Moreno N , González A .

             neurogenesis

	FIGURE 1. Pallial boundaries during development. Micrographs of transverse sections through the telencephalon of Xenopus laevis at embryonic (A–D), premetamorphic (E–G) and prometamorphic (H–N) stages. In each panel the developmental stage and the color code for the used markers are indicated. In the developing telencephalon, the combined immunohistochemical detection of Tbr1, expressed in the pallium, and Isl1, a subpallial marker, clearly allowed the identification of the boundary between both regions throughout the rostrocaudal extent (A–G,J,L–N). The localization of Tbr1 (H) at rostral level, in comparison with GABA (I), highlights the olfactory bulb, where GABA was very abundant, in contrast to the pallium, where the Tbr1 expression was observed (H,I). Simultaneous labeling for GABA and Isl1 discerns the SPa from the pallium (K). Scale bars = 50 μm (A–G), 100 μm (H–N). See list for abbreviations.
	FIGURE 2. Ventricular limits and mitotic cells. Micrographs of transverse sections through the pallium of Xenopus laevis at embryonic (A,A′,A′′,B,B′), premetamorphic (C,C′,C′′) and prometamorphic (D,D′) stages. The DAPI staining allowed the identification of the ventricular extent (A–D), and, additionally, to examine the position of mitotic cells (A′,A′′,B′,C′,C′′,D′). (A–C) Are confocal images, and the higher magnifications (A′,A′′,B′,C′,C′′,D′) correspond to the framed areas, as indicated (white boxes in A–D). Throughout development, in ventricular layer the cells are densely packed, but the thickness of this layer was larger at early stages (A,B), than later in larval stages (C,D). At embryonic stages, ventricular mitotic cells were primarily visualized (A′,A′′, see arrowhead in B), but also abventricular mitotic cells were detected (see asterisk in B′). During the larval period, mitotic cells were also observed in the ventricular side (asterisk in C′D′) and abventricularly (asterisk in C′′ and see arrowhead in D). Scale bars = 50 μm (A–C,A′,A′′), 25 μm (B′,C,C′′), 100 μm (D,D′). See list for abbreviations.
	FIGURE 3. Mitotic rate. Micrographs of transverse sections through the pallium of Xenopus laevis at embryonic (A,B), premetamorphic (C) and prometamorphic (D) stages showing the distribution of PH3, marker of proliferating and mitotic cells, in combination to DAPI. During development, mitotic cells were observed in the ventricular cell layer, but also abventricularly (arrowheads in A–D). The mitotic index significantly increased at the end of the embryonic period, but it significantly decreased at early larval stages, to drastically increase later at stage 54, when a neurogenetic peak is observed (E). This pattern is observed not only in the pallium, but also when pallial and subpallial regions separately analyzed, where significant differences in their mitotic index were not observed at any stage (F). Considering separately during development the DM and the VL, major differences in their mitotic index were not observed, with the exception of the stage 37/38 when the dorsomedial proliferation is slightly higher, but it did not continue later in development (G). Scale bars = 50 μm (A–C), 200 μm (D). See list for abbreviations. ∗∗P < 0.001, ∗P < 0.05.
	FIGURE 4. Proliferation analysis with BrdU. (A) Schematic drawing illustrating the experimental approach used, in which BrdU was administrated at the embryonic stages specified and the animals were sacrificed at the larval stages indicated. (B–E) Micrographs of transverse sections through the pallium of Xenopus laevis at embryonic (B,C) and premetamorphic larvae (D,E) stages showing the distribution of BrdU labeling in combination to PH3 and DAPI; the color code and the stages analyzed are indicated. The developmental stage of BrdU administration is indicated in each micrograph. After the BrdU administration at early embryonic stages and subsequent processing at late embryonic stages (B,C) and early larvae stages (D), the BrdU+ cells were situated in the mantle zone equally distributed and double PH3/BrdU labeled cells were not detected (B,C), but PH3 mitotic cells in ventricular and abventricular positions were observed (see arrowheads in B,C). After the BrdU administration at late embryonic stages and subsequent processing at early larvae stages (E) there were not PH3/BrdU+ double labeled cells, and the BrdU+ cells were situated in the mantle zone, but additionally in the ventricular layer. Scale bars = 50 μm (B–E). See list for abbreviations.
	FIGURE 5. Neuronal birth during pallial development. (A) Schematic drawing illustrating the experimental approach used, in which BrdU was administrated at the stages specified and the animals were sacrificed at the larval stages indicated. (B–E) Micrographs of transverse sections through the pallium of Xenopus laevis at premetamorphic (B), prometamorphic (C,D) and metamorphic (E) stages. Twenty four hour after the BrdU administration almost all the positive cells were concentrated in the ventricular zone (B) and additionally abventricular BrdU+ cells were found (arrowhead in B). 15 days after the BrdU, labeled cells were found away from the ventricle in adjacent layers (C). Similarly, 30 days (D) and 60 days (E) after the administration, the BrdU+ cells migrated to more superficial positions. Scale bars = 100 μm (B–E). See list for abbreviations.
	FIGURE 6. Analysis of progenitor cells at embryonic stages (BLBP, Lhx2, Sox2, Pax6, PH3). Micrographs of transverse sections through the pallium of Xenopus laevis at embryonic stages showing the codistribution of the progenitor markers BLBP (A,C), Lhx2 (B,C,E–G), Sox2 (D), and Pax6 (E,F′); and the combination of Lhx2 with the mitotic marker PH3 (G,H). In each panel the developmental stage and the color code for the used markers are indicated. (F,F′) Are confocal images, and the higher magnification shown in (F’) corresponds to the framed area indicated in (F). The BLBP (A) and the Lhx2 (B) labeling detected at stage 37/38 showed double labeled cells exclusively in the ventricle (C). The combination of Lhx2 and Sox2 also showed double labeled cells in the ventricle, but the cells detected for both markers in the mantle were never double labeled (D). In the case of Pax6, Lhx2/Pax6 double labeled cells were observed in the ventricular zone (E,F′), but never away from this region, where both cell populations were intermingled (F′). The labeling of Lhx2 in combination with PH3 showed that only the ventricular cells expressing Lhx2 were mitotic cells (G,H). Scale bars = 50 μm. See list for abbreviations.
	FIGURE 7. Analysis of progenitor cells at embryonic stages (Sox2, DCX, PH3). Micrographs of transverse sections through the pallium of Xenopus laevis at embryonic stages 37/38 (A–D,I,L) and 42 (E–H,J,K,M,N) showing the codistribution of the progenitor marker Sox2 (A,E) and the neuroblast marker DCX (B,F) in combination to DAPI (D,H), and the combination of DCX with the mitotic marker PH3 (I–K). In each panel the developmental stage and the color code for the used markers are indicated. All micrographs are confocal images, and the higher magnifications (L,M,N) correspond to the framed areas, as indicated (white boxes in C,G,K). At the ventricular zone there were observed double labeled cells for Sox2 and DCX (see arrowheads in A–C, E–G), and those cells were mitotic cells (see white circles and filled arrowheads in D,H). Additional double labeled cells were observed away from the ventricle (see empty arrowheads in E–H). The combination of DCX and PH3 showed double DCX/PH3 labeled cells in the ventricle and away from it (see arrowheads in I,J). Scale bars = 25 μm (A–H,L,M), 50 μm (I–K). See list for abbreviations.
	FIGURE 8. Analysis of progenitor cells at larval stages (Lhx2, Pax6, BLBP). Micrographs of transverse sections through the pallium of Xenopus laevis at the larval stage 54 showing the distribution of the progenitor markers Lhx2 (A–C,F,G), Pax6 (B,C) and BLBP (D–G). In each panel the color code for the used markers is indicated. The higher magnifications (B,E,F) are from the panels indicated in each case (white boxes in A,D). At this stage in the ventricular zone Lhx2 is expressed by virtually all cells (A,F), and those cells co-expressed Pax6 (B,C) and BLBP (G). Lhx2 expressing cells away from the ventricle, like in the medial pallium, were also labeled for Pax6 (B,C), but never expressed BLBP (G). Scale bars = 100 μm (A,D), 50 μm (B,C,E–G). See list for abbreviations.
	FIGURE 9. Analysis of progenitor cells at larval stages (Sox2, DCX, BLBP, PCNA, PH3). Micrographs of transverse sections through the pallium of Xenopus laevis at larval stages 46 (A–E,M) and 54 (F–L,N–R) showing the distribution of the progenitors markers Sox2 (A,C,F,H,I,J,L,N), the neuroblasts marker DCX (B,C,E,G–I,Q) and the progenitors markers Lhx2 (M,N,Q) and BLBP (O,P), and their combinations with the mitotic marker PCNA (L,O,P) and PH3 (M). In addition, the codistribution of DCX and calretinin is shown (Q). In each panel the developmental stage and the color code for the used markers are indicated. (A–E,O,P) Are confocal images, and the higher magnifications (O′,P′,R′) correspond to the framed areas, as indicated (white boxes in O,P,R). At stage 46 Sox2/DCX double labeled cells were observed in the ventricular zone and away from it (arrowheads in A–C), and DCX labeled mitotic cells away from the ventricle were observed (arrowheads in E). At stage 54 Sox2 is expressed in the ventricular and mantle zones, and cells that coexpressed DCX were observed (F–I). Close to the ventricle those Sox2 cells were mitotic cells (J,K), but the Sox2 expressing cells detected away from the ventricle were not mitotic (empty arrowhead in L). The Lhx2 expressing cells detected at larval stages were mitotic in the ventricle (M) and coexpressed Sox2 (N), but in the mantle zone they were not coexpressing PH3 (M) and were intermingled with the Lhx2 cell population (empty arowheads in N). The combination of BLBP and PCNA showed that the mitotic cells in the ventricular zone coexpressed BLBP (arrowheads in O′,P,P′), but not those separated from the ventricle (empty arrowhead in P′). The combination of Lhx2 and DCX showed that the Lhx2 cells detected close to the adjacent vz were double labeled (Q). The combination of Sox2 to calretinin, a marker of a population of pallial interneurons, showed that there were not double labeled cells (R,R′). Scale bars = 50 μm (A–E,L,M,O–P′), 200 μm (I), 100 μm (F–K,N). See list for abbreviations.
	FIGURE 10. Analysis of progenitor cells at larval stages (Tbr2, BLBP, Pax6, PH3). Micrographs of transverse sections through the pallium of Xenopus laevis at the larval stage 54 showing the distribution of the markers Tbr2 (A,C,D′,E′,F,K), BLBP (B,C,D,E) and Pax6 (G–J,L), and the combination of Tbr2 with the mitotic marker PH3 (M–P). In each panel the color code for the used markers is indicated. The higher magnifications (D,E) correspond to the framed areas, as indicated (white boxes in A,B). Tbr2 expressing cells were detected close to the ventricle and away from it (A,D′,E′,F,K) but only those cells in the ventricular zone expressed BLBP (D,D′,E,E′) or Pax6 (F–L). The combination of Tbr2 and PH3 showed that there are not Tbr2 mitotic cells away from the ventricle (M–P). Scale bars = 200 μm (A,B,F,G), 100 μm (C,H,J–M), 50 μm (D,E,I,N,O,P). See list for abbreviations.
	FIGURE 11. Summary diagram of the progenitor cells in the pallium of Xenopus laevis. Schematic representations showing that there are two phases of progenitor cells divisions, at mid-embryonic period and at mid-larval development. The pallial developmental order follows an outside-in pattern, in which BLBP, Pax6, Lhx2 and Sox2 are expressed in the ventricular proliferative zone and later Lhx2 and Pax6 are expressed in postmitotic cells away from the ventricle. Sox2 mitotic cells are present in ventricular and abventricular zones, and some of those cells express DCX. In the case of Tbr2, it is not expressed by mitotic abventricular cells.
	FIGURE 12. Pallial progenitor cells subtypes during evolution. Cladogram showing the pallial progenitor cells subtypes present in the different groups of tetrapod vertebrates. In mammals, the apical progenitors, or radial glial cells, proliferate and generate basal progenitors, or intermediate progenitors, which include Tbr2+ cells and specially the distinct svz, defined on the basis of the distribution of Tbr2+ cells. In birds, apical progenitors exist but there is a controversy about the nature of the basal progenitors. Nomura and collaborators (3) propose that basal progenitors and Tbr2+ cells are different cell populations. In contrast, Martínez-Cerdeño and collaborators (2) propose that birds posses a distinct svz with intermediate progenitors based on Tbr2+ expression. In lizards Tbr2 cells are present but there are not abventricular mitotic cells. In turtles there are Tbr2+ dividing cells, but a svz-like structure is only defined in the dorsal ventricular zone. Finally, in Xenopus the apical progenitors are conserved and there are abventricular mitosis, but the Tbr2+ cells are not dividing cells (present results). Thus, in evolutionary terms, the present evidences show that before the amniote evolution, in the tetrapod common ancestor subapical mitotic cells appeared and those are the origin of the basal progenitors and possible a distinct svz. 1: Martínez-Cerdeño et al., 2012; 2: Martínez-Cerdeño et al., 2016; 3: Nomura et al., 2016, 4: present results.

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