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To shed light on the organisation of the Xenopus laevis telencephalon, we have used two sets of developmental regulators: genes acting in early regional specification (x-Dll3, x-Nkx2.1, x-Emx1, x-Pax6, x-Eomes) or in cell determination (x-Lhx5 and x-Lhx7). After expression patterns analysis, separately or combined, on whole-mount brains and serial sections, we identify the Xenopus pallium and subpallium, and the subdivisions herein. The data show a conservation of the same basic Bauplan for Xenopus forebrain patterning compared to other vertebrates, and suggest the possibility for LIM-homeodomain genes to be candidate downstream target of the regionalization genes. Comparing the relative sizes of the deduced subdivisions, Xenopus seems to have an intermediate phylogenetic position in terms of pallium contribution to the telencephalon, and ventralpallium contribution to the pallium.
Fig.1. In toto analysis of x-Dll3, x-Nkx2.1, x-Emx1, x-Pax6 and x-Eomes expression in Xenopus brain. Whole-mount dissected brains at stage 32 (left column, entire brain) and stage 35 (right column, focused on the forebrain) are photographed in lateral views. In all panels, anterior is left and dorsal is up. The arrowhead in (A,C,E,G,I) indicates the position of the psb between the pallium (pa) and the subpallium (spa). The asterisk in (B) points to the x-Dll3 negative area in the rostral forebrain, see text. The inset indicates the plan of sections for transverse (t) and horizontal (h) sections in the next figures, as deduced from the axis of the brain. This antero-posterior axis is indicated by black arrows. Therefore, in the telencephalon, a horizontal section is parallel to the axis and allows the visualisation of transverse boundaries and divisions. Abbreviations are in Table 1. Scale BAR=100 μm.
Fig. 2. Analysis on sections of x-Dll3, x-Nkx2.1, x-Emx1, x-Pax6 and x-Eomes expression at stage 32 and 35. (A–C,E,G) Single labelling and (D,F,H) double-labelling for the indicated genes. The gene names are colour-coded to indicate the pink, orange or purple reaction associated to the probe. All panels show horizontal sections (presented from rostral to caudal) and/or transverse sections (presented from dorsal to ventral). Asterisk in (A) indicates the x-Dll3 negative area surrounded by the subpallium (same as Fig. 1, panel B), discussed in text as the rostral pallium. In all panels, arrowheads indicate the presence of pallial markers expressed in a subpallial (x-Dll3 expressing) location, discussed in text as being the striatum. In all panels, arrows indicate pallial markers expressed in the rostral pallium, discussed in text as being the olfactory bulb. Asterisk in (F) (transverse section) shows the absence of x-Pax6 expression in the MZ of a subregion of the pallium, discussed in text as the DP. The results are pooled from stage 32 (A,B,D,E,G and Hhorizontal) and 35 (C,F and Htransverse) embryos. Note that there is no strict correspondence between the antero-posterior/dorso-ventral levels shown in the different panels. See Table 1 for abbreviations. Scale BAR=100 μm.
Fig. 3. Relative expression of x-Dll3, x-Emx1, x-Pax6 and x-Eomes at stage 40. Expression of pallial markers (blue) relative to x-Dll3 (orange) on horizontal (A,B) and transverse (C) sections through the forebrain of stage 40 embryos. Horizontal sections and transverse sections are presented in a rostro-caudal and dorso-ventral order, respectively. Asterisk in (A) indicates the x-Dll3 negative area surrounded by the subpallium (same as Fig.1 and Fig. 2). In all panels, arrowheads indicate the presence of pallial markers expressed in a subpallial (x-Dll3 expressing) location. See Table 1 for abbreviations. Scale BAR=100 μm.
Fig. 4. Co-expression of Xenopus regionalisation genes and LIM-hd genes in the same forebrain subdivisions. Horizontal sections through the telencephalon and the diencephalon of stage 32 embryos double labelled for x-Pax6 and x-Lhx5 (A) and x-Nkx2.1 and x-Lhx7 (B). For example, x-Nkx2.1 and x-Lhx7 are co-localised in the mge and hypothalamus but not in branchial arches (ba). tec, tectum. See Table 1 for abbreviations. Scale BAR=100 μm.
Fig.5. Model summary of Xenopus embryonic forebrain subdivisions deduced from expression of x-Dll3, x-Nkx2.1, x-Emx1, x-Pax6 and x-Eomes. (A)
Schematic lateral view of an embryonic (compound stage 32/40) Xenopus brain with deduced subdivisions (orientation like in toto views in Fig. 1). Gene
expressions are colour-coded and migrated/migratory cells are indicated by little dots. The expression of each gene through the VZ, SVZ and MZ of the
neuroepithelium is recapitulated for each gene marker in each proposed subdivision. (B) Deduced subdivisions are indicated on a schematic hemi-section taken
from double-labelled embryos with the indicated probes. The subdivisions clearly emerge from the careful observation of labelling throughout the depth of the
neuroepithelium for each combination of genes. See Table 1 for abbreviations.
Fig. 6. Evolution of the relative size of telencephalic subdivisions in vertebrates. Schematic phylogenetic tree representing the major transitions in the
vertebrate lineage. For each species a schematic brain is drawn with pallial (purple) and subpallial (green) telencephalic divisions. The brain drawings are
obviously not to scale and therefore point to the relative size of the subdivisions. Lamprey is adapted from Murakami et al. (2001), zebrafish is deduced from
Rohr et al. (2001) and Hauptmann and Gerster (2000), and chick and mouse are adapted from Puelles et al. (2000). For zebrafish the pallial subdivisions are
tentative, as these data are not available.