The Postmigratory Alar Topography of Visceral Cranial Nerve Efferents Challenges the Classical Model of Hindbrain Columns

ABSTRACT The classic columnar model of cranial nerve central representation assumes that all motor and sensory hindbrain neurons develop within four radial migration domains, held to be separated by a sulcal alar–basal boundary (sulcus limitans). This essay reviews a number of developmental data that challenge these concepts. These results are interpreted within the framework of present day neuromeric conception of the brainstem (the prosomeric model). Advances in dorsoventral patterning of the spinal cord and hindbrain now show that there exist up to eight alar microzones and five basal microzones (molecularly and histogenetically distinct longitudinal progenitor domains). This reveals that the classic tetracolumnar model is excessively simplistic. There is both older and recent data revealing that the visceral efferent neurons of the cranial nerves (preganglionic and branchiomotor neurons) are generated next to the floor plate and later migrate dorsalwards before adopting their final topography in the mantle, contrary to the purely radial migration assumed in the classic model. Moreover, various results support the conclusion that at least the branchiomotor neurons end their migration and mature within the alar region of the mantle. Evidence on this point obtained in chick embryos is reviewed in detail, and novel evidence in mouse embryos is presented. Anat Rec, 302:485–504, 2019. © 2018 Wiley Periodicals, Inc.