Abstract
The prosomeric brain model contemplates progressive regionalization of the central nervous system (CNS) from a molecular and morphological ontogenetic perspective. It defines the forebrain axis relative to the notochord, and contemplates intersecting longitudinal (zonal, columnar) and transversal (neuromeric) patterning mechanisms. A checkboard pattern of histogenetic units of the neural wall results, where each unit is differentially fated by an unique profile of active genes. These natural neural units later expand their radial dimension during neurogenesis, histogenesis, and correlative differential morphogenesis. This fundamental topologic framework is shared by all vertebrates, as a Bauplan, each lineage varying in some subtle aspects. So far the prosomeric model has been applied only to neural structures, but we attempt here a prosomeric analysis of the hypothesis that major vessels invade the brain wall in patterns that are congruent with its intrinsic natural developmental units, as postulated in the prosomeric model. Anatomic and embryologic studies of brain blood vessels have classically recorded a conserved pattern of branches (thus the conventional terminology), and clinical experience has discovered a standard topography of many brain arterial terminal fields. Such results were described under assumptions of the columnar model of the forebrain, prevalent during the last century, but this is found insufficient in depth and explanatory power in the modern molecular scenario. We have thus explored the possibility that brain vascularization in rodents and humans may relate systematically to genoarchitectonic forebrain subdivisions contemplated in the prosomeric model. Specifically, we examined first whether early vascular invasion of some molecularly characterized prosomeric domains shows heterochrony. We indeed found a heterochronic pattern of vascular invasion that distinguishes between adjacent brain areas with differential molecular profiles. We next mapped topologically on the prosomeric model the major arterial branches serving the human brain. The results of this approach bear on the possibility of a developmentally-based modern arterial terminology.
Highlights
Once development of the closed neural tube progresses beyond patterning, regionalization and initial surface growth, the processes of neurogenesis and differentiation commence in an heterochronic pattern, showing gradual construction of a heterogeneous mantle layer
According to a number of studies, genes involved in the promotion of an arterial identity include EphrinB2a, Shh, Ihh, Notch1/4, Jag1/2, Dll4, and Np1; a venous identity obeys instead to the activity of COUP-TFII, Np2, EphB4 and Vegfr3 (Flt4)
We elected Vegfr2 (Flk1/Kdr) for our study because it is highly expressed from the beginning of vascularization of the central nervous system (CNS) and during early stages of development in the entire vascular network of the brain
Summary
Once development of the closed neural tube progresses beyond patterning, regionalization and initial surface growth, the processes of neurogenesis and differentiation commence in an heterochronic pattern, showing gradual construction of a heterogeneous mantle layer. Intersecting anteroposterior (AP) and dorsoventral (DV) patterning effects taking place during early brain regionalization specify primary cerebral compartments, as well as secondary subdivisions These display a checkboard pattern of orthogonal boundaries (AP patterning produces transverse segments or neuromeres, separated by interneuromeric boundaries, whereas DV patterning produces longitudinal zones). This establishes already at early neuroepithelial stages a checkered fundamental plan of construction of the neural tube wall (a brain Bauplan), which is apparently shared among all vertebrates (Nieuwenhuys and Puelles, 2016). Note the historically earlier columnar model (Herrick, 1910; Kuhlenbeck, 1973; Swanson, 2012) attended essentially to longitudinal subdivisions—e.g., ‘‘brain columns,’’—but disregarded transversal units other than the major brain vesicles. This feature, jointly with an arbitrarily-defined forebrain axis, eventually caused its present insufficiency as a brain model
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