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Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression

Department of Molecular Cell Biology, Max-Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany

View larger version (101K): [in a new window]   Fig. 1. Svet1 RNA distribution in developing cortex. (A,B,D,E,G,H,M,N,P,Q) dark field; (C,F,I.O,R) bright field. Svet1 expression begins in the SVZ immediately after its first appearance in the rostrolateral cortex (B). The arrowhead in C indicates the transition between the rostral part of the cortex where the SVZ has just begun to form and the caudal part where there is no SVZ yet. The dashed line in C denotes the boundary between SVZ and VZ, which coincides with that of Svet1 expression. (D-R) Comparison of Otx1 and Svet1 expression in the E13.5 (D-L) and E15.5 (M-R) cortex. Otx1 is expressed in the cells of the cortical ventricular zone of both E13.5 (D,G,J) and E15.5 (M,P). In the cortex of E15.5 embryos, Otx1 is expressed in the cortical plate and intermediate zone. Note that in P and Q the expression of Otx1 is at similar levels in the SVZ and IZ, while Svet1 is confined to the SVZ only. I and R are high magnification views of the regions boxed in F and O. The dashed line in R demarcates the boundary between SVZ and VZ, which coincides with the boundary between Svet1 and Otx1 expression. (J,K) High power view of the region boxed in F. Arrowheads show the lower limit of Svet1 (K) and upper limit of Otx1 (J) expression. Left sides of J and K have been digitally contrasted by means of Adobe Photoshope software in order to demonstrate silver grain density more clearly. (L) Immunohistochemistry with anti-BrdU antibody on an adjacent section. The dashed line denotes the approximate boundary between the VZ an SVZ (svz + iz according to Altman and Bayer). The cortical region is the same as indicated by the box in F. BN, basal nuclei; cp, cortical plate; HIP, hippocampus; iz, intermediate zone; NC, neocortex; pl, primordial plexiform layer; SEP, septum; Th, thalamus. Bar in F, 100 µm.

View larger version (94K): [in a new window]   Fig. 2. Comparison of Otx1 and Svet1 expression in the cortex at E18.5 (A-C) and P2 (D-F). (A,B,D,E) Dark-field images; (C-F) bright-field images. At E18.5 Otx1 is expressed in the ventricular zone and in the lower part of the cortical plate, as well as in some cells migrating through the intermediate zone (A). Svet1 is expressed in the SVZ, in migrating cells and in cells located outside of Otx1 domain (B). The arrowhead indicates Svet1 expression in the cortical plate. The dashed lines in C denote the boundaries between Svet1 and Otx1 expression in both SVZ/VZ and the cortical plate. On the second postnatal day, Otx1 is expressed in layers V-VI. (D); Svet1 is expressed in superficial layers (E). MZ, marginal zone; other abbreviations as in Fig. 1.

View larger version (143K): [in a new window]   Fig. 3. Localization of Svet1 RNA in the E13.5 (A,B) and E14.5 (E,F) midbrain region; E14.5 spinal cord (C,D) and E18.5 septum (G,H). DH, dorsal horn of the spinal cord; IC, inferior colliculus; PRT, pretectum; TC, tectum; TG, tegmentum; VH, ventral horn of the spinal cord. Bars in B and F, 100 µm; in D, 50 µm.

View larger version (107K): [in a new window]   Fig. 4. (A-C) BrdU labeling (A) and digoxigenin Svet1 hybridization (B) at E15.5. (C) Superimposition of A and B. Cells positive for both labels indicated by arrowheads. (D) Digoxigenin hybridization with Svet1 probe in E14.5 brains. (E) High magnification view of boxed region in D.

View larger version (101K): [in a new window]   Fig. 5. Localization of Svet1 RNA in the E18.5 and P3 wild-type and ‘reeler’ brains. (A,B,E,F) dark-field, (C,D,G,H) bright-field views. In C,D,G,H the Svet1 expression domain is indicated by arrowheads. Wt, wild type.

View larger version (145K): [in a new window]   Fig. 6. (A-F) Comparison of the Otx1 and Svet1 cortical expression at the stage E15.5 in wild type (A,B) and homozygous Sey mutant (D-E). The size of the ventricular zone in the Sey mutant is not affected, as revealed by Otx1 expression (D). The SVZ is enlarged, its morphology is altered and it does not express Svet1 (F), which can be seen only in the cingulate cortex (E). (G-L) Comparison of the Otx1 and Svet1 cortical expression at the stage E18.5 of wild-type (G-I) and Sey mutant (J-L). Deep layer neurons (Otx1-positive cells) are present in the Sey cortical plate (J). Superficial layer neurons (Svet1-positive cells; Otx1/Svet1-negative cells of the cortical plate) are absent in the Sey cortex. Svet1 is not expressed in the SVZ of the Sey cortex (K). Arrowheads in F, K and L mark the lateral limit of Svet1 expression.

View larger version (143K): [in a new window]   Fig. 7. Anteroposterior differences in the cortical lamination of the E18.5 Sey mutant. Transverse sections through the wild type (A-C) and Sey (D-F) frontal and the wild type (G-I) and Sey (J-L) occipital cortex. The dashed line on C,F,I and L demarcates the upper boundary of deep layers. Note the absence of granular cells of upper layers above the dashed line in F. Arrowheads in E and F mark the lateral limit of Svet1 expression. Svet1 cells are reduced in number but not completely missing in the SVZ of the mutant occipital cortex. Arrowheads in K mark the altered SVZ region. Note the presence of upper layer cells above the dashed line on L.

View larger version (22K): [in a new window]   Fig. 8. A hypothesis for the role of SVZ in cortical lamination (see Discussion for the details)