Examination of the Annular Tendon (Annulus of Zinn) as a Common Origin of the Extraocular Rectus Muscles: 2. Embryological Basis of Extraocular Muscles Anomalies

Abstract

Purpose: Many reports have described anomalous connections of the superior rectus (SR) with other extraocular rectus muscles, in which additional heads of the other three rectus muscles likely provided the connections. We examined how these connections are established during fetal development.

Methods: We analyzed paraffin-embedded horizontal sections from 25 late-stage fetuses. Horizontal sections are best suited for understanding the mediolateral relationships of muscle origins.

Results: We confirmed a common tendinous origin of the lateral rectus (LR), inferior rectus (IR) and medial rectus (MR) muscles that was separated from the SR origin. Notably, eight fetuses (32%) had tendinous or muscular connections between the SR and other rectus muscles that had one of four morphologies: (a) a thin tendon from the SR to the common tendon of the three rectus muscles (2 fetuses), (b) a thin tendon to the LR (one fetus), (c) a thin tendon to the inferior rectus muscle origin (two fetuses), and (d) SR muscle fibers arising from an additional head of the LR (three fetuses).

Conclusions: The SR seemed to issue a thin tendon that passed along the inferior or lateral side of the oculomotor nerve. Conversely, the LR and inferior rectus muscle were likely to carry a supernumerary bundle that reached the SR. The accessory head of the medial rectus muscle showed a stable morphology in that it seemed to also provide an anomalous double head. However, the presence of an accessory head in the LR was rare. In contrast with our previously published diagram of the orbital apex, the accessory head of the medial rectus muscle passed along the lateral side of the superior oblique.

Figure 1.

Sagittal sections along the long axis of the orbit in a fetus with a CRL of 276 mm. (A) The most lateral site and (D) the most medial site. (A) The most posterior part of the LR. (B and C) The SR and LPS originate from the superior margin of the exit of the optic nerve (ON). (C, arrow) The inferomedial end of the SR origin. (D) The major and accessory heads of the MR (MRacc). All images were prepared at the same magnification (scale bar in A, 1 mm; ×1 objective). MXN, maxillary nerve; OM, orbital muscle (smooth muscle); OPA, ophthalmic artery.

Figure 2.

Horizontal sections in a fetus with a CRL of 272 mm (normal fetus). (A) The most superior site. (G) The most inferior site. (A and B) The origin of the SR surrounds the optic nerve exit. (B) The accessory head of the MR (MRacc) originates from the sphenoid near the SR origin. (D) It provides an independent muscle bundle. (E) The main head of the MR is distant from and inferior to the accessory head. (G) The MR and LR sandwich the IR in the common tendon. ABN, abducent nerve; ICA, internal carotid artery; OCN, oculomotor nerve; ON, optic nerve; OPA, ophthalmic artery; OPN, ophthalmic nerve.

Figure 3.

A thin tendon from the SR origin to the common tendon for the other three rectus muscles in a fetus with a CRL of 217 mm. (A) The most superior site and (H) the most inferior site. (B and C) The SR originates from the sphenoid (black star in each image). (F–H) The LR, IR, and MR have a common origin (open star in K). (G) The common origin. The IR is between the LR and MR. (C) The accessory head of the MR (arrows) is adjacent to the lateral aspect of the origin of the SO. (D and E) The accessory head is detached. (F) An inferior view shows that the major head of the MR originates from the bone. (E) A thin fibrous band (arrowhead) that is shown at a higher magnification in (J). Images (I and K) are near sections of (J). The fibrous band (surrounded by a green line) extends from the inferior end of the SR (I) to the common tendinous origin for three rectus muscles (open star in F–H and K). (A–H) At ×1 objective) and (I–K) at ×2 objective were prepared at the same magnification, respectively (scale bars in A and J = 1 mm). ABN, abducent nerve; FN, frontal nerve; OCN, oculomotor nerve; ON, optic nerve; OPA, ophthalmic artery; OPN, ophthalmic nerve; SPS, superior petrosal sinus.

Figure 4.

SR–LR connection consists of a thin tendon connecting the SR with the common tendon of the three rectus muscles in a fetus with a CRL of 264 mm. (A) The most superior site and (H) the most inferior site. (A) The SR originates from the sphenoid (black star). (H) The LR, IR, and MR have a common origin (open star). (A) An additional head of the LR originates from the lateral margin of the SR (arrows). (C, D, and E) The abducent and oculomotor nerves (ABN, OCN) pass between the major and additional heads of the LR. (C, D, and G) A thin tendon (arrowheads; surrounded by green line) extends from the inferolateral end of the SR origin (C), via the medial side of the OCN (D), to a superior margin of the common tendon (G). All images were prepared at the same magnification (scale bar in A, 1 mm; ×1 objective). CG, ciliary ganglion; ON, optic nerve; OPA, ophthalmic artery.

Figure 5.

An additional origin of the SR from a part of the LR in a fetus with a CRL of 282 mm (A–E) and a fetus with a CRL of 340 mm (F–J). (A and F) The most superior site of each fetus. (A, F, and I) The SR originates from the sphenoid (black star in each image). (E and J) The LR, IR, and MR have a common origin (open star in each image). (B and C) An inferolateral marginal part of the SR (surrounded by a green line) originates from the superior margin of the LR. Much inferiorly (1.0 mm), (E) shows that major parts of the LR and MR sandwich the IR origin. In contrast, (G) shows that an inferior part of the SR (surrounded by a green line) originates from an additional head of the LR (arrows). (H and I) The accessory head (LRacc) is detached from the bone. Much inferiorly (1.3 mm), (J) shows a major head of the LR. All images were prepared at the same magnification (scale bar in F, 1 mm; ×1 objective). ICA, internal carotid artery; MRacc, accessory head of the MR; OCN, oculomotor nerve; ON, optic nerve; OPA, ophthalmic artery.

Figure 6.

Extraocular muscle origins and their anomalous connections: a revision of our previous diagram (IOVS 2019; 60:4573). Anterior view of the right orbital apex. The SR originates from the lateral half of the optic canal opening, and the LR, IR, and MR muscles provide a common tendon originating from the medial wall of the orbital fissure. The MR has an accessory head (MRacc) that originates from the superomedial margin of the optic canal opening. In contrast to our previous diagram, the MRacc passes along the lateral side of the origin of the SO. Thin tendons likely connect the SR and the LR and/or IR (arrowheads). The connection is usually over the abducent and oculomotor nerve (ABN, OCN), but likely passes along the inferior side of the nerve. ON, optic nerve.