To investigate the embryonic development of the central nervous system of the lamprey Lampetra fluviatilis, we have isolated and analysed the expression patterns of members of the LIM-homeodomain, Pax, Hedgehog and Nkx2.1 families. Using degenerate RT-PCR, single representatives of Lhx1/Lhx5, Lhx2/Lhx9, Pax3/Pax7 and Hedgehog families could be isolated in L. fluviatilis. Expression analysis revealed that the lamprey forebrain presents a clear neuromeric pattern. We describe the existence of 4 embryonic diencephalic prosomeres whose boundaries can be identified by the combined and relative expressions of LfPax37, LfLhx15 and LfLhx29. This suggests that the embryonic lamprey and gnathostome forebrain are patterned in a highly similar manner. Moreover, analysis of the LfHh gene, which is expressed in the hypothalamus, zona limitans intrathalamica and floor plate, reveals the possible molecular origin of this neuromeric brain pattern. By contrast, LfHh and LfNkx2.1 expressions suggest major differences in patterning mechanisms of the ventral telencephalon when compared to gnathostomes. In summary, our findings highlight a neuromeric organisation of the embryonic agnathan forebrain and point to the possible origin of this organisation, which is thus a truly vertebrate character. They also suggest that Hh/Shh midline signalling might act as a driving force for forebrain evolution.
Lampreys are a key species to study the evolution of morphological characters at the dawn of Craniates and throughout the evolution of the craniate's phylum. Here, we review a number of research fields where studies on lampreys have recently brought significant and fundamental insights on the timing and mechanisms of evolution, on the amazing diversification of morphology and on the emergence of novelties among Craniates. We report recent example studies on neural crest, muscle and the acquisition of jaws, where important technical advancements in lamprey developmental biology have been made (morpholino injections, protein-soaked bead applications or even the first transgenesis trials). We describe progress in the understanding and knowledge about lamprey anatomy and physiology (skeleton, immune system and buccal secretion), ecology (life cycle, embryology), phylogeny (genome duplications, monophyly of cyclostomes), paleontology, embryonic development and the beginnings of lamprey genomics. Finally, in a special focus on the nervous system, we describe how changes in signaling, neurogenesis or neuronal migration patterns during brain development may be at the origin of some important differences observed between lamprey and gnathostome brains.
In the anamniote model animals, zebrafish and Xenopus laevis, highly comparable early forebrain expression patterns of proneural basic helix-loop-helix (bHLH) genes relevant for neurogenesis (atonal homologs, i.e., neurogenins/NeuroD and achaete-scute homologs, i.e., Ascl/ash) were previously revealed during a particular period of development (zebrafish: 3 days; frog: stage 48). Neurogenins/NeuroD on the one hand and Ascl1/ash1 on the other hand exhibit essentially mutually exclusive spatial patterns, probably reflecting different positional information received within the neural tube, and appear to underlie glutamatergic versus GABAergic neuronal differentiation, respectively. Significant data suggest that similar complementary localizations of these proneural genes and corresponding differentiation pathways also exist in the mouse, the prominent mammalian model. The present article reports on detailed mouse brain bHLH gene expression patterns to fill existing gaps in the identification of expression domains, especially outside the telencephalon. Clearly, there are strong similarities in the complementarity of territories expressing Ascl1/Mash 1 versus neurogenins/NeuroD in the entire mouse forebrain, except for the pretectal alar plate and basal plate of prosomeres 1-3. The analysis substantiates localization of neurogenins/NeuroD in the pallium, eminentia thalami, and dorsal thalamus, and expression of Ascl1/Mash 1 in the striatal and septal subpallium, preoptic region, ventral thalamus, and hypothalamus, which is highly similar to the situation described in Xenopus and zebrafish. Thus, all three vertebrate model species display a "phylotypic stage or period" corresponding to a temporally and spatially defined control of neurogenesis during forebrain development, ultimately resulting in the differentiation of distinct populations of glutamatergic versus GABAergic neurons.
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