Jiménez S and Moreno N , Development of subdomains in the medial pallium...

XB-ART-59462

Front Neuroanat null;16:1039081. doi: 10.3389/fnana.2022.1039081.

Show Gene links Show Anatomy links

Development of subdomains in the medial pallium of Xenopus laevis and Trachemys scripta: Insights into the anamniote-amniote transition.

Jiménez S , Moreno N .

Abstract
In all vertebrates, the most dorsal region of the telencephalon gives rise to the pallium, which in turn, is formed by at least four evolutionarily conserved histogenetic domains. Particularly in mammals, the medial pallium generates the hippocampal formation. Although this region is structurally different among amniotes, its functions, attributed to spatial memory and social behavior, as well as the specification of the histogenetic domain, appears to be conserved. Thus, the aim of the present study was to analyze this region by comparative analysis of the expression patterns of conserved markers in two vertebrate models: one anamniote, the amphibian Xenopus laevis; and the other amniote, the turtle Trachemys scripta elegans, during development and in adulthood. Our results show that, the histogenetic specification of both models is comparable, despite significant cytoarchitectonic differences, in particular the layered cortical arrangement present in the turtle, not found in anurans. Two subdivisions were observed in the medial pallium of these species: a Prox1 + and another Er81/Lmo4 +, comparable to the dentate gyrus and the mammalian cornu ammonis region, respectively. The expression pattern of additional markers supports this subdivision, which together with its functional involvement in spatial memory tasks, provides evidence supporting the existence of a basic program in the specification and functionality of the medial pallium at the base of tetrapods. These results further suggest that the anatomical differences found in different vertebrates may be due to divergences and adaptations during evolution.

PubMed ID: 36406242
PMC ID: PMC9670315
Article link: Front Neuroanat

Species referenced: Xenopus laevis
Genes referenced: cux2 egfr lhx2 lmo4.1 mef2c pax6 prox1 sox2

Article Images: [+] show captions

	Figure 1. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis at embryonic (1), premetamorphic (2), prometamorphic larvae stages (3A–E) and adult (4A′–E′). Nissl staining allowed the anatomical identification of the medial pallium during embryonic stages prior to telencephalic evagination (1) or after evagination in premetamorphic (2), prometamorphic (3) larval stages and adult (4). The region of the medial pallium is pink-colored in the schematic drawings of telencephalon semi-hemispheres. Scale bar in 1, 2, (3A–E) = 200 μm, (4A′–E′) = 500 μm. See the abbreviation list.
	Figure 3. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis (A–D) and Trachemys scripta elegans (E–G) at the stages indicated in each photomicrograph, showing the direction of the radial glia in both models (arrows) by BLBP in X. laevis and GFAP in T. scripta. The asterisks indicate the pallial commissure. The thin dotted lines point to the ventricular surface and the thick dotted lines to the pallium-subpallium boundary. Scale bar = 200 μm. See the abbreviation list.
	Figure 4. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis (A–F) and Trachemys scripta elegans (G–I) of Lhx2 expression in the medial pallium at embryonic (A–C,G–I) and early (D) and late larvae stages (E,F). In each panel the developmental stage is indicated. Filled arrowheads point to ventricle expressing cells and empty arrowheads to mantle expressing cells. Scale bar (A–H) = 200 μm and (I) = 100 μm. See the abbreviation list.
	Figure 5. Photomicrographs of transverse sections through the developing telencephalon of Xenopus laevis (A–E) and Trachemys scripta elegans (F–M) showing the distribution of Lhx2 in combination with PH3, where only double-labeled mitotic cells are observed in the ventricular zone (arrowheads). The progenitor cell marker Sox2 (B,J) is observed in both cases in the ventricular region (filled arrowhead) and in X. laevis at these stages additionally in the mantle (empty arrowhead). The Lhx2 cells are proximal to the ventricle co-expressed Pax6 in the ventricle (filled arrowhead) and out of it [empty arrowheads in panel (C)]. The neuroblast marker doublecourtine (D,E,L,M) was detected in the ventricular region of the medial pallium in both cases (filled arrowheads). In each panel, the developmental stage and the color code for the used markers are indicated. Filled arrowheads point to ventricle-expressing cells and empty arrowheads to mantle-expressing cells. Scale bar in panels (A,B,D–L) = 200 μm and (C,M) = 100 μm. See the abbreviation list.
	Figure 6. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis at larval stages (A–C) and adult (D–F) showing, from rostral to caudal levels, Prox1 expression (A–F) and its combination with Lhx2 (G,H). In each panel, the developmental stage and the color code for the used markers are indicated. Empty arrowheads point to mantle-expressing cells. Scale bar = 200 μm. See the abbreviation list.
	Figure 8. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis (A–I) and Trachemys scripta elegans (J–L) showing, from rostral to caudal levels, the Er81 expression at embryonic (A), premetamorphic (B,C) and prometamorphic larval X. laevis stages (D–F) and adults (G–I) and adults Trachemys scripta elegans (J–L). Filled arrowheads point to ventricle expressing cells. Scale bar in panels (A–F,J–L) = 200 μm and (G–I) = 500 μm. See the abbreviation list.
	Figure 9. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis (A–G) and Trachemys scripta elegans (H–J) showing, from rostral to caudal levels, the Lmo4 expression at developmental stages (A–C,H, I) and adults (D–G,J). Scale bar in panels (A–E,G–J) = 200 μm and (F) = 500 μm. See the abbreviation list.
	Figure 10. Photomicrographs of transverse sections through the telencephalon of Xenopus laevis (A–D) showing, from rostral to caudal levels, the Prox1/Er81 (A,B) and the Prox1/Lmo4 expressions (C,D). The white box in the figures (A–D) corresponds to the magnifications shown in the adjacent photos with the single staining (A′–D′,A′′–D′′). In each panel, the color code for the used markers is indicated. Scale bar = 200 μm. See the abbreviation list.
	Figure 11. Photomicrographs of transverse sections through the developing and adult telencephalon of Xenopus laevis (A–J) and Trachemys scripta elegans (K–O). Ventricular expression is detected in the MP (filled arrowheads) and mantle (empty arrowheads), in prometamorphic larvae (A,B) of Xenopus and, adult (C). This localization is confirmed by the combination of Ctip2 with Er81, detected in the DMP (D). Expression of Cux2 (E), Mef2c (F,G) and EGFR (H–J) are localized in adult X. laevis in the MP region. Ctip2 expression in developing T. scripta is observed in MCx and in DMCx (K), whereas in the adult was observed mainly in the MCx (L,M), as well as Cux2 in developing (N) and in adults (O). In each panel, the developmental stage and the color code for the used markers are indicated. Filled arrowheads point to ventricle-expressing cells and empty arrowheads to mantle-expressing cells. Scale bar in panels (A,C–O) = 200 μm and (B) = 100 μm. See the abbreviation list.
	Figure 12. Photomicrographs of transverse sections through the developing and adult telencephalon of Xenopus laevis (A–D) and Trachemys scripta elegans (E–I) showing the combined expression of Satb1/2 with Prox1 (A–C,E–G) and Cux2 (D,H,I). In each panel, the developmental stage and the color code for the used markers are indicated. Yellow arrowheads (A–D) indicate double-labeled cells. The white box in Figure (E) corresponds to the magnified photo in panel (F). The white arrowheads point to Satb1/2 positive cells, no double-labeled. Scale bar in panels (A–E,G–I) = 200 μm and (F) = 100 μm. See the abbreviation list.
	Figure 13. (A) Summary diagram of the temporal gene expression of the markers analyzed in this study in the medial pallium of Xenopus laevis and Trachemys scripta elegans. (B) Schematic representations in development and adult showing that there are two subdivisions in both models, the MP/MCx: Prox1 + and the DMP/DMCx: Er81/Lmo4 +, related to mammalian DG and CA respectively. The X in the diagram indicates the lack of Prox1 expression at these developmental stages. The color code is indicated in each figure. Silhouette images of adult animals were obtained from phylopic.org. See the abbreviation list.

References [+] :

Abellán, Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. 2014, Pubmed