New neurons and glial cells continue to be born in restricted germinal regions in the adult mammalian brain (Alvarez-Buylla and Lim, 2004
; Zhao et al., 2008
). The largest germinal region of the adult brain is found on the walls of the lateral ventricles. In this region, primary neural progenitors reside in the subventricular zone (SVZ), displaced from the ventricles by ependymal cells. In contrast, primary neural progenitors in the developing brain reside in the ventricular zone (VZ), a pseudostratified epithelium in direct contact with the embryonic brain ventricles. Contact with the ventricle through an apical process is critical for maintaining germinal activity of the primary progenitors in the developing brain (Bittman et al., 1997
; Nadarajah et al., 1997
; Kosodo et al., 2004
; Weissman et al., 2004
). It is therefore intriguing that the primary progenitors in the adult brain are displaced from the ventricle.
In the embryonic VZ, the primary neural progenitors are radial glia (Noctor et al., 2007b
). These elongated stem cells maintain contact with both the pial surface and the ventricular surface. Shortly after birth however, radial glia transform into parenchymal astrocytes (Voigt, 1989
) and ependymal cells (Spassky et al., 2005
) and little remains of their unique morphology and behavior as the VZ is replaced by the ependymal epithelium.
Adult neural stem cells (NSC) in the SVZ generate large numbers of olfactory bulb interneurons and some oligodendrocytes in corpus callosum, fimbria and striatum (Jackson and Alvarez-Buylla, 2008
). These primary progenitors have been identified as a subpopulation of astrocytes called Type B1 cells (Doetsch et al., 1999a
), which are derived from radial glia (Merkle et al., 2004
). Interestingly, it has been shown that a small subpopulation of SVZ B1 cells have an apical membrane that contacts the ventricle and that the number of these contacts appears to be increased when SVZ proliferation is stimulated (Doetsch et al., 1999b
). For radial glia in the embryo, this apical membrane is a specialized structure enriched in prominin-1 (CD133) (Weigmann et al., 1997
), par-3 (Manabe et al., 2002
), and numb (Rasin et al., 2007
). It is the site where the primary cilium, basal body and daughter centriole are located during interphase (Cohen et al., 1988
), where the nucleus migrates for mitosis (Committee, 1970
), and where the midbody is found at the end of cytokinesis (Dubreuil et al., 2007
). Recent evidence suggests that the apical membrane may determine the symmetry of radial glial cell division (Kosodo et al., 2004
). The apical membrane of the ventricle-contacting B cells is therefore a potentially important link between adult neurogenesis from the SVZ and developmental neurogenesis from the VZ and may yield many insights into adult NSC function and niche organization.
We developed a new technique to study the apical and basal specializations and organization of different cell types that touch the ventricle in the adult brain. We find that most, if not all, B1 cells comprise a modified VZ in the adult brain with apical contacts and a unique pinwheel architecture. We have also characterized a novel type ependymal cell with 2 cilia and a previously undescribed basal body. This significantly reshapes our understanding of the architecture of this adult neurogenic niche. The work suggests that a neurogenic VZ persists in the adult mammalian brain.