Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping

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 (n...

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Main Authors: Luis Puelles, Rafael Martínez-Marin, Pedro Melgarejo-Otalora, Abdelmalik Ayad, Antonios Valavanis, José Luis Ferran
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnana.2019.00059/full
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author Luis Puelles
Rafael Martínez-Marin
Pedro Melgarejo-Otalora
Abdelmalik Ayad
Antonios Valavanis
José Luis Ferran
author_facet Luis Puelles
Rafael Martínez-Marin
Pedro Melgarejo-Otalora
Abdelmalik Ayad
Antonios Valavanis
José Luis Ferran
author_sort Luis Puelles
collection DOAJ
description 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.
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spelling doaj.art-be8f09fe335f4750bb84079d52098bb02022-12-21T19:05:22ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292019-06-011310.3389/fnana.2019.00059448980Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric MappingLuis Puelles0Rafael Martínez-Marin1Pedro Melgarejo-Otalora2Abdelmalik Ayad3Antonios Valavanis4José Luis Ferran5Department of Human Anatomy, School of Medicine, University of Murcia and IMIB-Arrixaca Institute, Murcia, SpainDepartment of Human Anatomy, School of Medicine, University of Murcia and IMIB-Arrixaca Institute, Murcia, SpainDepartment of Human Anatomy, School of Medicine, University of Murcia and IMIB-Arrixaca Institute, Murcia, SpainDepartment of Human Anatomy, School of Medicine, University of Murcia and IMIB-Arrixaca Institute, Murcia, SpainDepartment of Neuroradiology, University Hospital of Zurich, Zurich, SwitzerlandDepartment of Human Anatomy, School of Medicine, University of Murcia and IMIB-Arrixaca Institute, Murcia, SpainThe 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.https://www.frontiersin.org/article/10.3389/fnana.2019.00059/fullbrain arteriespenetrating vesselsarterial topologyarterial branchingterminal fieldsmolecular profile
spellingShingle Luis Puelles
Rafael Martínez-Marin
Pedro Melgarejo-Otalora
Abdelmalik Ayad
Antonios Valavanis
José Luis Ferran
Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping
Frontiers in Neuroanatomy
brain arteries
penetrating vessels
arterial topology
arterial branching
terminal fields
molecular profile
title Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping
title_full Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping
title_fullStr Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping
title_full_unstemmed Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping
title_short Patterned Vascularization of Embryonic Mouse Forebrain, and Neuromeric Topology of Major Human Subarachnoidal Arterial Branches: A Prosomeric Mapping
title_sort patterned vascularization of embryonic mouse forebrain and neuromeric topology of major human subarachnoidal arterial branches a prosomeric mapping
topic brain arteries
penetrating vessels
arterial topology
arterial branching
terminal fields
molecular profile
url https://www.frontiersin.org/article/10.3389/fnana.2019.00059/full
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