The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain

TLDR

Neural crest cells (NCCs) give rise to most head connective tissues and, through their developmental plasticity, have driven vertebrate forebrain growth during evolution. NCCs detach from posterior diencephalon, mesencephalon, and rhombencephalon folds, migrate ventrally between ectoderm and neuroepithelium, and encounter mesoderm‑derived endothelial precursors. In the avian embryo, NCC‑derived pericytes and smooth muscle cells form a vascular tree that ensheaths all aortic arch–derived vessels, supplies forebrain meninges, retinal choroids, and facial structures, and establishes distinct diencephalic/mesencephalic versus mesodermal pericyte territories that meet at specific anastomoses such as the circle of Willis.

Abstract

ABSTRACT Most connective tissues in the head develop from neural crest cells (NCCs), an embryonic cell population present only in vertebrates. We show that NCC-derived pericytes and smooth muscle cells are distributed in a sharply circumscribed sector of the vasculature of the avian embryo. As NCCs detach from the neural folds that correspond to the future posterior diencephalon, mesencephalon and rhombencephalon, they migrate between the ectoderm and the neuroepithelium into the anterior/ventral head, encountering mesoderm-derived endothelial precursors. Together, these two cell populations build a vascular tree rooted at the departure of the aorta from the heart and ramified into the capillary plexi that irrigate the forebrain meninges, retinal choroids and all facial structures, before returning to the heart. NCCs ensheath each aortic arch-derived vessel, providing every component except the endothelial cells. Within the meninges, capillaries with pericytes of diencephalic and mesencephalic neural fold origin supply the forebrain, while capillaries with pericytes of mesodermal origin supply the rest of the central nervous system, in a mutually exclusive manner. The two types of head vasculature contact at a few defined points, including the anastomotic vessels of the circle of Willis, immediately ventral to the forebrain/midbrain boundary. Over the course of evolution, the vertebrate subphylum may have exploited the exceptionally broad range of developmental potentialities and the plasticity of NCCs in head remodelling that resulted in the growth of the forebrain.