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We investigated whether gamma-amino butyric acidergic (GABAergic) cell populations correlate positionally with specific Dlx-expressing histogenetic territories in an anamniote tetrapod, the frog Xenopus laevis. To that end, we cloned a fragment of Xenopus GAD67 gene (xGAD67, expressed in GABAergic neurons) and compared its expression with that of Distal-less-4 gene (xDll-4, ortholog of mouse Dlx2) in the forebrain at late larval and adult stages. In Xenopus, GABAergic neurons were densely concentrated in xDll-4-positive territories, such as the telencephalic subpallium, part of the hypothalamus, and ventral thalamus, where nearly all neurons expressed both genes. In contrast, the pallium of Xenopus generally contained dispersed neurons expressing xGAD67 or xDll-4, which may represent local circuit neurons. As in amniotes, these pallial interneurons may have been produced in the subpallium and migrated tangentially into the pallium during development. In Xenopus, the ventral division of the classic lateral pallium contained extremely few GABAergic cells and showed only low signal of the pallial gene Emx1, suggesting that it may represent the amphibian ventral pallium, homologous to that of amniotes. At caudal forebrain levels, a number of GABAergic neurons was observed in several areas (dorsal thalamus, pretectum), but no correlation to xDll-4 was observed there. The location of GABAergic neurons in the forebrain and their relation to the developmental regulatory genes Dll and Dlx were very similar in Xenopus and in amniotes. The close correlation in the expression of both genes in rostral forebrain regions supported the notion that Dll/Dlx are among the genes involved in the acquisition of the GABAergic phenotype.
Fig. 1. Three rostrocaudal series of adjacent cross sections through the telencephalon of an adult
Xenopus at the level of the olfactory bulb, stained for cresyl violet (CV; A, D, G) or hybridized for xGAD67
(C, F, I). For each section level, a schema of the major forebrain divisions, cell groups, and fiber tracts
is shown (B, E, H). For abbreviations, see list. Scale bar 200 um.
Fig. 2. Three rostrocaudal series of adjacent cross sections through the telencephalon of an adult
Xenopus at the level of the olfactory bulb, stained for cresyl violet (CV; A, D, G) or hybridized for xGAD67
(C, F, I). For each section level, a schema of the major forebrain divisions, cell groups, and fiber tracts
is shown (B, E, H). For abbreviations, see list. Scale bar 200 m.
Fig. 3. Three rostrocaudal series of adjacent cross sections through the telencephalon of an adult
Xenopus at the level of the olfactory bulb, stained for cresyl violet (CV; A, D, G) or hybridized for xGAD67
(C, F, I). For each section level, a schema of the major forebrain divisions, cell groups, and fiber tracts
is shown (B, E, H). For abbreviations, see list. Scale bar 200 m.
Fig. 4. Three rostrocaudal series of adjacent cross sections through the telencephalon of an adult
Xenopus at the level of the olfactory bulb, stained for cresyl violet (CV; A, D, G) or hybridized for xGAD67
(C, F, I). For each section level, a schema of the major forebrain divisions, cell groups, and fiber tracts
is shown (B, E, H). For abbreviations, see list. Scale bar 200 m.
Fig. 5. Three rostrocaudal series of adjacent cross sections through the telencephalon of an adult
Xenopus at the level of the olfactory bulb, stained for cresyl violet (CV; A, D, G) or hybridized for xGAD67
(C, F, I). For each section level, a schema of the major forebrain divisions, cell groups, and fiber tracts
is shown (B, E, H). For abbreviations, see list. Scale bar 200 m.
Fig. 6. Three rostrocaudal series of adjacent cross sections through the telencephalon of an adult
Xenopus at the level of the olfactory bulb, stained for cresyl violet (CV; A, D, G) or hybridized for xGAD67
(C, F, I). For each section level, a schema of the major forebrain divisions, cell groups, and fiber tracts
is shown (B, E, H). For abbreviations, see list. Scale bar 200 m.
Fig. 7. A–L: Rostrocaudal series of adjacent cross sections through the telencephalon and diencephalon
of an adult Xenopus, at levels similar to those shown in Figures 1–6. These are doubled-labeled
sections hybridized for xGAD67 (dark blue) and immunoreacted for calretinin (CR; brown). For abbreviations,
see list. Scale bar 200 m.
Fig. 8. Rostrocaudal series of adjacent cross sections through the
telencephalon and diencephalon of an adult Xenopus, at levels similar
to those shown in Figures 1–6, hybridized for xDll-4 (A, B, D–H) or
xEmx-1 (C). C: Note the strong periventricular expression of xEmx1 in
the dorsal pallium (DP) and lateralpallium (LP), which gradually and
rapidly decreases upon entering the ventralpallium (VP). For abbreviations,
see list. Scale bar 200 m.
Fig. 9. Sagittal sections through the forebrain of larval Xenopus at a medial or lateral level hybridized
for xDll-4 (A, B; stage 49) or xGAD67 (C, D; stage 42). Note the similarity of the signal patterns in most
forebrain regions, except in the alar and basal regions caudal to the zona limitans intrathalamica (the
p3/p2 boundary; i.e., caudal to the ventral thalamus). Scale bars 100 m in A,B 200 m in C, D.
gaad1.1 (glutamate decarboxylase 1) gene expression in adult Xenopus laevis, rostrocaudal cross-section through the telencephalon at the level of the olfactory bulb, assayed via in situ hybridized, with a schema of the major forebrain divisions, cell groups, and fiber tracts shown to left (B).
Key: aob= accessory olfactory bulb; igl= internal granular layer (olfactory bulb); mob= main olfcatory bulb
