Cerebral neurovascular embryology, anatomic variations, and congenital brain arteriovenous lesions

Correspondence to Dr Jesse M Klostranec, Department of Neuroradiology, Montreal Neurological Institute and Hospital, Montreal, Canada; [email protected]

Development of the cerebrovascular system is a complex yet reproducible process with numerous spatially and temporally coordinated events. Early anatomic descriptions made by Streeter¹ and Padget^{2 3} provide the foundational knowledge used today, with further insights from radiological correlates advanced by Lasjaunias^{4 5} and Raybaud.^6–8 Cerebral neurovascular development can be divided into two parts: vasculogenesis followed by angiogenesis. Herein, a timeline of events of typical development is reviewed and examined in order to explain the presentation of anatomic variants and congenital intracranial arteriovenous shunting lesions that are encountered in endovascular neuroradiological practice.

Vasculogenesis

The first endothelial tubes formed by a single layer of endothelium are constituted during vasculogenesis, which begins with the differentiation of multipotent mesodermal cells into endothelial cell (EC) precursor angioblasts.⁹ Some of these angioblasts migrate to the extra-embryonic yolk sac and cluster with hematopoietic stem cells to form hemangioblastic aggregates. These organize into blood islands, which are collections of hematopoietic stem cells surrounded by ECs, that coalesce to form a primitive vascular network.¹⁰ Other angioblasts remain intra-embryonic and organize into a long axial precursor vessel that undergoes arterial/venous segregation to form the paired dorsal aorta and cardinal vein.^{11 12} Connections exist between the primitive longitudinal vessels and the primordial capillary plexus, which extends intra-embryonally and cranially to invade the solid mesenchyme of the meninx primitiva surrounding the closed cranial neural pore at 4 weeks post-conception. Shortly after, endothelial channels proliferate to form the perineural vascular network of the meninx primitiva, which has superficial and deep layers. The superficial (dural) plexiform vascular network communicates with the paired dorsal aorta and cardinal veins, while the deep layer (pial) resembles a capillary network. Communicating segments exist between the layers (arachnoid) that later organize into the recognizable pattern of surface brain arteries and veins. The meninx primitiva overlying the forebrain (anterior neural plate) is of neural crest origin, giving rise to later anterior circulation autonomic control, while the remainder is from somitic mesoderm.⁸ The EC differentiation of angioblasts is regulated by tissue-derived factors, including vascular endothelial growth factor (VEGF), fibroblast growth factor 2, and bone morphogenic protein 4 (BMP4).⁹

Initially...