Human Ophthalmic and Ocular branches

The Primitive Maxillary Artery

The ocular vascular supply in 4- to 5-mm embryos derives from the cranial division of the ICA, which surrounds the caudal aspect of the optic vesicle and ends in the olfactory region. The primitive MA originates from the future cavernous ICA, and provides a lateral branch that transiently supplies the optic vesicle and a medial branch that aims towards Rathke’s pouch (the future hypophysis). The lateral branch, well visible in 4-mm embryos, starts regressing at the 5- to 6-mm stage. Its remnant will form the inferolateral trunk and its branches, including the deep recurrent OA (De La Torre & Netsky, 1960; Padget, 1948), which enters the orbit through the medial aspect of the superior orbital fissure (SOF) (Gailloud, Gregg, & Ruiz, 2009). The medial branch will become the inferior hypophyseal artery, a component of the meningohypophyseal trunk (Padget, 1948).

Potential Contributions from the Primitive Olfactory Artery

A small vessel sprouting from the ICA at the level of origin of the posterior communicating artery (PComA) (or caudal division of the ICA) represents the future primitive dorsal OA(Padget, 1948). In 5- to 6-mm embryos, it courses over the dorsal margin of the optic vesicle to reach the site of the future lens (Padget, 1948). Both the primitive olfactory artery and the primitive dorsal OA arise from the ICA distally to the origin of the primitive MA.

In rats, the primitive olfactory artery provides a branch that connects to the regressing primitive MA and contributes to a capillary network surrounding the optic stalk; from this branch derive the small chiasmatic rami of the adult anterior cerebral artery (ACA). Moffat named this vessel the recurrent primitive olfactory artery and speculated that it may also be present in humans (Moffat, 1967; D. B. Moffat, 1961). This periocular capillary network is visible in 6- to 9-mm embryos in rats (D. Moffat, 1961), 12-somite embryos in chickens (Sabin, 1917), and 4- to 9-mm embryos in man (Mann, 1964; Padget, 1948). Although Padget did not indicate a direct connection between the periocular plexus and the primitive olfactory artery, she mentioned that several small branches from the cranial division of the ICA supply the cranial part of the optic vesicle prior to the appearance of the primitive ventral OA. She also noted that the arteries surrounding the optic vesicle near the primitive olfactory artery had a plexiform configuration until embryos reach a length of 12 to 14 millimeters. Through these small branches (Padget’s figure 3a and 3b (Padget, 1948)), the primitive olfactory artery connects with the other primitive arteries supplying the periocular plexus. These connections are involved in the formation of variants such as an anomalous OA origin from the ACA or an infraoptic ACA (Gregg et al., 2015)(Graphic Embryo Figure below).

Addition of Primitive Ventral OA

In 7- to 12-mm embryos , the primitive ventral OA emerges from the ICA at the level of the AChoA and courses to the cranioventral portion of the optic cup, supplementing the primitive dorsal OA supply. The primitive olfactory artery also provides a new medial twig that will become the ACA, while the optic (lateral) branch of the primitive MA regresses (Padget, 1948).

In 12- to14-mm embryos, the primitive dorsal OA provides the temporociliary and hyaloid arteries (a prominent branch in the zebrafish), while the primitive ventral OA gives the future common nasal ciliary artery. By the time the embryo reaches 14-mm, the midline fusion of the ACAs arising from the primitive olfactory artery forms the anterior communicating artery (AComA). The stapedial artery, a branch of the hyoid artery is also visible; the stapedial artery will annex the distal branches of the ventral pharyngeal artery, which will become the maxillomandibular division of the external carotid artery (Padget, 1948).

Transfer of Ophthalmic Branches

It is only near the end of the 16- to 18-mm stage that the adult OA origin can be detected, proximally to the regressing primitive ventral and dorsal OAs, and distally to the remnants of the primitive MA. The stem of the adult OA annexes the branches of the primitive ventral and dorsal OAs through an anastomotic process that is not fully elucidated. The stalks of the two primitive OAs soon involute while the olfactory artery begins to regress. The dorsal (orbital branch) and ventral (maxillary and mandibular branches) divisions of the stapedial artery are clearly discernable; the dorsal division supplies the orbital component of the future OA through the primitive orbital artery (Padget, 1948).

The Arterial Loop and the Stapedial Artery

In 20- to 24-mm embryos, the medial branch of the primitive MA has developed into the inferior hypophyseal artery, and the primitive olfactory artery has regressed into a small ACA branch. The MA (embryologically distinct from the primitive MA) connects with the ventral division of the stapedial artery; the latter then separates completely from the hyoid artery to become a branch of the MA, thus forming the adult external carotid artery. The primitive orbital artery, stemming from the stapedial artery, establishes an intraorbital anastomosis with the OA, thus forming a complete arterial loop around the optic nerve (Padget, 1948).

Adult Branching Pattern

In the 40-mm embryo, the OA has taken over the primitive orbital artery and its supply to non-neural orbital structures. The supraorbital division of the stapedial artery distal to its anastomosis with the MA is now the adult middle meningeal artery (Padget, 1948). The cranioventral segment the arterial ring surrounding the optic nerve regresses, leaving the typical optic loop of the OA (Padget, 1948). With the exception of the hyaloid artery, which involutes during the fetal period, the OA has reached its adult configuration.

Graphic Summary of Primitive Artery Involvement in OA Anomalies

Diagrammatic summary of the involvement of primitive arteries (primitive MA, recurrent primitive olfactory artery, primitive dorsal OA, primitive ventral OA and stapedial artery) in the development of the normal adult OA from a lateral view, left side. Images A-D depict normal development while image E-L depict adult anomalies that each primitive artery may contribute to through variations in development.