Interactions and fates of avian craniofacial mesenchyme

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Abstract
Craniofacial mesenchyme is composed of three mesodermal populations – prechordal plate, lateral mesoderm and paraxial mesoderm, which includes the segmented occipital somites and the incompletely segmented somitomeres – and the neural crest. This paper outlines the fates of each of these, as determined using quail–chick chimaeras, and presents similarities and differences between these cephalic populations and their counterparts in the trunk. Prechordal and paraxial mesodermal populations are the sources of all voluntary muscles of the head. The latter also provides most of the connective precursors of the calvaria, occipital, otic–parietal and basisphenoid tissues. Lateral mesoderm is the source of peripharyngeal connective tissues; the most rostral skeletal tissues it forms are the laryngeal and tracheal cartilages. When migrating neural crest cells encounter segmented paraxial mesoderm (occipital and trunk somites), most move into the region between the dermamyotome and sclerotome in the cranial half of each somite. In contrast, most cephalic crest cells migrate superficial to somitomeres. There is, however, a small subpopulation of the head crest that invades somitomeric mesoderm. These cells subsequently segregate presumptive myogenic precursors of visceral arch voluntary muscles from underlying mesenchyme. In the neurula-stage avian embryo, all paraxial and lateral mesodermal populations contain precursors of vascular endothelial cells, which can be detected in chimaeric embryos using anti-quail endothelial antibodies. Some of these angioblasts differentiate in situ, contributing directly to pre-existing vessels or forming isolated, nonpatent, cords that subsequently vesiculate and fuse with nearby vessels. Many angioblasts migrate in all directions, invading embryonic mesenchymal and epithelial tissues and participating in new blood vessel formation in distant sites. The interactions leading to proper spatial patterning of craniofacial skeletal, muscular, vascular and peripheral neural tissues has been studied by performing heterotopic transplants of each of these mesodermal and neural crest populations. The results consistently indicate that connective tissue precursors, regardless of their origin, contain spatial information used by the precursors of muscles and blood vessels and by outgrowing peripheral nerves. Some of these connective tissue precursors (e.g. the neural crest, paraxial mesoderm) acquire their spatial programming while in association with the central nervous system or developing sensory epithelia (e.g. otic, optic, nasal epithelia).