The evolution of nervous system centralization

Abstract

It is yet unknown when and in what form the central nervous system in Bilateria first came into place and how it further evolved in the different bilaterian phyla. To find out, a series of recent molecular studies have compared neurodevelopment in slow-evolving deuterostome and protostome invertebrates, such as the enteropneust hemichordate Saccoglossus and the polychaete annelid Platynereis. These studies focus on the spatially different activation and, when accessible, function of genes that set up the molecular anatomy of the neuroectoderm and specify neuron types that emerge from distinct molecular coordinates. Complex similarities are detected, which reveal aspects of neurodevelopment that most likely occurred already in a similar manner in the last common ancestor of the bilaterians, Urbilateria. This way, different aspects of the molecular architecture of the urbilaterian nervous system are reconstructed and yield insight into the degree of centralization that was in place in the bilaterian ancestors.

Figure 1

Different degrees of centralization in metazoan brains. (a) Centralized nervous system of an oligochaete worm. (b) Nerve net of a cnidarian polyp representing a typical non-centralized nervous system. Schematized drawings modified with permission from Bullock & Horridge (1965).

Figure 2

Comparison of mediolateral neurogenic columns across Bilateria. Expression of nk2.2/nk2.1 (orange; Shimamura et al. 1995), Nk6 (yellow; Rubenstein et al. 1998), Pax6 (violet; Mastick et al. 1997; Urbach & Technau 2003a,b), gooseberry/Pax3/7 (green; Matsunaga et al. 2001; Puelles et al. 2003) and msh/Msx (blue; Shimeld et al. 1996) orthologues in the neuroectoderm of Drosophila, Platynereis and mouse at pre-differentiation stages. The Drosophila and Platynereis schematics represent ventral views, and the mouse one is a dorsal view with the neural tube unfolded into a neural plate for better comparison. Neurogenic columns are demarcated by expression boundaries and represent cells with a unique combination of transcription factors. All expression patterns are symmetrical but are shown on only one side for clarity.

Figure 3

Conserved neural cell types in annelid and vertebrate. The neuron types emerging from homologous regions in the molecular coordinate systems in annelid and vertebrate and expressing orthologous effector genes are marked with the same colour. Homologous cell types include the molecular clock cells positive for bmal (dark green), ciliary photoreceptors positive for c-opsin and rx (white), rhabdomeric photoreceptors positive for r-opsin, atonal and pax6 (yellow), vasotocinergic cells positive for nk2.1, rx and otp (orange), serotonergic cells positive for nk2.1/nk2.2 (red), cholinergic motor neurons positive for pax6, nk6 and hb9 (violet), interneurons positive for dbx (pink), as well as trunk sensory cells positive for atonal and msh (light blue).