Prospective protochordate homologs of vertebrate midbrain and MHB, with some thoughts on MHB origins - PubMed (original) (raw)

Review

Prospective protochordate homologs of vertebrate midbrain and MHB, with some thoughts on MHB origins

Thurston C Lacalli. Int J Biol Sci. 2006.

Abstract

The MHB (midbrain-hindbrain boundary) is a key organizing center in the vertebrate brain characterized by highly conserved patterns of gene expression. The evidence for an MHB homolog in protochordates is equivocal, the "neck" region immediately caudal to the sensory vesicle in ascidian larvae being the best accepted candidate. It is argued here that similarities in expression patterns between the MHB and the ascidian neck region are more likely due to the latter being the principal source of neurons in the adult brain, and hence where all the genes involved in patterning the latter will necessarily be expressed. The contrast with amphioxus is exemplified by pax2/5/8, expressed in the neck region in ascidian larvae, but more caudally, along much of the nerve cord in amphioxus. The zone of expression in each case corresponds with that part of the nerve cord ultimately responsible for innervating the adult body, which suggests the spatially restricted MHB-like expression pattern in ascidians is secondarily reduced from a condition more like that in amphioxus. Patterns resembling those of the vertebrate MHB are nevertheless found elsewhere among metazoans. This suggests that, irrespective of its modern function, the MHB marks the site of an organizing center of considerable antiquity. Any explanation for how such a center became incorporated into the chordate brain must take account of the dorsoventral inversion chordates have experienced relative to other metazoans. Especially relevant here is a concept developed by Claus Nielsen, in which the brain is derived from a neural center located behind the ancestral mouth. While this is somewhat counterintuitive, it accords well with emerging molecular data.

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Conflict of interest statement

Conflict of interest: The author has declared that no conflict of interest exists.

Figures

Figure 1

Dorsal views of the larval nerve cords of (A) amphioxus and (B) Ciona, a representative ascidian, showing expression domains for the main CNS patterning genes. This is somewhat simplified, as the exact extent of the expression domains can vary with developmental stage, and the ascidian hox genes, in particular, are expressed in non-overlapping domains with some gaps.

Figure 2

Two alternatives for explaining the origin of a dorsally positioned brain in chordates, using the hemichordate embryo (A) as a starting point; indicates the mouth (m), anus (a), apical plate (orange), and the ancestral dorsal (a-dorsal) and ventral (a-ventral) surfaces; the light blue rectangle is the expression “hot zone” (hz) in which homologs of genes characteristic of the vertebrate MHB are expressed, typically in circumferential bands within ectoderm of the collar and anterior trunk. Older explanations of chordate origins, e.g. Garstang's hypothesis, retain an ancestral dorsoventral orientation (as in B). This allows the dorsal condensation of tissue that became the brain (dark blue) to form within the hot zone of MHB-like expression, co-opting the latter for neural patterning functions. With inversion (C, left side), the ancestral ventral surface becomes dorsal. In contrast with B, any brain-like condensation that forms on the new dorsal surface would necessarily then be post-oral in position, but it could still incorporate the MHB-like hot zone. Then, to generate the vertebrate condition (C, right side), with mouth and brain on opposing sides of the body, one needs to move the mouth over the front or side of the snout by differential growth of an expansion zone (ez) located somewhere forward of the brain.

References

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Prospective protochordate homologs of vertebrate midbrain and MHB, with some thoughts on MHB origins - PubMed (original) (raw)