Morphogenesis underlying the development of the everted teleost telencephalon
Open accessAbstract
Background: Although the mechanisms underlying brain patterning and regionalization are very much conserved, the morphology of different brain regions is extraordinarily variable across vertebrate phylogeny. This is especially manifest in the telencephalon, where the most dramatic variation is seen between ray-finned fish, which have an everted telencephalon, and all other vertebrates, which have an evaginated telencephalon. The mechanisms that generate these distinct morphologies are not well understood. Results: Here we study the morphogenesis of the zebrafish telencephalon from 12 hours post fertilization (hpf) to 5 days post fertilization (dpf) by analyzing forebrain ventricle formation, evolving patterns of gene and transgene expression, neuronal organization, and fate mapping. Our results highlight two key events in telencephalon morphogenesis. First, the formation of a deep ventricular recess between telencephalon and diencephalon, the anterior intraencephalic sulcus (AIS), effectively creates a posterior ventricular wall to the telencephalic lobes. This process displaces the most posterior neuroepithelial territory of the telencephalon laterally. Second, as telencephalic growth and neurogenesis proceed between days 2 and 5 of development, the pallial region of the posterior ventricular wall of the telencephalon bulges into the dorsal aspect of the AIS. This brings the ventricular zone (VZ) into close apposition with the roof of the AIS to generate a narrow ventricular space and the thin tela choroidea (tc). As the pallial VZ expands, the tc also expands over the upper surface of the telencephalon. During this period, the major axis of growth and extension of the pallial VZ is along the anteroposterior axis. This second step effectively generates an everted telencephalon by 5 dpf. Conclusion: Our description of telencephalic morphogenesis challenges the conventional model that eversion is simply due to a laterally directed outfolding of the telencephalic neuroepithelium. This may have significant bearing on understanding the eventual organization of the adult fish telencephalon.
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The telencephalon of actinopterygian fish develops by eversion of the embryonic telencephalic walls, contrasting with evagination in non-actinopterygian vertebrates.
“The telencephalon of actinopterygian fish presents a very divergent process of development compared with all other vertebrates, namely the “folding out” or eversion of the embryonic telencephalic walls, that contrast with the “folding in” or evagination that takes place in non-actinopterygian vertebrates [160,161,162,163].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [160]
The Background identifies the ray-finned fish telencephalon as everted and the more conventional vertebrate telencephalon as evaginated. But the Background and Conclusion explicitly challenge the claim that eversion develops through outward folding of the telencephalic walls; the paper describes that as a conventional model its data do not support. (LLM, conf=0.90)
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Spatial Cognition in Teleost Fish: Strategies and Mechanisms
Rodríguez, F., Quintero, B., Amores, L., Madrid, D., Salas-Peña, C., & Salas, C. (2021) · Animals · doi:10.3390/ani11082271 · Cited by 59 · see citing works
- Authors
- Folgueira, M., Bayley, P., Navratilova, P., Becker, T. S., Wilson, S. W., & Clarke, J. D.
- Affiliations
- University College London (GB)
- The University of Sydney (AU)
- Guy's Hospital (GB)
- Corresponding author
- Clarke, Jonathan DW
- Venue
- Neural Development
- Published
- 2012-09-18
- Volume
- 7
- Issue
- 1
- Pages
- 32-32
- ISSN
- 1749-8104 (ISSN-L)
- PMC
- PMC3520737
- OpenAlex
- W2145435031
- Cited by
- 120
- References
- 3
- Citations by year
- 2026: 3 · 2025: 12 · 2024: 11 · 2023: 9 · 2022: 13 · 2021: 13 · 2020: 11 · 2019: 13 · 2018: 3 · 2017: 6 · 2016: 10 · 2015: 8 · 2014: 5 · 2013: 3
- FWCI
- 1.73
- Type
- journal article
- Language
- en
- Update notices
- erratum (2015-10-02)
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Neural Development (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Wellcome Trust
- Universidade da Coruña
- Biotechnology and Biological Sciences Research Council (BB/H013016/1, BB/H012516/1)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Keywords
- diencephalon, brain regionalization, fate mapping, gene expression patterns
- MeSH terms
- Animals, Brain Mapping, Bromodeoxyuridine, Embryo, Nonmammalian, Morphogenesis, Neural Pathways, Neurons, RNA, Messenger, Telencephalon, Time Factors, Zebrafish, Microscopy, Confocal, Body Patterning, Neuropil, Zebrafish Proteins, Animals, Genetically Modified, Green Fluorescent Proteins
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