Abstract

Primary neurulation is the process by which the neural tube, the central nervous system precursor, is formed from the neural plate. Incomplete neural tube closure occurs frequently, yet underlying causes remain poorly understood. Developmental studies in amniotes and amphibians have identified hingepoint and neural fold formation as key morphogenetic events and hallmarks of primary neurulation, the disruption of which causes neural tube defects. In contrast, the mode of neurulation in teleosts has remained highly debated. Teleosts are thought to have evolved a unique mode of neurulation, whereby the neural plate infolds in absence of hingepoints and neural folds, at least in the hindbrain/trunk where it has been studied. Using high-resolution imaging and time-lapse microscopy, we show here the presence of these morphological landmarks in the zebrafish anterior neural plate. These results reveal similarities between neurulation in teleosts and other vertebrates and hence the suitability of zebrafish to understand human neurulation.

Highlights

  • Primary neurulation is the process by which the neural tube, the central nervous system precursor, is formed from the neural plate

  • The zebrafish anterior neural plate (ANP) is quite distinct from the neural plate in more posterior regions, as it undergoes precocious epithelialization[37]

  • We observed that at 2–5 som the ANP has a V shape marked by a medial neural groove flanked by the elevated lateral edges of the ANP, which are reminiscent of Neural Folds (NFs) (Fig. 2a, b)

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Summary

Introduction

Primary neurulation is the process by which the neural tube, the central nervous system precursor, is formed from the neural plate. More anterior regions of the neural tube undergo primary neurulation as described above, most vertebrates exhibit a distinct type of neural tube formation in more posterior regions, termed secondary neurulation During this process, a mesenchymal cell population condenses into a solid neural rod that subsequently epithelializes and forms a central lumen[25,26]. Examination of the tissue architecture in zebrafish[28,29,30] and other teleosts[31,32] revealed that the neural rod is shaped by infolding of a neural plate (albeit incompletely epithelialized), which best fits the description of primary neurulation[33] Despite this evidence, differences in tissue architecture, the multi-layered organization of the neural plate and the apparent lack of hingepoints, neural groove and NFs are difficult to reconcile with a mode of primary neurulation and have contributed to the persistent view that neural tube formation in teleosts is different than in other vertebrates[34,35,36]

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