Anterior cephalic neural crest is required for forebrain viability.
The prosencephalon, or embryonic forebrain, grows within a mesenchymal matrix of local paraxial mesoderm and of neural crest cells (NCC) derived from the posterior diencephalon and mesencephalon. Part of this NCC population forms the outer wall of capillaries within the prosencephalic leptomeninges and neuroepithelium itself. The surgical removal of NCC from the anterior head of chick embryos leads to massive cell death within the forebrain neuroepithelium during an interval that precedes its vascularization by at least 36 hours. During this critical period, a mesenchymal layer made up of intermingled mesodermal cells and NCC surround the neuroepithelium. This layer is not formed after anterior cephalic NCC ablation. The neuroepithelium then undergoes massive apoptosis. Cyclopia ensues after forebrain deterioration and absence of intervening frontonasal bud derivatives. The deleterious effect of ablation of the anterior NC cannot be interpreted as a deficit in vascularization because it takes place well before the time when blood vessels start to invade the neuroepithelium. Thus the mesenchymal layer itself exerts a trophic effect on the prosencephalic neuroepithelium. In an assay to rescue the operated phenotype, we found that the rhombencephalic but not the truncal NC can successfully replace the diencephalic and mesencephalic NC. Moreover, any region of the paraxial cephalic mesoderm can replace NCC in their dual function: in their early trophic effect and in providing pericytes to the forebrain meningeal blood vessels. The assumption of these roles by the cephalic neural crest may have been instrumental in the rostral expansion of the vertebrate forebrain over the course of evolution.
Etchevers
H C
HC
Institut d'Embryologie Cellulaire et Moléculaire du CNRS et du Collège de France, 94736 Nogent-sur-Marne Cedex, France. etchever@infobiogen.fr
Couly
G
G
Vincent
C
C
Le Douarin
N M
NM
D000818:Animals; D017209:Apoptosis; D016380:Brain Tissue Transplantation; D002642:Chick Embryo; D002678:Chimera; D003370:Coturnix; D004027:Diencephalon / Q000166:cytology / Q000196:embryology*; D004625:Embryo, Nonmammalian / Q000502:physiology*; D016332:Fetal Tissue Transplantation; D008636:Mesencephalon / Q000166:cytology / Q000196:embryology*; D008648:Mesoderm / Q000166:cytology / Q000502:physiology* / Q000637:transplantation; D009024:Morphogenesis; D009432:Neural Crest / Q000166:cytology / Q000502:physiology*; D016548:Prosencephalon / Q000166:cytology / Q000196:embryology*; D012249:Rhombencephalon / Q000166:cytology / Q000196:embryology / Q000637:transplantation; D014183:Transplantation, Heterologous