Sensory system evolution at the origin of craniates

Abstract

The multiple events at the transition from non-craniate invertebrate ancestors to craniates included the gain and/or elaboration of migratory neural crest and neurogenic placodes. These tissues give rise to the peripherally located, bipolar neurons of all non-visual sensory systems. The brain was also elaborated at or about this same time. Were the peripheral and central events simultaneous or sequential? A serial transformation hypothesis postulates that paired eyes and an enlarged brain evolved before the elaboration of migratory neural crest placodal sensory systems. Circumstantial evidence for this scenario is derived from the independent occurrence of the combination of large, paired eyes plus a large, elaborated brain in at least three taxa (cephalochordates, arthropods and craniates) and partly from the exclusivity of the diencephalon for visual system-related distal sensory components versus the restricted distribution of migratory neural crest-placodal sensory systems to the remaining parts of the neuraxis. This scenario accounts for the similarity of all central sensory system pathways due to the primary establishment of descending visual pathways via the diencephalon and midbrain tectum to brainstem motor regions and the subsequent exploitation of the same central beachhead by the migratory neural crest-placodal systems as a template for their organization.