Introduction

Extraocular muscles (EOMs) are crucial for ocular movement. The superior and inferior obliques and the 4 recti work together to move the eyes in various directions (see Image. Oculomotor Nerve Pathway). The inferior oblique is almost entirely muscular, unlike the superior oblique, which is both muscular and tendinous. The inferior oblique is primarily responsible for the eye's external rotation. The muscle's secondary and tertiary actions are elevation and abduction, respectively.[1]

Inferior oblique overaction is a common cause of vertical strabismus and can be seen in conditions like infantile esotropia. Inferior oblique dysfunction can affect ocular torsion, leading to diplopia. Surgery on the inferior oblique is a common procedure to correct strabismus. Understanding the inferior oblique's anatomy and function is essential for diagnosing and managing various ocular conditions, particularly those involving eye movement and alignment.

Structure and Function

The inferior oblique is the shortest of all the eye muscles, measuring approximately 37 mm long. Unlike all other EOMs, the inferior oblique does not originate from the annulus of Zinn or the common tendinous ring. Instead, this EOM arises from the orbital floor lateral to the nasolacrimal groove.[2]

The slender muscle continues from its origin, running along the inferior surface of the eye, passing between the floor of the orbit and the inferior rectus to eventually insert on the eye's posterior inferolateral surface. The inferior oblique's width at the insertion point varies, averaging 9 mm. The inferior oblique has 2 surfaces: the superior ocular and the inferior orbital surfaces.

The muscle is defined by its anterior and posterior border at the orbital groove. The inferior oblique tendon inserts in the sclera under the lateral rectus. The anterior border is about 10 mm from the lateral rectus insertion point, while the posterior border is 1 to 2 mm in front of the macula. The muscle itself is not only shorter than other EOMs, but its tendon, which measures 1 to 2 mm, is also shorter than its counterparts.[3]

The inferior oblique is responsible for extorsion, elevation, and abduction. The superior and inferior obliques are the only EOMs capable of depressing and elevating the adducted eye, respectively, due to their unique anatomical paths.

Embryology

The inferior oblique and the superior, inferior, and medial recti are derived from the prechordal mesoderm. The inferior oblique's embryological origin is distinct from the other EOMs, which develop from the mesodermal cells in the prechordal plate and cranial mesoderm in conjunction with migrating neural crest cells. Specifically, the inferior oblique arises from the mesenchymal tissue at the anterior inferomedial part of the orbit near the maxila's orbital surface.[4]

Around 7 to 8 weeks of gestation, the inferior oblique begins to form from a dense mesenchymal condensation near the infraorbital nerve. Unlike the extraocular rectus muscles, which have a common origin at the annulus of Zinn, the inferior oblique originates from a different region and lacks cartilaginous tissue at its origin. By 12 to 15 weeks of gestation, the inferior oblique's muscular origin appears, attaching to dense fibrous tissue and eventually merging with the posterior part of the sclera.[5]

The embryological origin of the inferior oblique involves the coordinated action of multiple genes and signaling pathways that regulate the migration, proliferation, and differentiation of myogenic precursor cells from the cranial mesoderm.[6] The paired box gene 3 (Pax3) has been demonstrated to be important in the early development of the EOMs. Pax3 is crucial for the migration and proliferation of myogenic precursor cells from the cranial mesoderm.

In addition, homeobox genes such as Lhx2 and Pitx2 have been explored in the specification and patterning of the EOMs. These genes influence the inferior oblique, in particular, during the morphogenesis of the ocular region. The interaction between these genes and the downstream signaling pathways, including Wnt and bone morphogenetic protein (BMP) pathways, orchestrates the formation and proper positioning of the inferior oblique.[7]

Blood Supply and Lymphatics

The inferior oblique is perfused by a medial muscular branch of the ophthalmic artery and the infraorbital artery. The ophthalmic artery, a branch of the internal carotid artery, supplies most of the EOMs. The infraorbital artery, a branch of the maxillary artery, provides additional blood supply.[8] The inferior orbital vein drains the muscle.

Lymph from the inferior oblique follows the general lymphatic flow within the ocular region. Lymph from the orbit and periorbital structures, including the EOMs, initially flows toward the preauricular (parotid) and submandibular nodes before draining into the deep cervical lymph nodes.[9]

Nerves

The inferior division of the oculomotor nerve (cranial nerve III) runs inferolaterally along the inferior rectus to innervate the inferior oblique. The nerve is approximately 27 mm long, running from the orbital apex to the inferior oblique. The nerve to the inferior oblique is the longest branch of the inferior division of the oculomotor nerve. The nerve enters the muscle through its orbital surface. The nerve to the inferior oblique has been measured to be approximately 1.04 mm on the right and 1.07 mm on the left.

Interestingly, the nerve accompanies an artery, vein, and fibrous tissue component. The terminal 8 mm of the nerve is encased in this fibrous component. Hence, innervation of the inferior oblique occurs through a neurofibrovascular bundle, a unique feature of this EOM. This feature is of particular anatomical importance in anterior transposition surgeries. The neurofibrovascular bundle serves as the origin for the inferior oblique and provides an ancillary origin for its posterior fibers after transposition.[10]

The oculomotor nerve's inferior division also carries parasympathetic fibers to the ciliary ganglion near the optic nerve. These fibers innervate the sphincter pupillae and ciliary muscles.[11]

Muscles

EOMs are specialized skeletal muscles. EOMs possess both slow tonic- and saccadic-type muscle fibers. Unlike other muscles, EOMs have a large nerve-fiber-to-skeletal-muscle-fiber ratio of 1:3 to 1:5. In contrast, other skeletal muscles typically only have 1:50 to 1:125.[12]

Physiologic Variants

Though rare, anatomical variations of EOMs include the absence or duplication of muscles and innervation or insertion anomalies. These variations can cause extraocular movement dysfunction and may require surgical evaluation. Congenital aplasia or hypoplasia of the inferior oblique can result from disruptions in the normal developmental processes.[13]

The inferior oblique exhibits anatomical variations more frequently than other EOMs. These variations include the following:

• Multiple muscle bellies: The inferior oblique may present with 2 or more muscle bellies, as documented by different studies.[14][15][16]
• Muscular bridge: Another notable variation is the presence of a muscular bridge between the inferior oblique and inferior rectus.[17]
• Obliquus accessorius inferior: This accessory muscle originates from the orbital apex and inserts near the inferior rectus insertion. Although functionally similar to the inferior rectus, this muscle is distinct in its anatomical origin and insertion.
• Insertion variations: While the inferior oblique typically has a close relationship with the inferior rectus at its insertion, case reports document instances of the inferior oblique inserting near or adjacent to the lateral rectus. These unusual insertion sites can affect the muscle's mechanical action on the eye.

Surgical Considerations

The inferior oblique externally rotates, elevates, and abducts the eye. Any injury to this muscle may result in strabismus, a significant misalignment of the eyes. While patients may develop compensatory mechanisms for this movement disability, surgical intervention is often required for cosmetic and functional correction.

Inferior oblique overaction exists in 70% of patients with esotropia and 30% of patients with exotropia. This condition is characterized by disproportionate elevation of the eye during adduction. Inferior oblique overaction can be categorized into primary and secondary types. Primary inferior oblique overaction is congenital or of unclear etiology, often associated with bilateral overaction leading to infantile esotropia.[18] Secondary overaction typically occurs unilaterally and results from a defect in the superior oblique, which normally controls abduction, internal rotation, and eye depression. Superior oblique paralysis leaves the inferior oblique unopposed, causing excessive elevation.

Surgical correction methods for inferior oblique overaction include disinsertion, extirpation and denervation, recession, myectomy, and anterior transposition of the muscle. The anterior transposition technique is particularly effective for patients with inferior oblique overaction with dissociated vertical deviation.[19][20] This procedure converts the inferior oblique into a depressor, significantly reducing its normal action and limiting upward gaze to 30° to 35°.[21]

A myectomy is performed in patients with vertical hypertropia without dissociated vertical deviation. This procedure is both prophylactic and cosmetic, as patients with inferior oblique overaction have an increased risk of developing retinal holes and tears due to the muscle's traction on the thin sclera. The inferior oblique is often transected during enucleation to provide traction to the globe (see Image. Eye Enucleation and the Inferior Oblique).

Clinical Significance

Inferior oblique dysfunction is often discovered by parents and pediatricians during infancy, allowing an early referral to an ophthalmologist. In the early stages, the condition is treated by patching the dominant eye, which forces the abnormal eye to compensate and strengthen. Surgical intervention is recommended if patching fails.[22]

Other Issues

The inferior oblique is susceptible to injury during lower blepharoplasty resection. Patients with postsurgical inferior oblique injury typically present with symptoms ranging from transient diplopia to permanent strabismus. Diplopia resulting from an inferior oblique injury usually manifests with a distorted visual image with an upward lateral gaze. Patients often unknowingly compensate by tilting their heads or lifting their chins.[23]