Temporal-Spatial Correlation between Angiogenesis and Corticogenesis in the Developing Chick Optic Tectum

Abstract

The developing chick optic tectum is a widely used model of corticogenesis and angiogenesis. Cell behaviors involved in corticogenesis and angiogenesis share several regulatory mechanisms. In this way the 3D organizations of both systems adapt to each other. The consensus about the temporally and spatially organized progression of the optic tectum corticogenesis contrasts with the discrepancies about the spatial organization of its vascular bed as a function of the time. In order to find out spatial and temporal correlations between corticogenesis and angiogenesis, several methodological approaches were applied to analyze the dynamic of angiogenesis in the developing chick optic tectum. The present paper shows that a typical sequence of developmental events characterizes the optic tectum angiogenesis. The first phase, formation of the primitive vascular bed, takes place during the early stages of the tectal corticogenesis along which the large efferent neurons appear and begin their early differentiation. The second phase, remodeling and elaboration of the definitive vascular bed, occurs during the increase in complexity associated to the elaboration of the local circuit networks. The present results show that, apart from the well-known influence of the dorsal-ventral and radial axes as reference systems for the spatial organization of optic tectum angiogenesis, the cephalic-caudal axis also exerts a significant asymmetric influence. The term cortico-angiogenesis to describe the entire process is justified by the fact that tight correlations are found between specific corticogenic and angiogenic events and they take place simultaneously at the same position along the cephalic-caudal and radial axes.

How Necessary is the Vasculature in the Life of Neural Stem and Progenitor Cells? Evidence from Evolution, Development and the Adult Nervous System

“…However, SEZ NSCs can influence the function of BVs, for example, the blood flow (Lacar et al, 2012b ), and oligodendrocyte progenitors can control angiogenesis through hypoxia-inducible factors (Yuen et al, 2014 ). These are in concert with evidence that embryonic cortical NSCs are important for the establishment of the developing vasculature (Gerhardt et al, 2004 ; Ma et al, 2013 ) and that in many cases vascularization tightly follows the maturation of the nervous system (Rodriguez Celin et al, 2015 ). Recently published work with human NSCs also showed that they provide the necessary juxtacrine and paracrine signals to drive human endothelial cells to form “vasculature-like structures” (Chou et al, 2014 ) and promote angiogenesis in the rodent brain (Hicks et al, 2013 ).…”

“…As soon as NSCs become specified the processes of self-renewal and expansion are initiated. Low levels of proliferation, adequate for the generation of single neurons and glia and for the construction of primitive neuronal networks and of the early neural tube, can occur in the absence of vascularization (Rodriguez Celin et al, 2015 ). The emergence of larger and more complicated nervous systems required higher levels of proliferation in embryonic neural stem and progenitor cells, and this was partly achieved through their diversification.…”

“…However, only limited evidence exists to suggest a contribution of the vasculature. The chicken germinal cortical zones remain largely a-vascular (Rodriguez Celin et al, 2015 ) and in mice, even though BVs appear at the time of expansion of the neuroepithelial cell pool, only transit amplifying neural progenitors proliferate in close proximity to them (Vasudevan et al, 2008 ; Javaherian and Kriegstein, 2009 ). Nevertheless, in both examples the long basal processes of radial glia remain in constant contact with BVs positioned deeper in the tissue (Vasudevan et al, 2008 ; Rodriguez Celin et al, 2015 ) a feature shared by adult NSCs (Mirzadeh et al, 2008 ).…”