The earliest craniates achieved a unique condition among bilaterally symmet
rical animals: they possessed enlarged, elaborated brains with paired sense
organs and unique derivatives of neural crest and placodal tissues, includ
ing peripheral sensory ganglia, visceral arches, and head skeleton. The cra
niate sister taxon, cephalochordates, has rostral portions of the neuraxis
that are homologous to some of the major divisions of craniate brains. More
over, recent data indicate that many genes involved in patterning the nervo
us system are common to all bilaterally symmetrical animals and have been i
nherited from a common ancestor. Craniates, thus, have an "old" brain in a
new head, due to re-expression of these anciently acquired genes. The trans
ition to the craniate brain from a cephalochordate-like ancestral form may
have involved a mediolateral shift in expression of the genes that specify
nervous system development from various parts of the ectoderm. It is sugges
ted here that the transition was sequential. The first step involved the pr
esence of paired, lateral eyes, elaboration of the alar plate, and enhancem
ent of the descending visual pathway to brainstem motor centers. Subsequent
ly, this central visual pathway served as a template for the additional sen
sory systems that were elaborated and/or augmented with the "bloom" of migr
atory neural crest and placodes. This model accounts for the marked uniform
ity of pattern across central sensory pathways and for the lack of any neur
al crest-placode cranial nerve for either the diencephalon or mesencephalon
. Anat Rec (New Anat) 261:111-125, 2000. (C) 2000 Wiley-Liss, Inc.