Identification of neural progenitor cells and their progeny reveals long distance migration in the developing octopus brain.

Astrid Deryckere,Ruth Styfhals,Ali Murat Elagoz,Eve Seuntjens,Gregory E Maes

doi:10.7554/elife.69161

Astrid Deryckere, Ruth Styfhals + Show 3 more

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https://doi.org/10.7554/elife.69161

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Abstract

Cephalopods have evolved nervous systems that parallel the complexity of mammalian brains in terms of neuronal numbers and richness in behavioral output. How the cephalopod brain develops has only been described at the morphological level, and it remains unclear where the progenitor cells are located and what molecular factors drive neurogenesis. Using histological techniques, we located dividing cells, neural progenitors and postmitotic neurons in Octopus vulgaris embryos. Our results indicate that an important pool of progenitors, expressing the conserved bHLH transcription factors achaete-scute or neurogenin, is located outside the central brain cords in the lateral lips adjacent to the eyes, suggesting that newly formed neurons migrate into the cords. Lineage-tracing experiments then showed that progenitors, depending on their location in the lateral lips, generate neurons for the different lobes, similar to the squid Doryteuthis pealeii. The finding that octopus newborn neurons migrate over long distances is reminiscent of vertebrate neurogenesis and suggests it might be a fundamental strategy for large brain development.

Highlights

Cephalopod mollusks represent an invertebrate lineage that exhibits morphological as well as behavioral complexity reminiscent of vertebrates
In clades harboring species with diffuse nerve nets such as cnidaria and hemichordates, the proliferating neural progenitor cells are distributed throughout the ectoderm generating local neurons, while inphyla with a centralized nervous system including vertebrates, arthropods and some annelids, the neural progenitor cells are grouped in the neurectoderm
In a hybridization chain reaction experiment combined with immunohistochemistry (Figure 5), we show that Ov-ngn and Ov-ascl1 are likely expressed in a different subset of progenitor cells, since their expression was not overlapping (Figure 5F)

Summary

Introduction

Cephalopod mollusks represent an invertebrate lineage that exhibits morphological as well as behavioral complexity reminiscent of vertebrates. Studying species from this group brings an opportunity to understand the genetic drivers of the development of organ systems that evolved convergently with vertebrates. In clades harboring species with diffuse nerve nets such as cnidaria and hemichordates, the proliferating neural progenitor cells are distributed throughout the ectoderm generating local neurons, while in (sub)phyla with a centralized nervous system including vertebrates, arthropods and some annelids, the neural progenitor cells are grouped in the neurectoderm. Neuronal migration has been described in developing invertebrate nervous systems as well, this process is generally limited to restricted cell populations, e.g. the Q, CAN and HSN neuroblasts in Caenorhabditis elegans (Blelloch et al, 1999; Forrester et al, 1998; Montell, 1999), or to short-range migratory events, e.g. in the Drosophila visual system (Apitz & Salecker, 2015; Bhat, 2007; Morante et al, 2011)

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