Identification of neural progenitor cells and their progeny reveals long distance migration in the developing octopus brain
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Evaluation Summary:
This is a well-presented study on the development of the central nervous system in the octopus O. vulgaris which is of broad interest to scientists in the field of evolutionary developmental biology. The authors provide an excellent in situ gene expression study of neural genes whose expression is conserved in the developing CNS across the animal kingdom. To identify the origin of neural progenitors in the early embryo, the study furthermore includes cell lineage tracing and the analysis of mitotic activity.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)
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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.
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Reviewer #3 (Public Review):
This is a well-presented study on the development of the CNS in the octopus O. vulgaris. The aim of the study is to identify the origin of the neural progenitors of the brain. The authors provide an excellent gene expression study of conserved neural genes to identify the location of these progenitors. Furthermore, by cell lineage tracing, they confirm the results of a previous study by Koenig et al. showing that the progeny of neural progenitors generated in the so-called lateral lips, a region adjacent to the eyes, migrate to different brain areas. The neural precursor location in the brain can be correlated with their spatial origin from the neural progenitors in the lateral lips. The authors suggest that the spatial map of the lateral lips is conserved in cephalopods. Furthermore, they analyse the …
Reviewer #3 (Public Review):
This is a well-presented study on the development of the CNS in the octopus O. vulgaris. The aim of the study is to identify the origin of the neural progenitors of the brain. The authors provide an excellent gene expression study of conserved neural genes to identify the location of these progenitors. Furthermore, by cell lineage tracing, they confirm the results of a previous study by Koenig et al. showing that the progeny of neural progenitors generated in the so-called lateral lips, a region adjacent to the eyes, migrate to different brain areas. The neural precursor location in the brain can be correlated with their spatial origin from the neural progenitors in the lateral lips. The authors suggest that the spatial map of the lateral lips is conserved in cephalopods. Furthermore, they analyse the mitotic activity in the developing brain by Ov-pcna in situ hybridisation and anti-PH3 immunohistochemistry. The authors conclude that "grossly, the embryonic octopus brain does not contain dividing progenitor cells." Based on the cell lineage studies, the strong expression of neural genes in the lateral lip and the observed mitotic activity, the authors overall conclude that the lateral lips represent the neurogenic zone in the developing brain of the octopus, i.e. that the neural progenitors of the brain derive from this area. I agree with the authors that the lateral lips are neurogenic regions, however, it is also possible that neural progenitors do arise from other regions of the developing brain. Overall this is a valuable contribution to our knowledge of neurogenesis in deuterostomian invertebrates and in a wider context the evolution of neural developmental processes.
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Reviewer #2 (Public Review):
The authors established a comprehensive map of neurogenetic sites with evolutionary conserved neurogenic and postmitotic gene expression in a common octopus, Octopus vulgaris that has been a historically important species in comparative neuroscience and behavioral studies. The selected molecules include representative regulatory genes such as achaete-scute, neurogenin, and neuroD, and also proliferating cell markers such as elav and PCNA. In subsequent experiments by using a fluorescent dye, the authors carefully traced the migratory pathways from the target ectodermal sites surrounding eyes to many developing brain lobes of clearing staged embryos with light sheet microscopy for 3D reconstruction.
They found that the special regions called lateral lip and other special ectodermal areas produced a pool of …
Reviewer #2 (Public Review):
The authors established a comprehensive map of neurogenetic sites with evolutionary conserved neurogenic and postmitotic gene expression in a common octopus, Octopus vulgaris that has been a historically important species in comparative neuroscience and behavioral studies. The selected molecules include representative regulatory genes such as achaete-scute, neurogenin, and neuroD, and also proliferating cell markers such as elav and PCNA. In subsequent experiments by using a fluorescent dye, the authors carefully traced the migratory pathways from the target ectodermal sites surrounding eyes to many developing brain lobes of clearing staged embryos with light sheet microscopy for 3D reconstruction.
They found that the special regions called lateral lip and other special ectodermal areas produced a pool of migratory postmitotic neurons that might contribute a novelty for developing octopus large and complex brains as in mammals, in contrast to those of other invertebrates such as flies or worms.
I find the bodies of evidence convincing. A good study usually opens many new questions. Before publication, I found two major points that may enhance the author's conclusions.
Are the migratory cells only neurons, or could they also be glia, neurosecretory, blood, or immune cells? The enlarged views of the migratory cells and the cytological features must be clarified.
The expression of canonical neurogenic genes disappears during middle and late stages, meaning that octopus has very unique neurogenic mechanisms compared to mammals? Consider the octopus-specific novelty.
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Reviewer #1 (Public Review):
The authors first use light sheet microscopy to reconstruct embryonic brain development of O. vulgaris. From these images they note a region adjacent to the eye and the developing brain that initially increases in size and subsequently shrinks. They perform transcriptomics and use phylogenetic analyses to identify 4 classes of genes involved in neurogenesis: those that specify the neuroectoderm, neurogenic genes, and markers for differentiated neurons and mature neurons. They perform spatio-temporal analyses of these genes to demonstrate that the lateral lip is the neurogenic region that harbours neuronal progenitors. This region is distinct from the brain, suggesting that neurons migrate long distances from where they are specified to populate the brain. They perform lineage tracing to provide evidence for …
Reviewer #1 (Public Review):
The authors first use light sheet microscopy to reconstruct embryonic brain development of O. vulgaris. From these images they note a region adjacent to the eye and the developing brain that initially increases in size and subsequently shrinks. They perform transcriptomics and use phylogenetic analyses to identify 4 classes of genes involved in neurogenesis: those that specify the neuroectoderm, neurogenic genes, and markers for differentiated neurons and mature neurons. They perform spatio-temporal analyses of these genes to demonstrate that the lateral lip is the neurogenic region that harbours neuronal progenitors. This region is distinct from the brain, suggesting that neurons migrate long distances from where they are specified to populate the brain. They perform lineage tracing to provide evidence for this migration and demonstrate that the lateral lip is spatially fated so that regions within it generate neurons specific to parts of the brain.
In summary, this is an elegant study that provides deep insight into embryonic neurogenesis in O. vulgaris.
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Evaluation Summary:
This is a well-presented study on the development of the central nervous system in the octopus O. vulgaris which is of broad interest to scientists in the field of evolutionary developmental biology. The authors provide an excellent in situ gene expression study of neural genes whose expression is conserved in the developing CNS across the animal kingdom. To identify the origin of neural progenitors in the early embryo, the study furthermore includes cell lineage tracing and the analysis of mitotic activity.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)
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