schematic line diagram of the eye showing the insertion of extraocular muscles, the relative distance of insertion from the limbus, and the spiral of tillaux

The medial rectus inserts closest to the limbus, around 5.5mm, followed by the inferior rectus, which inserts at 6.5mm; the lateral rectus at 6.9mm and the superior rectus inserts farthest from the limbus, which is 7.7mm.[1] These insertion distances may vary from individual to individual. The spiral formed by joining the insertion points of the four recti muscles is referred to as the Spiral of Tillaux, as shown in Figure 2. The origin and insertion of each muscle are discussed under separate headings below.

Applied Anatomy

The Trochlear nerve passes above the annulus of Zinn and does not lie within the muscle cone. Thus, the retrobulbar anesthesia, directed into the muscle cone, spares the trochlear nerve and, therefore, the superior oblique muscle.[14]

Listing Plane and Fick’s Axis

Figure 3- Schematic line diagram depicting the Listing’s plane, the center of rotation of the eye, and different Fick’s axis

The listing plane is an imaginary equatorial plane containing the globe's center of rotation.[15] Fick’s axis is the axis around which the globe rotates. X and Z axis are included in the Listing plane, and the Y axis is a sagittal axis that lies perpendicular to the Listing plane. Vertical rotations occur around the X-axis, horizontal movements around the Z-axis, and torsional around the Y-axis.[16] The different Fick’s axis and movements around each axis are demonstrated in Figure 3.

Description of Individual Muscles

Medial Rectus (MR)

Course: The medial rectus originates from the medial part of the annulus of Zinn at the orbital apex and passes forward to get inserted at around 5.5mm away from the limbus. The medial rectus has the shortest tendon (4.5mm) among all the recti muscles. This is the only rectus muscle with no oblique muscle running tangentially.[17]

Action – Adduction[5]

Innervation – Oculomotor nerve (Third cranial nerve)[18]

Applied aspects – In case the medial rectus muscle gets lost or slips following trauma or iatrogenic causes such as during squint or pterygium surgery, there is no reference point to retrieve this muscle.[19]

Lateral Rectus (LR)

Course: The lateral rectus originates from the lateral part of the annulus of Zinn and progresses forwards to get inserted approximately 6.9mm from the limbus. The lateral rectus muscle has the broadest arc of contact, i.e., 12mm, among all the recti muscles.[20] The lateral rectus is the thinnest extraocular muscle having a width of only 9.2 mm. The intermuscular septa attach the lateral rectus to the inferior oblique muscle.

Action – Abduction

Innervation – Abducens nerve (Sixth cranial nerve)

Applied aspects - During recession or resection procedures, the lateral rectus must be separated from the inferior oblique fibers. Otherwise, there might be an inadvertent shifting of the inferior oblique tendon with the lateral rectus.[21]

Superior Rectus

Course: The superior rectus muscle originates from the superior part of the annulus of Zinn and proceeds anteriorly along the orbital wall to get inserted into the sclera at a distance of approximately 7.7mm from the limbus. The superior rectus is attached to the fibers of the levator palpebrae superioris that courses above this muscle from the point of origin. The superior oblique muscle lies between the superior rectus and the sclera.[22] Both the muscles are connected to each other by the intermuscular septa.

Action – Primary action is elevation. Additional actions include incyclotorsion and adduction.

Innervation – Oculomotor nerve (Third cranial nerve)

Applied aspects – A pseudoptosis may appear in a hypotropic eye as the upper eyelid follows the superior rectus muscle. A squint surgery involving superior rectus resection can result in drooping of the upper lid.[23]

Inferior Rectus (IR)

Course: The inferior rectus muscle originated from the inferior part of the annulus of Zinn and then proceeds anteriorly to get inserted at an approximate distance of 6.5mm from the limbus. The inferior oblique muscle passes beneath the inferior rectus.[24] The inferior rectus muscle is also strongly connected to the lower eyelid retractors.

Action – Primary action is depression. Additional actions include excyclotorsion and adduction.

Innervation – Oculomotor nerve (Third cranial nerve)

Applied Aspects – Recession or resection procedures involving the inferior rectus muscle may result in widening or narrowing of the lower eyelid, respectively.[23]

Superior Oblique

Figure 4- Intraoperative picture of the eye showing the superior rectus and superior oblique muscles. After reflection from the trochlea, the superior oblique passes beneath the superior rectus to get inserted on its lateral aspect.

Course: The superior oblique muscle originates from the periosteum of the sphenoid bone, superomedial to the optic foramen, and the common tendinous ring. It then progresses anteriorly, parallel to the medial wall of the orbit, to reach the trochlea.[25] The trochlea is a cartilaginous loop attached to the frontal bone's nasal part. After looping through the trochlea, the muscle becomes a tendon, turning posterolateral and passing beneath the superior rectus. It finally gets inserted posterior and lateral to the insertion of the superior rectus, as shown in Figure 4. The superior oblique is the longest muscle of all the extraocular muscles.

Action – Primary action is incyclotorsion. Additional actions include depression and abduction.

Innervation – Trochlear nerve (Fourth cranial nerve)

Applied aspects - The superior oblique is the only muscle that receives innervation from the Trochlear nerve. The trochlear nerve is the only cranial nerve that emerges from the posterior aspect of the brainstem.[26]

Inferior Oblique (IO)

Course: It originates from the orbital floor lateral to the nasolacrimal groove. The muscle then runs along the orbit floor and crosses below the inferior rectus muscle. It then ascends posterolateral to pass between the lateral rectus and the orbit floor. It then inserts posterior to the equator in the inferolateral quadrant onto the sclera. The fascial sheath of the inferior oblique blends with the sheath of the inferior rectus, which then blends with the medial and lateral check ligaments.[27] The fusion of all these forms the suspensory ligament of the eyeball, which is a hammock-like sling that supports the eyeball. The inferior check ligament is an anterior expansion from the fused sheaths of the inferior rectus and oblique muscles that attach to the tarsus muscle of the lower eyelid.[28]

Action – Primary action is excyclotorsion. Additional actions include elevation and abduction.

Innervation – Oculomotor nerve (Third cranial nerve)

Figure 5- Intraoperative picture of the eye showing the lateral rectus and inferior oblique muscles. The inferior oblique can be seen as a rounded cord-like structure.

Applied Aspects – Inferior oblique muscle overaction is commonly associated with congenital squints, especially congenital esotropias.[29] The inferior oblique is the only muscle that must be retrieved from the tenons, not directly from the scleral insertion point. Since the fibers are closely associated with the lateral rectus, isolating the inferior oblique while operating on the lateral rectus muscle is important, as shown in Figure 5.

Levator Palpebrae Superioris (LPS)

Course: The LPS is a thin triangular muscle extending along the bony orbit’s roof. It originates from the inferior aspect of the lesser wing of the sphenoid, superior to the annulus of Zinn. The muscle originates as a short and narrow tendon, which fans out and gradually widens as it courses anteriorly.[30] Once it reaches the Whitnall’s ligament, a transverse suspensory ligament, the LPS muscle becomes more tendinous and changes its direction to become vertical, called the vertical levator aponeurosis. The levator aponeurosis has multiple insertions. The aponeurosis has medial and lateral wings which attach to the medial and lateral canthal tendons, respectively. It inserts anteriorly into the upper eyelid skin, inferiorly into the anterior surface of the upper tarsal plate, and has few extensions to the superior conjunctival fornix.

Action- Elevates upper eyelid

Innervation- Oculomotor nerve (Third cranial nerve)

Applied Aspects- Myogenic or neurogenic problems related to LPS can lead to ptosis.[31] It is essential to separate the LPS from the superior rectus during squint or ptosis surgery to avoid iatrogenic side effects on the lid position.

Arc of Contact

All the rectus muscles arise from the annulus of Zinn and proceed anteriorly to reach the globe. The point of tangency is where the muscle first comes in contact with the globe. This point of first contact is defined as the effective insertion point of muscle that determines the vector of force exerted by the muscle.[32] The arc of contact is defined as the circular area the muscle travels from the first point of contact (point of tangency) to the anatomical insertion point. Applied aspects: Recession of muscle acts by shortening its effective length and arc of contact. Resection has a strengthening effect as it increases the effective length as well as the arc of contact.[33]

Actions of Extraocular Muscles

All the extraocular muscles are responsible for the eye’s movement in different gazes. There are a few basic concepts that are important to understand muscle actions. The extraocular muscles have different actions in different eye positions.[34] The primary action of the muscle is the major action of muscle in the primary position. Subsidiary actions are which occur in different positions of the globe. The different muscle actions are listed in Table 2.

Primary, Secondary and Tertiary action of extraocular muscles
Muscle Primary Action Secondary Action Tertiary Action
Lateral rectus Abduction - -
Medial rectus Adduction - -
Superior rectus Elevation Intorsion Adduction
Inferior rectus Depression Extorsion Adduction
Superior oblique Intorsion Depression Abduction
Inferior oblique Extorsion Elevation Abduction
Levator palpebrae superioris Elevation of upper lid - -

Types of Eye Movements

Ductions - These are monocular movements around the Fick’s axis. These include adduction, abduction, elevation, depression, intorsion, and extorsion.

Versions - These are binocular, simultaneous, conjugate movements. These include dextroversion, levoversion, elevation, depression, dextroelevation, dextrodepression, levoelevation, levodepression, dextrocycloversion, or levocycloversion.[35]

Figure 6- Schematic diagram showing different ocular movements, including the versions and vergences.

Vergences - These are bilateral, simultaneous, disconjugate movements. These include convergence and divergence. These are shown in Figure 6.

Positions of Eye

Primary - This is defined as the eye position when one is looking straight ahead with an erect head and body, the object of regard at infinity, and lies at the intersection of the sagittal plane of the head and a horizontal plane passing through the center of rotation of two eyeballs.[36]

Secondary - These include eye positions obtained with movement around the X and Z axis. These include adduction, abduction, elevation, or depression.[37]

Tertiary - These include movement of the globe around the Y axis, that is, detroelevation, dextrodepression, levoelevation, and levodepression.

Positions of Gaze

Cardinal positions - There are six cardinal positions. In each eye, one principal muscle is responsible for moving the eye into that position.[38]

Figure 7- Schematic diagram depicting the primary (pink), cardinal (highlighted green), and diagnostic positions of the eye. Two yolk muscles (i.e., one muscle from each eye) are responsible for each cardinal position, mentioned in pairs in the diagram.

Diagnostic positions - There are a total of nine diagnostic positions. These include the six cardinal positions (highlighted green), primary position (pink circle), elevation, and depression, as depicted in Figure 7.

Laws of Ocular Motility

Agonist-Antagonist

These are muscles that move the eye in opposite directions. Agonist is the primary muscle of the eye that moves it in a particular direction. An antagonist is a muscle in the same eye that moves it in the opposite direction.[39] For example – the left medial rectus adducts the eye, and its antagonist’s muscle is the left lateral rectus which abducts the same eye.

Synergist

These are muscles of the same eye that move the eye in the same direction.[21] For example – the left inferior rectus and the left superior oblique are synergists for depression.

Yoke Muscles (Contralateral synergist)

These are pairs of muscles, one in each eye, that produce conjugate eye movements. Example- right superior rectus and left inferior oblique.

Donder’s Law

States that for any gaze direction, the eye’s spatial orientation is unique and independent of previous eye orientation/gaze directions.[40]

Listing’s Law

As per this law, all eye orientations can be achieved starting from a primary eye position. Different gazes can be achieved by moving around the axis within the Listing’s plane.[41]

Hering Law

This is the law of equal innervation. This law states that equal and simultaneous innervation flows to the yoke muscles for conjugate eye movement.[42]

Example – For levoversion, equal and simultaneous innervation is received by the left lateral rectus and right medial rectus. An exception to this law is dissociated vertical or horizontal deviation.

Applied aspects: In patients with paralytic strabismus, an excess innervation is required to fixate with the eye with paralyzed muscle. This leads to a similar concomitant excess supply to the yoke muscle leading to a greater secondary deviation than the primary deviation.

Sherrington’s Law

This is the law of reciprocal innervation. As per this law, the increased innervation to one muscle is accompanied by a reciprocal decrease in innervation to the antagonist’s muscle. For example - during levoversion, there is an increased innervation to the left lateral rectus, accompanied by a simultaneous decrease in innervation received by the left medial rectus.[43] An exception to this law is Duane’s retraction syndrome.

Muscle Orientation

Vertical recti

Fig 8: Schematic diagram showing a) the orbital axis and the muscle axis at 23° for rectus muscles, b) with 23° abduction, the orbital and muscle axis come in the same plane, and the muscle acts as a pure elevator/ depressor, c) with 67° adduction, the orbital axis and muscle axis lie perpendicular to each other, and muscle acts as a pure torsional muscle

The vertical recti muscles (superior, inferior rectus) form an angle of 23° with the visual axis, as shown in Figure 8. The visual and the orbital axis coincide once the eye is 23° abducted. The eye has no subsidiary actions in this gaze, and recti muscles act as pure elevator/ depressor. Once the eye is 67° adducted, the visual axis forms an angle of 90° with the orbital axis. In this position, the recti muscles act as pure torsional muscles.[12]

Oblique muscles

Fig 9: Schematic diagram showing a) the orbital axis and the muscle axis at 51° for oblique muscles, b) with 51° adduction, the orbital and muscle axis lie in the same plane, and the muscle acts as a pure elevator/ depressor c) with 39° abduction, the orbital axis and muscle axis lie perpendicular to each other, and muscle acts as a pure torsional muscle

The oblique muscles form an angle of 51°with the visual axis, as shown in Figure 9. When the globe is 51° adducted, the visual and the orbital axis align, and the oblique muscles act as pure elevators/depressors. In 39° abduction, the visual axis and the orbital axis are at 90° to each other, and the oblique muscles work as pure torsional muscles.[44]

Extraocular Muscle Microscopy in Normal Eyes

Figure 10- Schematic diagram depicting normal sarcomere structure, consisting of A band and I band in an extraocular muscle.

The extraocular muscle fibers are skeletal muscles that histologically show tight and normally arranged striations. The transmission electron microscopy consists of skeletal muscle fibers with intact basal membrane and sarcolemma, tightly aligned myofibrils with well-arranged sarcomeres, Z line, and H zone, along with normal distribution of mitochondria.[45] These are depicted in Figure 10.

Extraocular Muscle Microscopy in Strabismic Eyes

Martinez et al. studied the myofibrillar structure in the strabismic eyes and found marked variations in muscle fiber shape and size.[46] They also noted small, hypertrophied, whorled, ringbiden fibers in the myofibrils. Sarcomere disruption was also reported in 2-3mm sections. Ultrastructural features revealed vacuoles within myofilament bundles, smearing of Z bands, and nemaline rods. They also found abnormal mitochondria and “Zebra” or “Striated” foreign bodies in a few extraocular muscles. Falki et al. also reported the skeletal muscle fibers to be disarranged, atrophied, swollen, or disintegrated in strabismic patients.[47] Electron microscopy revealed vacuolation and degenerated myofibrils, lipid droplet accumulation, and clustered mitochondria in strabismic eyes.

Developmental Anomalies of Extraocular Muscles

Congenital Absence of Muscle

These patients may present mimicking muscle paralysis. It is difficult to differentiate and diagnose the absence of muscle pre-operatively and comes as a surprise intraoperatively.[48] Surgeons should be prepared with alternative surgical procedures in such cases. These have been more commonly reported in patients with craniofacial dysostosis.[49][50]

Accessory Extraocular Muscle

Three different types of accessory extraocular muscles have been reported in the literature. These include anomalous muscle bands bridging two muscles, fibrous tissues adjacent to muscles that attach to the globe, and muscles arising from posterior orbit and inserting on globe or extraocular muscles.[51] Wahl proposed that these fibromuscular tissue bands represent atavistic retractor bulbi muscles.[52] Dobbs et al reported a case of large exotropia with Gorlin syndrome who was found to have bilateral anomalous extraocular muscles inferolateral to the optic nerves.[53]

Fascial Sheath Anomalies

This is more common. The fascial sheath acts as a check for active and passive movements of the globe. Anomaly of the fascial sheaths may lead to ocular movement abnormality even with normal anatomical and functional muscles. Examples include the Tendon sheath syndrome of Brown syndrome.[54]

Clinical Relevance

Cranial Nerve Palsies

The extraocular muscles receive innervation from three cranial nerves, including the oculomotor, trochlear, and abducens. Damage to extraocular muscles or their innervation can affect ocular motility, resulting in altered ocular alignment or binocular double vision.[55]

Oculomotor Nerve Palsy

An insult to the oculomotor nerve affects most of the extraocular muscles. The patient typically presents with a dropping of the lid, along with the limitation of adduction, elevation, and depression to varying degrees. The eye assumes a down-and-out position, secondary to functional lateral rectus (abduction) and superior oblique (depression).[56][57]

Trochlear Nerve Palsy

An insult to the trochlear nerve that paralyzes the superior oblique muscle. Examination fails to reveal any noticeable difference in the resting position of the eyeballs. Careful slit lamp examination often reveals a limited intorsion. The patient often complains of binocular double vision, which is more troublesome in the downgaze. There is usually an associated head tilt away from the site of the lesion.[58] [59]

Abducens Nerve Palsy

An insult to the abducens nerve paralyzes the abducens muscles. The affected muscle rests in adduction because of the effect of the medial rectus muscle. The patient presents with a face turn towards the side of the affected muscle. Multiple cases have been reported secondary to giant cell arthritis, trauma, and post-COVID-19 vaccination.[60][61] Recently a case of bilateral sixth nerve palsy with subdural hematoma was reported secondary to vitamin B12 deficiency.[62]

Strabismus

Strabismus often referred to as crossed eyes or lazy eye, is abnormal alignment of both eyes. This can occur secondary to defects in extraocular muscles or due to defects in their neurological control. Different types of deviations can be esotropia (crossed eyes), exotropia (wall eyed), vertical deviations (hyper- or hypotropia). A customized surgical approach to correct the misalignments include weakening or strengthening procedures. Few latest modifications include the transposition, or transplantation of muscles to correct the ocular misalignment.[63] [64]

Figure 11- Intraoperative picture of an eye with exotropia undergoing medial rectus resection

Muscle strengthening procedures include resection, advancement, plication or muscle tucking.[65] Figure 11 shows intraoperative resection of medial rectus in a patient with exotropia.

Figure 12- Intraoperative picture of an eye with exotropia undergoing lateral rectus recession

Muscle weakening procedures include recession, myotomy, myectomy, dissinsertion or denervation.[66] Figure 12 shows intraoperative recession of lateral rectus muscle.

Horner Syndrome

Horner syndrome refers to the triad of symptoms resulting from damage to the sympathetic trunk in the neck. Horner syndrome can occur secondary to a tumor of the apex of the lung (Pancoast tumor), aortic aneurysm, or thyroid carcinoma.[67] The classical triad consists of the following:

Partial ptosis - Secondary to denervation of the superior tarsus muscle.

Miosis - Secondary to denervation of the dilator pupillae muscle.

Ipsilateral anhidrosis - Secondary to denervation of the sweat glands.

Additional Resources

References

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