Abstract
Mesenchephalic and rhombencephalic neural crest cells generate the craniofacial skeleton, special sensory organs, and subsets of cranial sensory receptor neurons. They do so while preserving the anterior-posterior (A-P) identity of their neural tube origins. This organizational principle is paralleled by central nervous system circuits that receive and process information from facial structures whose A-P identity is in register with that in the brain. Prior to morphogenesis of the face and its circuits, however, neural crest cells act as “inductive ambassadors” from distinct regions of the neural tube to induce differentiation of target craniofacial domains and establish an initial interface between the brain and face. At every site of bilateral, non-axial secondary induction, neural crest constitutes all or some of the mesenchymal compartment for non-axial mesenchymal/epithelial (M/E) interactions. Thus, for epithelial domains in the craniofacial primordia, aortic arches, limbs, the spinal cord, and the forebrain (Fb), neural crest-derived mesenchymal cells establish local sources of inductive signaling molecules that drive morphogenesis and cellular differentiation. This common mechanism for building brains, faces, limbs, and hearts, A-P axis specified, neural crest-mediated M/E induction, coordinates differentiation of distal structures, peripheral neurons that provide their sensory or autonomic innervation in some cases, and central neural circuits that regulate their behavioral functions. The essential role of this neural crest-mediated mechanism identifies it as a prime target for pathogenesis in a broad range of neurodevelopmental disorders. Thus, the face and the brain “predict” one another, and this mutual developmental relationship provides a key target for disruption by developmental pathology.
Highlights
60 years ago, Demyer et al (1964) published a description of a series of cases with varying degrees of craniofacial malformations: from near cyclopia in still born fetuses to two patients, described in detail, with mild, but detectable, craniofacial anomalies
Subsets of neural crest cells that migrate to distinct peripheral sites of morphogenesis, including the facial primorida, bring with them a record of A-P neural tube position and presumably share aspects of molecular identity with neural progenitor cells that remain behind
Observations in WT and mutant embryos define the central role of neural crest in local M/E interactions, especially those mediated by retinoic acid (RA) signals provided by neural crest mesenchymal cells, for the coordination of morphogenesis and subsequent connectivity of the olfactory system during early stages of Fb development
Summary
60 years ago, Demyer et al (1964) published a description of a series of cases with varying degrees of craniofacial malformations: from near cyclopia in still born fetuses to two patients, described in detail, with mild, but detectable, craniofacial anomalies. If the face predicts the brain, it is essential to define the nature of the prediction This relationship reflects the central role of interactions between the craniofacial primordia, cranial placodes, and the rhombencephalic and mesencephalic neural crests, which provides a “mirror” representation of the axial organization of the neural tube to distal sites of secondary induction and differentiation: the facial skeleton and cartilage, key sensory structures, like the nose, eyes, ears, and cranial ganglia, and their targets in the central nervous system. Our work using transgenic reporters and molecular markers for neural crest have reinforced the likely presence of neural crest in the limb bud mesenchyme (Maynard et al, 2002; Bhasin et al, 2003; Meechan et al, 2006; Rawson et al, 2010) prior to the ingression of nerves and
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