Subpallial Dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the cerebral cortex and white matter

Abstract

The precise origins of postnatal subventricular zone (SVZ) cells are not known. Furthermore, the gliogenic potential of progenitors expressing Dlx genes that migrate ventrodorsally from the ganglionic eminences has not been explored in vivo. Here, we identify the embryonic origins of two distinct populations of postnatal SVZ cells: SVZ border cells, which express Zebrin II, and migratory cells in the central SVZ, which are generally devoid of Zebrin II expression (Staugaitis et al., 2001). Zebrin II is expressed by all cells of the telencephalic primordium, with its expression becoming restricted to astrocytes in the mature telencephalon. As the neuroepithelium folds during corticostriatal sulcus formation (embryonic day 13-15), a wedge of Zebrin II+ cells is created at the presumptive site of the dorsolateral SVZ. At this time, Dlx2-expressing cells and their progeny begin to migrate ventrodorsally along a medial path from the ganglionic eminences. These migratory subpallial cells invade the wedge of Zebrin II+ cells to form the central region of the SVZ. We used a Dlx2/tauLacZ knock-in to perform a short-term lineage analysis of Dlx2-expressing cells throughout SVZ formation and the postnatal peak of gliogenesis. Dlx2/tauLacZ [β-galactosidase (β-gal)]-expressing cells populate the central SVZ, whereas Zebrin II-expressing cells form its borders. Furthermore, β-gal expression demonstrates a lineage relationship between Dlx2-expressing cells and glia residing in the dorsal telencephalon. We propose a model for the formation of the postnatal SVZ and demonstrate that subpallium-derived Dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the white matter and cerebral cortex.