Embryonic origin and lineage hierarchies of the neural progenitor subtypes building the zebrafish adult midbrain

Abstract

Neurogenesis in the post-embryonic vertebrate brain varies in extent and efficiency between species and brain territories. Distinct neurogenesis modes may account for this diversity, and several neural progenitor subtypes, radial glial cells (RG) and neuroepithelial progenitors (NE), have been identified in the adult zebrafish brain. The neurogenic sequences issued from these progenitors, and their contribution to brain construction, remain incompletely understood. Here we use genetic tracing techniques based on conditional Cre recombination and Tet-On neuronal birthdating to unravel the neurogenic sequence operating from NE progenitors in the zebrafish post-embryonic optic tectum. We reveal that a subpopulation of her5-positive NE cells of the posterior midbrain layer stands at the top of a neurogenic hierarchy involving, in order, the amplification pool of the tectal proliferation zone (TPZ), followed by her4-positive RG cells with transient neurogenic activity. We further demonstrate that the adult her5-positive NE pool is issued in lineage from an identically located NE pool expressing the same gene in the embryonic neural tube. Finally, we show that these features are reminiscent of the neurogenic sequence and embryonic origin of the her9-positive progenitor NE pool involved in the construction of the lateral pallium at post-embryonic stages. Together, our results highlight the shared recruitment of an identical neurogenic strategy by two remote brain territories, where long-lasting NE pools serve both as a growth zone and as the life-long source of young neurogenic RG cells.

Wnt signaling regulates proliferation and differentiation of radial glia in regenerative processes after stab injury in the optic tectum of adult zebrafish

“…In the adult telencephalon, radial glia (RG) operate as neural stem cells in both physiological and regenerative conditions and Notch and FGF signaling have been reported to control the ability of RG to generate new neurons in both conditions (Ganz, Kaslin, Hochmann, Freudenreich, & Brand, ; Kishimoto, Shimizu, & Sawamoto, ). However, few studies have examined other parts of the brain, such as the olfactory bulb, optic tectum, and cerebellum (Galant et al, ; Kaslin et al, ).…”

Involvement of sonic hedgehog and notch signaling in regenerative neurogenesis in adult zebrafish optic tectum after stab injury

“…Optic tectum of adult zebrafish has two neuronal stem cell populations, NE and RG (Ito, Tanaka, Okamoto, & Ohshima, ). In post‐embryonic phase including adult stage, NE in tectal proliferation zone (TPZ) and her5‐positive NE in peripheral midbrain layer (PML) generate both neurons and RG in periventricular gray zone (PGZ) under physiological condition (Galant et al, ; Ito et al, ). Most of RG are, however, quiescent in physiological condition.…”

Tectal stem cells display diverse regenerative capacities

“…Cross-sections through the posterior tectum reveal that at this neuroanatomical level (yellow line), a larger domain of EdU + NE progenitor cells can be identified ( Fig. 1e; dashed lines), from which the tectal NE lineage and RG cells are derived (Galant et al, 2016). These distinctive stem/progenitor niches within the adult optic tectum provide an exceptional experimental system to investigate how each population ( Fig.…”

“…Embryonically these cells are derived from slow-amplifying progenitors (Recher et al, 2013). Recently it has been demonstrated that these NE-Ap are the final progenitor phenotype of a well-defined NE lineage that originate from Her5-positive NE stem cells in the posterior tectum (Galant et al, 2016). Moreover, recent evidence suggests that NE cells of the zebrafish tectum rely on Wnt/β-catenin signalling to promote stem cell proliferation towards a neuronal phenotype (Shitasako et al, 2017), similar to the role of Wnt in the adult mammalian stem cell niches (Adachi et al, 2007;Jang et al, 2013;Seib et al, 2013).…”