Patterning of a telencephalon-like region in the adult brain of amphioxus

Benito‐Gutiérrez, Èlia; Stemmer, Manuel; Sd, Rohr; Ln, Schuhmacher; Tang, Jocelyn L.Y.; Marconi, Aleksandra; Jékely, Gáspár; Arendt, Detlev

doi:10.1101/307629

Cited by 10 publications

(5 citation statements)

References 41 publications

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“…In order to test such hypothesis, we pharmacologically arrested proliferation, at the time when this early regionalisation of the brain starts, coinciding with the time at which proliferation resumes and restricts to the cerebral vesicle (and chordoneural hinge posteriorly). We found that localised proliferation in the amphioxus brain is necessary to generate the anterior serotonergic cells of the frontal eye complex, as we previously proposed (Benito-Gutiérrez et al, 2018). In stark contrast, we found that glutamatergic neurons, including those anterior cells associated to the frontal eye complex, remain in place despite the absence of proliferation.…”

Section: Discussionsupporting

confidence: 84%

Restricted proliferation during neurogenesis contributes to regionalization of the amphioxus nervous system

Gattoni

Andrews

Benito‐Gutiérrez

2021

Preprint

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The central nervous system of the cephalochordate amphioxus consists of a dorsal neural tube with an anterior brain. Two decades of gene expression analyses in developing amphioxus embryos have shown that despite the lack of overt segmentation the amphioxus neural tube is highly regionalized at the molecular level. However, little is known about the mechanisms that generate such precise regionalization. Proliferation is a key driver of pattern formation and cell type diversification, but in amphioxus it has never been studied in detail nor in the specific context of neurogenesis. Here, we describe the dynamics of cell division during the formation of the central nervous system in amphioxus embryos and its contributions to the regionalization of the neural axis. We show that after gastrulation, proliferation pauses to become spatially restricted to the anterior and posterior ends of the neural tube at neurula stages. Only at the onset of larval life, proliferation resumes in the central part of the nervous system. By marking specific populations and inhibiting cell division during neurulation, we demonstrate that proliferation in the anterior cerebral vesicle is required to establish the full cell type repertoire of the frontal eye complex and the putative hypothalamic region of the amphioxus brain, while posterior proliferating progenitors, which were found here to derive from the dorsal lip of the blastopore, contribute to elongate the caudal floor plate. Between these proliferative domains, we find trunk nervous system differentiation is independent from cell division, which decreases during neurulation and resumes at the early larval stage. Taken together, our results highlight multiple roles for proliferation in shaping the amphioxus nervous system.

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Section: Discussionsupporting

confidence: 84%

Restricted proliferation during neurogenesis contributes to regionalization of the amphioxus nervous system

Gattoni

Andrews

Benito‐Gutiérrez

2021

Preprint

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“…We found that localised proliferation in the amphioxus anterior brain is necessary to generate the anterior serotonergic cells of the frontal eye complex, as we previously proposed ( Benito-Gutiérrez et al, 2018 ). These neurons are born from progenitors proliferating between the 6 and 7 ss stage.…”

Section: Discussionsupporting

confidence: 84%

Restricted Proliferation During Neurogenesis Contributes to Regionalisation of the Amphioxus Nervous System

2022

Self Cite

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The central nervous system of the cephalochordate amphioxus consists of a dorsal neural tube with an anterior brain. Two decades of gene expression analyses in developing amphioxus embryos have shown that, despite apparent morphological simplicity, the amphioxus neural tube is highly regionalised at the molecular level. However, little is known about the morphogenetic mechanisms regulating the spatiotemporal emergence of cell types at distinct sites of the neural axis and how their arrangements contribute to the overall neural architecture. In vertebrates, proliferation is key to provide appropriate cell numbers of specific types to particular areas of the nervous system as development proceeds, but in amphioxus proliferation has never been studied at this level of detail, nor in the specific context of neurogenesis. Here, we describe the dynamics of cell division during the formation of the central nervous system in amphioxus embryos, and identify specific regions of the nervous system that depend on proliferation of neuronal precursors at precise time-points for their maturation. By labelling proliferating cells in vivo at specific time points in development, and inhibiting cell division during neurulation, we demonstrate that localised proliferation in the anterior cerebral vesicle is required to establish the full cell type repertoire of the frontal eye complex and the putative hypothalamic region of the amphioxus brain, while posterior proliferating progenitors, which were found here to derive from the dorsal lip of the blastopore, contribute to elongation of the caudal floor plate. Between these proliferative domains, we find that trunk nervous system differentiation is independent from cell division, in which proliferation decreases during neurulation and resumes at the early larval stage. Taken together, our results highlight the importance of proliferation as a tightly controlled mechanism for shaping and regionalising the amphioxus neural axis during development, by addition of new cells fated to particular types, or by influencing tissue geometry.

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“…In addition to the frontal eye complex of the cerebral vesicle, VGlut ‐expressing neurons in the CNS are only found in young larvae in the primary motor center and in association with the first pigment spot (Lacalli, 1996; Lacalli & Candiani, 2017). More develop in the dorsal pre‐infundibular part of the cord as the larvae mature and metamorphose, in a region now thought to be a homolog of the vertebrate telencephalon (Benito‐Gutiérrez et al, 2018). The glutamatergic neurons of the amphioxus primary motor center have been identified as the third set of large paired neurons (the LPN3s, Lacalli & Candiani, 2017).…”

Section: Discussionmentioning

confidence: 99%

Amphioxus neuroglia: Molecular characterization and evidence for early compartmentalization of the developing nerve cord

Bozzo

Lacalli

Obino

et al. 2021

Glia

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Glial cells play important roles in the development and homeostasis of metazoan nervous systems. However, while their involvement in the development and function in the central nervous system (CNS) of vertebrates is increasingly well understood, much less is known about invertebrate glia and the evolutionary history of glial cells more generally. An investigation into amphioxus glia is therefore timely, as this organism is the best living proxy for the last common ancestor of all chordates, and hence provides a window into the role of glial cell development and function at the transition of invertebrates and vertebrates. We report here our findings on amphioxus glia as characterized by molecular probes correlated with anatomical data at the transmission electron microscopy (TEM) level. The results show that amphioxus glial lineages express genes typical of vertebrate astroglia and radial glia, and that they segregate early in development, forming what appears to be a spatially separate cell proliferation zone positioned laterally, between the dorsal and ventral zones of neural cell proliferation. Our study provides strong evidence for the presence of vertebrate‐type glial cells in amphioxus, while highlighting the role played by segregated progenitor cell pools in CNS development. There are implications also for our understanding of glial cells in a broader evolutionary context, and insights into patterns of precursor cell deployment in the chordate nerve cord.

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Patterning of a telencephalon-like region in the adult brain of amphioxus

Cited by 10 publications

References 41 publications

Restricted proliferation during neurogenesis contributes to regionalization of the amphioxus nervous system

Restricted proliferation during neurogenesis contributes to regionalization of the amphioxus nervous system

Restricted Proliferation During Neurogenesis Contributes to Regionalisation of the Amphioxus Nervous System

Amphioxus neuroglia: Molecular characterization and evidence for early compartmentalization of the developing nerve cord

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