Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
Expression of the genes Emx1, Tbr1, and Eomes (Tbr2) in the telencephalon of Xenopus laevis confirms the existence of a ventral pallial division in all tetrapods.
Brox A
,
Puelles L
,
Ferreiro B
,
Medina L
.
???displayArticle.abstract???
To investigate the pallial organization and the exact location and extension of the ventralpallium in amphibians, we cloned a fragment of the homeobox XenopusTbr1 (xTbr1) gene and analyzed its expression compared with that of the genes xEomes (Tbr2) and xEmx1 in the telencephalon of the frog Xenopus laevis during embryonic and larval development. The expression of xEmx1 was also analyzed in the adult frog. We compared the expression patterns of these pallial marker genes with that of the subpallial gene xDistal-less-4 (xDll4). Our results indicate that the whole pallium of Xenopus expresses the T-box genes xTbr1 and xEomes (in proliferating cells and/or mantle) during embryonic and larval development, and the expression of these genes is topographically complementary to that of xDll4 in the subpallium. In addition to their massive expression in the pallium, both xTbr1 and xEomes are expressed in a few dispersed cells in the subpallium, which may represent immigrant cells of pallial origin, because these genes are not found in the subpallial proliferating cells. On the other hand, during development xEmx1 is expressed in a large part of the pallium (proliferating and postmitotic cells) except for an area adjacent to the pallio-subpallial boundary, where xEmx1 is observed only in some mantle cells. This pallial area poor in xEmx1 expression and poor in expression of the subpallial gene xDll4, but expressing the pallial marker genes xTbr1 and xEomes, appears to represent the amphibian ventralpallium, comparable to that described in other vertebrates (Puelles et al. [2000] J. Comp. Neurol. 424:409-438). In the adult frog, the ventralpallium appears to include the rostral part of the lateral amygdalar nucleus as well as a large part of the medial amygdalar nucleus (as defined by Marín et al. [1998] J. Comp. Neurol. 392:285-312). In contrast, the caudal part of the previously termed lateral amygdalar nucleus shows strong xEmx1 expression and may be a lateral pallial derivative. The possible homology of these amphibian amygdalar nuclei is discussed. Finally, expression of xTbr1, xEomes, and xEmx1 is observed in the mitral cell layer of the olfactory bulb from early developmental stages, further supporting that this structure is a pallial derivative.
Figure 1. A: Lateral view of a whole-mount brain of a Xenopus embryo at stage 33–34, hybridized for xDll4. The red dashed lines represent the horizontal section plane and level of the sections shown in panels B–L (a, telencephalic level, similar to those shown in panels B–E and I–J; b, section through the preoptic region [PO] and eminentia thalami [ET], similar to those shown in F–H and K–L). B: Schema of a horizontal section through the embryonic telencephalon of Xenopus showing the major telencephalic divisions based on the gene expression patterns shown in panels C–E. C–E,I,J: Horizontal sections through the telencephalon of Xenopus embryos at stages 33–34 (E), 35–36 (C,D), or 37–38 (I,J), hybridized for xEomes (C,I), xEmx1 (D,J) or xDll4 (E). Note the broad expression of xEomes in the pallium (P; in proliferating and postmitotic cells), which is complementary to that of xDll4 in the subpallium (SP; C,E). xEmx1 is also broadly expressed in the majority of the pallium, except for a ventral pallial area (ventralpallium or VP) that contains only xEmx1-expressing cells in the mantle (D, J). The ventralpallium shows the strongest xEomes expression (C,I). In addition to the expression of xEomes and xEmx1 in the pallium, signal of these genes is observed in the subpallial mantle and may represent immigrant cells coming from the pallium. F–H,K,L: Horizontal sections through the PO and ET of Xenopus embryos at stages 33–34 (H), 35–36 (F,G), or 37–38 (K,L), hybridized for xEomes (F,K), xEmx1 (G,L), or xDll4 (H). Note the strong expression of pallial marker genes in the ET and the absence of xDll4 expression in this region. Asterisks in J and L represent an artifact. See text for more details. For abbreviations , see list. Scale bars = 100 μm in A; 50 μm in C (applies to C–L).
Figure 2. Sagittal sections through the forebrain of Xenopus at late embryonic stages (stage 43), hybridized from xEomes (A,B), xEmx1 (C,D), or xDll4 (E,F). Note the general expression of xEomes and xEmx1 in the pallium and developing mitral cell layer of the olfactory bulb (A–D). The ventralpallium is a pallial subdivision rich in xEomes (A) but having only scattered cells expressing xEmx1 (C). The subpallium, rich in cells expressing xDll4 (E,F), contains a few cells expressing xEomes or xEmx1 in the mantle (A,B). More caudally, the eminentia thalami (ET) appears as a distinct domain located rostrodorsal to the ventralthalamus (VT), rich in xEomes (A) but poor in xDll4 (E). Note the strong xEmx1 expression domain in the basal plate of prosomere 2 (p2b). See text for more details. For abbreviations , see list. Scale bar = 50 μm in A (applies to all).
Figure 3. Sagittal sections through the forebrain of Xenopus at premetamorphic larval stages (stages 44–49), hybridized from xTbr1 (A,B), xEmx1 (E,F), or xDll4 (C,D). Note the general expression of xTbr1 and xEmx1 in the pallium and developing mitral cell layer of the olfactory bulb. The expression of these genes in the pallium is complementary to that of xDll4 in the subpallium (C,D). A few scattered cells expressing xTbr1 or xEmx1 are observed in the subpallial mantle (B,F). In the olfactory bulb, the majority of the cells in the internal granular layer (igl) and some cells in the glomerular layer (gl) express xDll4. Caudally, the eminentia thalami (ET) appears as a distinct domain located rostrodorsal to the ventralthalamus (VT), rich in xTbr1 (A) but poor in xDll4 (C). See text for more details. For abbreviations , see list. Scale bar = 50 μm in A (applies to all).
Figure 4. Frontal thick sections through the telencephalon of adult Xenopus, from rostral (left) to caudal (right) levels, hybridized for xEmx1 (A–C), xEomes (E–G), or xNkx2.1 (D). Note the strong periventricular expression of xEmx1 in the majority of the pallium (medial, dorsal, and lateral divisions), except the ventralpallium (VP; A–C). The posterolateral amygdalar nucleus (PLA) also shows strong xEmx1 signal (C). Strong xEomes expression is observed in the mitral cell layer of the olfactory bulb (ml; E), as well as in the eminentia thalami (ET; G). However, this gene is apparently downregulated in the pallium of the adult frog (E–G). Note the expression of xNkx2.1 in the pallidal telencephalic domain of adult Xenopus (D), and also note that a major part of the medial amygdalar nucleus does not show any periventricular xNkx2.1 signal. See text for more details. For abbreviations , see list. Scale bar = 200 μm in A (applies to all).
Figure 5. Frontal paraffin sections through the telencephalon of an adult Xenopus, from rostral (top) to intermediate (bottom) levels, hybridized for xEmx1 (A,C,E) or xDll4 (B,D,F). Note the strong xEmx1 expression in the majority of the pallium (specially in the dorsal and lateral divisions) except for the ventralpallium. Only a few xEmx1-expressing cells are observed in the VP mantle. In the pallium, including the ventralpallium, only some scattered mantle cells express the subpallial marker gene xDll4, and these are probably immigrant cells of subpallial origin. The rostral part of the lateral amygdalar nucleus (LA) is similar to the ventralpallium in its gene expression profile and may thus be a ventral pallial derivative. See text for more details. For abbreviations , see list. Scale bar = 200 μm in A (applies to all).
Figure 6. Frontal paraffin sections through the telencephalon of an adult Xenopus, from intermediate (top) to caudal (bottom) levels, hybridized for xEmx1 (A,C,E) or xDll4 (B,D,F). Note the strong xEmx1 expression in the majority of the pallium (specially in the dorsal and lateral divisions) except for the ventralpallium. Only a few xEmx1-expressing cells are observed in the VP mantle. In the pallium, including the ventralpallium, only some scattered mantle cells express the subpallial marker gene xDll4, and these are probably immigrant cells of subpallial origin. The caudal part of the lateral amygdalar nucleus, here called the posterolateral amygdalar nucleus (PLA), is rich in xEmx1 expression and may be a lateral pallial derivative. On the other hand, the medial amygdalar nucleus is poor in both xEmx1 and xDll4, and at least a major part of it may be a ventral pallial derivative. See text for more details. For abbreviations , see list. Scale bar = 200 μm in A (applies to all).
Figure 7. Schematics of frontal sections through the telencephalon of adult Xenopus, at intermediate (A) or caudal (B) levels, showing some of the major telencephalic divisions (pallium, subpallium) and subdivisions (striatum and pallidum in the subpallium; ventral pallium in the pallial domain), and the nuclei or areas included in them, as inferred from the expression patterns of several homeobox genes during development and in the adult. In frogs, the ventral pallium appears to include the postolfactory eminence (in the rostral septum), the ventral part of the classical lateral pallium, and some amygdalar nuclei, such as the lateral amygdalar nucleus (LA) and a major part of the medial amygdalar nucleus (MeA). The frog posterolateral amygdalar nucleus appears to belong to the lateral pallium. As in amniotes (Puelles et al., 2000), expression patterns of xDll4 and xNkx2.1 indicate that striatal-like and pallidal-like molecular subdivisions of the subpallium are found in the lateral telencephalic wall (including the basal ganglia and part of the amygdala) as well as in the septum of frogs (González et al., 2002a, b; Broxet al., 2003). In the subpallial amygdala, the so-called anterior and central amygdalar nuclei of frogs appear to belong to the striatal domain (Broxet al., 2003). On the other hand, a small part of the frog MeA may belong to the subpallium (maybe including a pallidal part; González et al., 2002a, b; Moreno and González, 2003). Thus, as in amniotes (Puelles et al., 2000), the amphibian amygdala appears to consist of lateral pallial, ventral pallial, striatal, and possibly pallidal subdivisions. See text for more details. For abbreviations , see list.
