Abstract
Adult neurogenesis, i.e., the generation of neurons from neural stem cells (NSCs) in the adult brain, contributes to brain plasticity in all vertebrates. It varies, however, greatly in extent, location and physiological characteristics between species. During the last decade, the teleost zebrafish (D. rerio) was increasingly used to study the molecular and cellular properties of adult NSCs, in particular as a prominent NSC population was discovered at the ventricular surface of the dorsal telencephalon (pallium), in territories homologous to the adult neurogenic niches of rodents. This model, for its specific features (large NSC population, amenability to intravital imaging, high regenerative capacity) allowed rapid progress in the characterization of basic adult NSC features. We review here these findings, with specific comparisons with the situation in rodents. We specifically discuss the cellular nature of NSCs (astroglial or neuroepithelial cells), their heterogeneities and their neurogenic lineages, and the mechanisms controlling NSC quiescence and fate choices, which all impact the neurogenic output. We further discuss the regulation of NSC activity in response to physiological triggers and non-physiological conditions such as regenerative contexts.
Highlights
The teleost zebrafish (D. rerio) was increasingly used to study the molecular and cellular properties of adult neural stem cells (NSCs), in particular as a prominent NSC population was discovered at the ventricular surface of the dorsal telencephalon, in territories homologous to the adult neurogenic niches of rodents
Newlyborn neurons are physiologically important for the plasticity of specific circuits, notably involved in learning and memory, and impaired adult neurogenesis can correlate with emotional disorders (Anacker and Hen, 2017; Jorgensen, 2018; Toda et al, 2019)
Pharmacological blockade of Notch signaling in zebrafish, which globally leads to NSC quiescence exit, revealed different lag phases to re-enter cycling, and approximately 5% of quiescent NSCs did not respond to the blockade (Alunni et al, 2013)
Summary
These compounds (BrdU, CldU, EdU) incorporate into the DNA of cycling cells during the S phase. Clonal tracing in a number of adult stem cell systems rather supports a model where stem cells are self-renewing and bi-potent at the population level, choosing stochastically between balanced numbers of amplifying, asymmetric or differentiative divisions This is no exception in the adult brain where several studies, both in mouse and zebrafish, are compatible, at least in part, with such “population asymmetry” ensuring both neural stem cell maintenance and neuronal production. Pallial Neurogenesis in Zebrafish Is the Output of a Proliferative Hierarchy Involving Functionally Specialized NSC Sub-Pools The zebrafish adult pallium is amenable to NSC fate studies for several reasons: (i) its superficial location permits intravital imaging the direct tracing, during several weeks, of NSC fate in the absence of biased genetic tools and under non-invasive conditions (Barbosa et al, 2015b; Dray et al, 2015), (ii) its small size permits analyzing clones in whole-mount preparations, avoiding the risk of losing cells that occurs when studying brain sections, and (iii) the absence of cell death and migrations makes it easier to quantify clones in their entirety (Than-Trong et al, 2020). Quiescence Length Remains to Be Measured With Precision Through genetic lineage tracings and live imaging in zebrafish and mouse, we know that NSCs can re-enter quiescence after activation
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