A Functional Perspective on the Embryology and Anatomy of the Cerebral Blood Supply

Abstract

The anatomy of the arterial system supplying blood to the brain can influence the development of arterial disease such as aneurysms, dolichoectasia and atherosclerosis. As the arteries supplying blood to the brain develop during embryogenesis, variation in their anatomy may occur and this variation may influence the development of arterial disease. Angiogenesis, which occurs mainly by sprouting of parent arteries, is the first stage at which variations can occur. At day 24 of embryological life, the internal carotid artery is the first artery to form and it provides all the blood required by the primitive brain. As the occipital region, brain stem and cerebellum enlarge; the internal carotid supply becomes insufficient, triggering the development of the posterior circulation. At this stage, the posterior circulation consists of a primitive mesh of arterial networks that originate from projection of penetrators from the distal carotid artery and more proximally from carotid-vertebrobasilar anastomoses. These anastomoses regress when the basilar artery and the vertebral arteries become independent from the internal carotid artery, but their persistence is not uncommon in adults (e.g., persistent trigeminal artery). Other common remnants of embryological development include fenestration or duplication (most commonly of the basilar artery), hypoplasia (typically of the posterior communicating artery) or agenesis (typically of the anterior communicating artery). Learning more about the hemodynamic consequence that these variants may have on the brain territories they supply may help understand better the underlying physiopathology of cerebral arterial remodeling and stroke in patients with these variants.

Keywords: Arterial variants; Cerebral arteries; Circle of willis; Embryology; Remodeling; Stroke.

Figure 1. This diagram describes the chronological development of cerebral brain arteries initially with the rise of the internal carotid artery and subsequently with the development of the posterior circulation. The brain differential growth rate is the pacemaker for the development of the cerebral circulatory system with a coupling of the tissue energy demand and the blood supply.

Figure 2. In early phases of development (A), the posterior circulation relies almost entirely from blood supply coming from the anterior circulation through carotid-vertebrobasilar anastomoses. Subsequently, as the posterior fossa structures and the occipital lobe growth, the posterior circulation becomes progressively independent from the anterior circulation with obliteration of the anterior-posterior anastomoses from caudal to rostral maintaining in the majority of adult only one connection between the distal basilar arteries with the carotid artery via the posterior communicating artery (B and C).

Figure 3. Arterial fenestration can occur in any of the arteries supplying the brain with blood. Fenestrations are defined as splitting of an arterial segment into two separate conducts with a common origin and common convergence prior to a true arterial bifurcation. (A) show an example of a fenestration in the first segment of the middle cerebral artery with convergence prior to the bifurcation into anterior and inferior division. (B) demonstrates the radiological appearance of a basilar artery fenestration, typically located in the most proximal part. (C) shows a cross-sectional view of a basilar artery fenestration (H&E, ×10 magnification) where it can be observed that the endothelium of both conduits are independent and they are separated by a septum of arterial wall.

Figure 4. An Azygous anterior cerebral artery is characterized by the fusion of the distal segments of the anterior cerebral artery that later bifurcates to supply the medial aspects of both hemispheres (A). In cross-sectional view of time of flight MRA, a single, typically large anterior cerebral artery can be observed (B).

Figure 5. The most common persistent embryonic carotid-vertebrobasilar anastomosis is the trigeminal artery (A). A persistent trigeminal artery consists of a connection between the intracranial internal carotid artery and the basilar artery, usually in the basilar midsegment or distally near the origin of the superior cerebellar arteries. A rarer variant is the persistence of the hypoglossal artery (B), which is distinguished from a persistent proatlantal artery because it enters the skull via the hypoglossal canal rather than the foramen magnum.