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.

Association between the developing sphenoid and adult morphology: A study using sagittal sections of the skull base from human embryos and fetuses

“…The results of this study suggested differences in the origins of the extraocular muscles, with the superior rectus and obliquus superior originating from the OS‐sup and the inferior and medial recti from the OSpost. This result was consistent with our previous studies in late‐term fetuses and adults (Kim et al, 2020; Naito et al, 2019), which showed that the superior obliquus, levator palpebrae superioris, and superior rectus originated from the upper margin of the optic canal, whereas the other three recti arose from the medial wall of the fetal large orbital fissure (i.e., the OSpost). After birth, these origins may be connected or bundled by the future tendinous annulus.…”

“…Paraffin‐embedded sagittal sections were obtained from 25 embryos and fetuses of approximate GA 6–34 weeks and CRL 12–295 mm. Because sagittal sections show topographical anatomy better than horizontal sections, sagittal sections of the sphenoid have been used to assess the anatomy of the developing cavernous sinus (Sato et al, 2020) and extraocular rectus muscles (Kim et al, 2020; Naito et al, 2019). The specimens were categorized into four groups by age and size, with Group 1 consisting of four embryos of GA 6 weeks and CRL 12–15 mm, Group 2 of six early fetuses of GA 7–8 weeks and CRL 24–35 mm, Group 3 of eight midterm fetuses of GA 12–15 weeks and CRL 71–115 mm, and Group 4 of seven late‐term fetuses of GA 25–34 weeks and CRL 200–295 mm.…”

“…Most photographs were taken with a Nikon Eclipse 80, whereas photographs at ultra‐low magnification (objective lens less than ×1) were obtained using a high‐grade flat scanner with translucent illumination (Epson scanner GTX970). In addition to the sagittal sections from 25 specimens, structures requiring identification were assessed by reexamining photographs of horizontally or frontally sectioned sphenoids taken for previous studies (Cho et al, 2010, 2013; Honkura et al, 2017; Jin et al, 2011; Katori, Kawamoto, et al, 2013; Katori, Kawase, et al, 2013; Kim et al, 2020; Kiyokawa et al, 2012; Osanai et al, 2011; 2011, 2017; Yamamoto et al, 2017, 2018). In these previous specimens, horizontal and frontal sections from 25 late‐term fetuses (GA 28–40 weeks and CRL 217–340 mm; Kim et al, 2020) were especially useful for detailed understanding of topographical anatomy.…”

“…In addition to the sagittal sections from 25 specimens, structures requiring identification were assessed by reexamining photographs of horizontally or frontally sectioned sphenoids taken for previous studies (Cho et al, 2010, 2013; Honkura et al, 2017; Jin et al, 2011; Katori, Kawamoto, et al, 2013; Katori, Kawase, et al, 2013; Kim et al, 2020; Kiyokawa et al, 2012; Osanai et al, 2011; 2011, 2017; Yamamoto et al, 2017, 2018). In these previous specimens, horizontal and frontal sections from 25 late‐term fetuses (GA 28–40 weeks and CRL 217–340 mm; Kim et al, 2020) were especially useful for detailed understanding of topographical anatomy. Therefore, the observations will be added in the final subsection of the results with figure demonstration of two of the 25 specimens.…”

Optic nerve‐associated connective tissue structures revisited: A histological study using human fetuses and adult cadavers

“…The dural sheath has recently been recognized to be bilaminar from a biomechanical point of view (Shin et al, 2020), but no studies have demonstrated that both the meningeal and periosteal laminae of the dura continue to the dural sheath of the optic nerve. Our recent studies on the bony origin of the extraocular rectus muscles (Kim et al, 2020;Naito et al, 2019) demonstrated that the periosteum of the sphenoid is continuous with the dural sheath of the intraorbital optic nerve.…”