Morphogenesis underlying the development of the everted teleost telencephalon

Abstract

BackgroundAlthough 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.ResultsHere 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.ConclusionOur 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.

Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

“…In topological terms, this possibility could still be compatible with the simple eversion hypothesis if we consider that the eversion occurs not only in a lateral direction but also caudally. Nieuwenhuys [2011] agrees with this developmental pattern, which was originally proposed by Yamamoto et al [2007] and received some empirical support from a recent zebrafish study reporting that the embryonic posterior pallial territories evert and enlarge in a caudolateral direction [Folgueira et al, 2012]. If the Dlv lies in the most distal pallial position, and the pallium out-folds in a caudolateral direction, then the Dp would occupy a topological position comparable to that of the parahippocampal cortices of mammals and birds, that is, proximally surrounding the hippocampal pallium and interfacing it with the dorsal pallium.…”

Subdivisions of the adult zebrafish pallium based on molecular marker analysis

“…However, in ray-finned fishes the rostral neural tube is thought to bend outward resulting in two telencephalic hemispheres separated by an unpaired ventricle and covered by a thin roof plate, thus referred to as “everted” 1, 3, 4 . In the rayfin teleost zebrafish, it has been shown that the morphogenetic movement that creates this different layout of the telencephalon does not result from a simple lateral outward bending of the telencephalic walls 5 . Instead, telencephalon morphogenesis comprises first the generation of a ventricular outfolding between telencephalon and diencephalon, followed by an enlargement of the pallial territory rostrally 5 .…”

“…In the rayfin teleost zebrafish, it has been shown that the morphogenetic movement that creates this different layout of the telencephalon does not result from a simple lateral outward bending of the telencephalic walls 5 . Instead, telencephalon morphogenesis comprises first the generation of a ventricular outfolding between telencephalon and diencephalon, followed by an enlargement of the pallial territory rostrally 5 . The different development of the telencephalon results in an unpaired ventricle and a different arrangement of the parts in the pallium compared to all other vertebrates 1, 4, 6 .…”

Notch3 signaling gates cell cycle entry and limits neural stem cell amplification in the adult pallium

“…The morphology of the juvenile telencephalon resembles that of the adult, with an externally located ('everted') ventricular zone (Folgueira et al, 2012) composed for a majority of RG, as revealed using the glial markers GS or BLBP (Figs 6, 7).…”