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Dev Dyn
2015 Oct 01;24410:1202-14. doi: 10.1002/dvdy.24312.
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Evolutionary Conservation of the Early Axon Scaffold in the Vertebrate Brain.
Ware M
,
Dupé V
,
Schubert FR
.
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The early axon scaffold is the first axonal structure to appear in the rostral brain of vertebrates, paving the way for later, more complex connections. Several early axon scaffold components are conserved between all vertebrates; most notably two main ventral longitudinal tracts, the tract of the postoptic commissure and the medial longitudinal fascicle. While the overall structure is remarkably similar, differences both in the organization and the development of the early tracts are apparent. This review will bring together extensive data from the last 25 years in different vertebrates and for the first time, the timing and anatomy of these early tracts have been directly compared. Representatives of major vertebrate clades, including cat shark, Xenopus, chick, and mouse embryos, will be compared using immunohistochemistry staining based on previous results. There is still confusion over the nomenclature and homology of these tracts which this review will aim to address. The discussion here is relevant both for understanding the evolution of the early axon scaffold and for future studies into the molecular regulation of its formation.
Figure 1. Schematics of the established early axon scaffold in the vertebrate brain of model organisms. Each tract that forms in the anamniotes or amniotes is colour coded to show where the neurons are located and the projection of their axons. A: Cat shark, stage 25 (80 somites) (adapted from Ware et al., 2014b). B: Zebrafish, 24 hpf. Gray circles highlight neuronal populations and older terminology for population names. C: Xenopus stage 32 (26 somites). D: Chick HH18 (31 somites) (adapted from Ware and Schubert, 2011). E: Mouse E10.5 (33–37 somites). Transversal gray lines mark the prosomeric boundaries. Longitudinal gray line marks the alar/basal boundary. For abbreviations, see Table 1.Download figure to PowerPoint
Figure 2. Schematic representation of the early axon scaffold tracts throughout vertebrate evolution. Lamprey is an example of a nonjawed vertebrate. The first divergence represented for jawed vertebrates is cartilaginous fish with cat shark. The next divergence is for the bony fish with zebrafish, turbot and medaka shown as representatives. The next major divergence is for the tetrapods, with Xenopus and axolotl representing amphibians. The next divergence to be made is the amniotes. Chick and alligator are examples for birds and reptiles, respectively. With further divergence for the mammals, mouse is used as an example. The neuron origin is represented by a black circle and the arrowheads indicates the direction of the axonprojection from their neurons (where known). For abbreviations see Table 1.Download figure to PowerPoint
Figure 3. Comparison of the initial neurons that arise in the cat shark, Xenopus, chick, and mouse embryonic brains. A–F: The first neurons to arise in the rostral brain are MLF neurons in (A,B) cat shark (Tuj1) at stage 18 (arrow) (adapted from Ware et al., 2014b), (C,D) Xenopus (HNK-1) at stage 22 (arrow), asterisk shows peripheral staining, and (E,F) chick (Tuj1) at HH11 (arrow) (adapted from Ware and Schubert, 2011). G: In mouse (Tuj1), the first neurons give rise to the DTmesV at E8.5. H: The first MLF neurons appear at E9 (arrow). A,E: White box indicates higher magnification from the same embryo in B and F. For abbreviations, see Table 1. Scale bars = 100 µm.Download figure to PowerPoint
Figure 4. Comparison of the developing early axon scaffold at an intermediate stage in the cat shark, Xenopus, chick, and mouse embryonic brains. All images are in lateral view of whole-mount embryos. More neuron populations are forming and neurons are projecting axons to form tracts. A,B: Cat shark (Tuj1), Stage 22 (adapted from Ware et al., 2014b), scattered neurons located rostral to the MLF axon tract (arrow). Scattered neurons are present, rostral to the MLF tract (arrow in B). C,D: Xenopus (HNK-1), Stage 27. The DVDT, TPOC and DLT have formed tracts. E,F: Chick (Tuj1), HH15. The TPOC and DTmesV have started forming tracts. The MLF is formed from three populations of neurons: central (arrow), ventral (unfilled arrow) and dorsal (arrowhead). MTT neurons are located rostrally to the MLF neurons (unfilled arrowhead). G,H: Mouse (Tuj1), E9.5. Ventral neurons located in the diencephalon and mesencephalon that belong to the nMLF (arrow). C,E,G: White box indicates higher magnification from the same embryo in D, F, and H. For abbreviations see Table 1. Scale bars = 100 µm.Download figure to PowerPoint
Figure 5. Comparison of the established early axon scaffold in the vertebrate embryonic brain. All images are in lateral view of whole-mount embryos. The early axon scaffold is well established. A,B: Cat shark (Tuj1) at Stage 25 (adapted from Ware et al., 2014b). D–F: Xenopus (HNK-1) at stage 32. G–I: Chick (Tuj1) at HH18 (adapted from Ware and Schubert, 2011). J,K: Mouse (Tuj1) at E10.5. G,J: Asterisk: olfactory placode and constitute of the terminal nerveganglion. Organization of the MLF neuronal populations are highlighted using HuC/D which labels the neuronal cell bodies in all the vertebrates here. C: Cat shark, stage 23. Two nMLF populations: ventral (arrow) and dorsal (arrowhead). F: Xenopus, stage 32. I: Chick. The MLF is formed from three populations of neurons: central (arrow), ventral (unfilled arrow) and dorsal (arrowhead). MTT neurons are located rostrally to the MLF neurons (unfilled arrowhead). L: Mouse, E9.5. MLF neurons are located ventrally (arrow), while DTmesV are present throughout the mesencephalon. A,D,G,F: White box indicates higher magnification from the same embryo in B, E, H and K. For abbreviations, see Table 1. Scale bars = 100 µm.Download figure to PowerPoint
