Skip to main content
Log in

Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone

  • Review
  • Published:
Frontiers in Biology

Abstract

Background

The origin and classification of neural stem cells (NSCs) has been a subject of intense investigation for the past two decades. Efforts to categorize NSCs based on their location, function and expression have established that these cells are a heterogeneous pool in both the embryonic and adult brain. The discovery and additional characterization of adult NSCs has introduced the possibility of using these cells as a source for neuronal and glial replacement following injury or disease. To understand how one could manipulate NSC developmental programs for therapeutic use, additional work is needed to elucidate how NSCs are programmed and how signals during development are interpreted to determine cell fate.

Objective

This review describes the identification, classification and characterization of NSCs within the large neurogenic niche of the ventricular-subventricular zone (V-SVZ).

Methods

A literature search was conducted using Pubmed including the keywords “ventricular-subventricular zone,” “neural stem cell,” “heterogeneity,” “identity” and/or “single cell” to find relevant manuscripts to include within the review. A special focus was placed on more recent findings using single-cell level analyses on neural stem cells within their niche(s).

Results

This review discusses over 20 research articles detailing findings on V-SVZ NSC heterogeneity, over 25 articles describing fate determinants of NSCs, and focuses on 8 recent publications using distinct single-cell analyses of neural stem cells including flow cytometry and RNA-seq. Additionally, over 60 manuscripts highlighting the markers expressed on cells within the NSC lineage are included in a chart divided by cell type.

Conclusions

Investigation of NSC heterogeneity and fate decisions is ongoing. Thus far, much research has been conducted in mice however, findings in human and other mammalian species are also discussed here. Implications of NSC heterogeneity established in the embryo for the properties of NSCs in the adult brain are explored, including how these cells may be redirected after injury or genetic manipulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aguirre A, Rubio M E, Gallo V (2010). Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature, 467(7313): 323–327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ahn S, Joyner A L (2005). In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature, 437(7060): 894–897

    Article  CAS  PubMed  Google Scholar 

  • Altman J (1962). Autoradiographic study of degenerative and regenerative proliferation of neuroglia cells with tritiated thymidine. Exp Neurol, 5(4): 302–318

    Article  CAS  PubMed  Google Scholar 

  • Altman J, Das G D (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol, 124 (3): 319–335

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, García-Verdugo J M, Tramontin A D (2001). A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci, 2(4): 287–293

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Seri B, Doetsch F (2002). Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull, 57(6): 751–758

    Article  PubMed  Google Scholar 

  • Anthony T E, Klein C, Fishell G, Heintz N (2004). Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron, 41(6): 881–890

    Article  CAS  PubMed  Google Scholar 

  • Azim K, Zweifel S, Klaus F, Yoshikawa K, Amrein I, Raineteau O (2013). Early decline in progenitor diversity in the marmoset lateral ventricle. Cereb Cortex, 23(4): 922–931

    Article  PubMed  Google Scholar 

  • Bannerman D M, Rawlins J N, McHugh S B, Deacon R M, Yee B K, Bast T, Zhang W N, Pothuizen H H, Feldon J (2004). Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev, 28(3): 273–283

    Article  CAS  PubMed  Google Scholar 

  • Barraud P, Thompson L, Kirik D, Björklund A, Parmar M (2005). Isolation and characterization of neural precursor cells from the Sox1-GFP reporter mouse. Eur J Neurosci, 22(7): 1555–1569

    Article  PubMed  Google Scholar 

  • Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie D C, Beckers J, Yoder B, Irmler M, Götz M (2010). In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell, 7(6): 744–758

    Article  CAS  PubMed  Google Scholar 

  • Bendall S C, Davis K L, Amir A D, Tadmor M D, Simonds E F, Chen T J, Shenfeld D K, Nolan G P, Pe’er D (2014). Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development. Cell, 157(3): 714–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benner E J, Luciano D, Jo R, Abdi K, Paez-Gonzalez P, Sheng H, Warner D S, Liu C, Eroglu C, Kuo C T (2013). Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. Nature, 497(7449): 369–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentivoglio M, Mazzarello P (1999). The history of radial glia. Brain Res Bull, 49(5): 305–315

    Article  CAS  PubMed  Google Scholar 

  • Bergmann O, Liebl J, Bernard S, Alkass K, Yeung M S, Steier P, Kutschera W, Johnson L, Landén M, Druid H, Spalding K L, Frisén J (2012). The age of olfactory bulb neurons in humans. Neuron, 74(4): 634–639

    Article  CAS  PubMed  Google Scholar 

  • Bernier P J, Bedard A, Vinet J, Levesque M, Parent A (2002). Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA, 99(17): 11464–11469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhardwaj R D, Curtis M A, Spalding K L, Buchholz B A, Fink D, Björk-Eriksson T, Nordborg C, Gage F H, Druid H, Eriksson P S, Frisén J (2006). Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci USA, 103(33): 12564–12568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bignami A, Dahl D (1974). Astrocyte-specific protein and radial glia in the cerebral cortex of newborn rat. Nature, 252(5478): 55–56

    Article  CAS  PubMed  Google Scholar 

  • Bignami A, Eng L F, Dahl D, Uyeda C T (1972). Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res, 43(2): 429–435

    Article  CAS  PubMed  Google Scholar 

  • Breton-Provencher V, Lemasson M, Peralta M R 3rd, Saghatelyan A (2009). Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci, 29(48): 15245–15257

    Article  CAS  PubMed  Google Scholar 

  • Briscoe J, Sussel L, Serup P, Hartigan-O’Connor D, Jessell T M, Rubenstein J L, Ericson J (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature, 398(6728): 622–627

    Article  CAS  PubMed  Google Scholar 

  • Brown K N, Chen S, Han Z, Lu C H, Tan X, Zhang X J, Ding L, Lopez-Cruz A, Saur D, Anderson S A, Huang K, Shi S H (2011). Clonal production and organization of inhibitory interneurons in the neocortex. Science, 334(6055): 480–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brus M, Meurisse M, Gheusi G, Keller M, Lledo P M, Lévy F (2013). Dynamics of olfactory and hippocampal neurogenesis in adult sheep. J Comp Neurol, 521(1): 169–188

    Article  CAS  PubMed  Google Scholar 

  • Burns K A, Ayoub A E, Breunig J J, Adhami F, Weng W L, Colbert M C, Rakic P, Kuan C Y (2007). Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia hypoxia. Cereb Cortex, 17(11): 2585–2592

    Article  PubMed  Google Scholar 

  • Calaora V, Chazal G, Nielsen P J, Rougon G, Moreau H (1996). mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience, 73(2): 581–594

    Article  CAS  PubMed  Google Scholar 

  • Calzolari F, Michel J, Baumgart E V, Theis F, Götz M, Ninkovic J (2015). Fast clonal expansion and limited neural stem cell selfrenewal in the adult subependymal zone. Nat Neurosci, 18(4): 490–492

    Article  CAS  PubMed  Google Scholar 

  • Cameron H A, McKay R D (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol, 435 (4): 406–417

    Article  CAS  PubMed  Google Scholar 

  • Cameron R S, Rakic P (1991). Glial cell lineage in the cerebral cortex: a review and synthesis. Glia, 4(2): 124–137

    Article  CAS  PubMed  Google Scholar 

  • Campbell K (2003). Dorsal-ventral patterning in the mammalian telencephalon. Curr Opin Neurobiol, 13(1): 50–56

    Article  CAS  PubMed  Google Scholar 

  • Capela A, Temple S (2002). LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron, 35(5): 865–875

    Article  PubMed  Google Scholar 

  • Chanas-Sacré G, Thiry M, Pirard S, Rogister B, Moonen G, Mbebi C, Verdière-Sahuqué M, Leprince P (2000). A 295-kDA intermediate filament-associated protein in radial glia and developing muscle cells in vivo and in vitro. Dev Dyn, 219(4): 514–525

    Article  PubMed  Google Scholar 

  • Chen X, Lepier A, Berninger B, Tolkovsky A M, Herbert J (2012). Cultured subventricular zone progenitor cells transduced with neurogenin-2 become mature glutamatergic neurons and integrate into the dentate gyrus. PLoS ONE, 7(2): e31547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christian K M, Song H, Ming G L (2014). Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci, 37(1): 243–262

    Article  CAS  PubMed  Google Scholar 

  • Chuong C M, Edelman G M (1984). Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci, 4(9): 2354–2368

    CAS  PubMed  Google Scholar 

  • Codega P, Silva-Vargas V, Paul A, Maldonado-Soto A R, Deleo A M, Pastrana E, Doetsch F (2014). Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron, 82(3): 545–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corti S, Nizzardo M, Nardini M, Donadoni C, Locatelli F, Papadimitriou D, Salani S, Del Bo R, Ghezzi S, Strazzer S, Bresolin N, Comi G P (2007). Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol, 205 (2): 547–562

    Article  CAS  PubMed  Google Scholar 

  • Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti J C, Hutnick L, Krueger R C Jr, Fan G, de Vellis J, Sun Y E (2008). CD133 + neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA, 105(3): 1026–1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curtis M A, Kam M, Nannmark U, Anderson M F, Axell M Z, Wikkelso C, Holtås S, van Roon-Mom W M, Björk-Eriksson T, Nordborg C, Frisén J, Dragunow M, Faull R L, Eriksson P S (2007). Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science, 315(5816): 1243–1249

    Article  CAS  PubMed  Google Scholar 

  • Dahl D, Rueger D C, Bignami A, Weber K, Osborn M (1981). Vimentin, the 57 000 molecular weight protein of fibroblast filaments, is the major cytoskeletal component in immature glia. Eur J Cell Biol, 24 (2): 191–196

    CAS  PubMed  Google Scholar 

  • Davis A A, Temple S (1994). A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature, 372(6503): 263–266

    Article  CAS  PubMed  Google Scholar 

  • Dayer A G, Cleaver K M, Abouantoun T, Cameron H A (2005). New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol, 168(3): 415–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daynac M, Morizur L, Kortulewski T, Gauthier L R, Ruat M, Mouthon M A, Boussin F D (2015). Cell Sorting of Neural Stem and Progenitor Cells from the Adult Mouse Subventricular Zone and Live-imaging of their Cell Cycle Dynamics. J Vis Exp, (103)

  • De Marchis S, Bovetti S, Carletti B, Hsieh Y C, Garzotto D, Peretto P, Fasolo A, Puche A C, Rossi F (2007). Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci, 27(3): 657–664

    Article  PubMed  CAS  Google Scholar 

  • Delgado R N, Lim D A (2015). Embryonic Nkx2.1-expressing neural precursor cells contribute to the regional heterogeneity of adult VSVZ neural stem cells. Dev Biol, 407(2): 265–274

    Article  CAS  PubMed  Google Scholar 

  • Deng W, Aimone J B, Gage F H (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci, 11(5): 339–350

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, Møllgård K, Belin M F (1986). Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, nonspecialized ventricular ependyma and adjacent neuropil. Cell Tissue Res, 245(2): 343–351

    Article  CAS  PubMed  Google Scholar 

  • Doetsch F (2003). The glial identity of neural stem cells. Nat Neurosci, 6 (11): 1127–1134

    Article  CAS  PubMed  Google Scholar 

  • Doetsch F, Alvarez-Buylla A (1996). Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA, 93(25): 14895–14900

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Doetsch F, Caillé I, Lim D A, García-Verdugo J M, Alvarez-Buylla A (1999a). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97(6): 703–716

    Article  CAS  PubMed  Google Scholar 

  • Doetsch F, García-Verdugo J M, Alvarez-Buylla A (1997). Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci, 17(13): 5046–5061

    CAS  PubMed  Google Scholar 

  • Doetsch F, García-Verdugo J M, Alvarez-Buylla A (1999b). Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA, 96(20): 11619–11624

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Doetsch F, Petreanu L, Caille I, Garcia-Verdugo J M, Alvarez-Buylla A (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron, 36(6): 1021–1034

    Article  CAS  PubMed  Google Scholar 

  • Edwards M A, Yamamoto M, Caviness V S Jr (1990). Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience, 36(1): 121–144

    CAS  PubMed  Google Scholar 

  • Egger V, Urban N N (2006). Dynamic connectivity in the mitral cellgranule cell microcircuit. Semin Cell Dev Biol, 17(4): 424–432

    Article  PubMed  Google Scholar 

  • Ehninger D, Kempermann G (2003). Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex, 13(8): 845–851

    Article  PubMed  Google Scholar 

  • Ellis P, Fagan B M, Magness S T, Hutton S, Taranova O, Hayashi S, McMahon A, Rao M, Pevny L (2004). SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci, 26(2-4): 148–165

    Article  CAS  PubMed  Google Scholar 

  • Englund C, Fink A, Lau C, Pham D, Daza R A, Bulfone A, Kowalczyk T, Hevner R F (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci, 25(1): 247–251

    Article  CAS  PubMed  Google Scholar 

  • Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004). Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci, 24(38): 8354–8365

    Article  CAS  PubMed  Google Scholar 

  • Ericson J, Briscoe J, Rashbass P, van Heyningen V, Jessell T M (1997a). Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb Symp Quant Biol, 62(1): 451–466

    Article  CAS  PubMed  Google Scholar 

  • Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell T M, Briscoe J (1997b). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell, 90(1): 169–180

    Article  CAS  PubMed  Google Scholar 

  • Eriksson P S, Perfilieva E, Björk-Eriksson T, Alborn A M, Nordborg C, Peterson D A, Gage F H (1998). Neurogenesis in the adult human hippocampus. Nat Med, 4(11): 1313–1317

    Article  CAS  PubMed  Google Scholar 

  • Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisén J (2014). Neurogenesis in the striatum of the adult human brain. Cell, 156(5): 1072–1083

    Article  CAS  PubMed  Google Scholar 

  • Fan G, Martinowich K, Chin M H, He F, Fouse S D, Hutnick L, Hattori D, Ge W, Shen Y, Wu H, ten Hoeve J, Shuai K, Sun Y E (2005). DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development, 132(15): 3345–3356

    Article  CAS  PubMed  Google Scholar 

  • Fanselow M S, Dong H W (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1): 7–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feliciano D M, Bordey A (2013). Newborn cortical neurons: only for neonates? Trends Neurosci, 36(1): 51–61

    Article  CAS  PubMed  Google Scholar 

  • Feng L, Hatten M E, Heintz N (1994). Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron, 12(4): 895–908

    Article  CAS  PubMed  Google Scholar 

  • Ferri A L, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi P P, Sala M, De Biasi S, Nicolis S K (2004). Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development, 131(15): 3805–3819

    Article  CAS  PubMed  Google Scholar 

  • Florio M, Albert M, Taverna E, Namba T, Brandl H, Lewitus E, Haffner C, Sykes A, Wong F K, Peters J, Guhr E, Klemroth S, Prüfer K, Kelso J, Naumann R, Nüsslein I, Dahl A, Lachmann R, Pääbo S, Huttner W B (2015). Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science, 347 (6229). 1465–1470

    Article  CAS  PubMed  Google Scholar 

  • Frantz G D, McConnell S K (1996). Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron, 17(1): 55–61

    Article  CAS  PubMed  Google Scholar 

  • Fuccillo M, Joyner A L, Fishell G (2006). Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat Rev Neurosci, 7(10): 772–783

    Article  CAS  PubMed  Google Scholar 

  • Fuentealba L C, Obernier K, Alvarez-Buylla A (2012). Adult neural stem cells bridge their niche. Cell Stem Cell, 10(6): 698–708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentealba L C, Rompani S B, Parraguez J I, Obernier K, Romero R, Cepko C L, Alvarez-Buylla A (2015). Embryonic Origin of Postnatal Neural Stem Cells. Cell, 161(7): 1644–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gage F H (2002). Neurogenesis in the adult brain. J Neurosci, 22(3): 612–613

    CAS  PubMed  Google Scholar 

  • Galileo D S, Gray G E, Owens G C, Majors J, Sanes J R (1990). Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-specific antibodies. Proc Natl Acad Sci USA, 87(1): 458–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia A D, Doan N B, Imura T, Bush T G, Sofroniew M V (2004). GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci, 7(11): 1233–1241

    Article  CAS  PubMed  Google Scholar 

  • Garner C C, Brugg B, Matus A (1988). A 70-kilodalton microtubuleassociated protein (MAP2c), related to MAP2. J Neurochem, 50(2): 609–615

    Article  CAS  PubMed  Google Scholar 

  • Giachino C, Basak O, Lugert S, Knuckles P, Obernier K, Fiorelli R, Frank S, Raineteau O, Alvarez-Buylla A, Taylor V (2014). Molecular diversity subdivides the adult forebrain neural stem cell population. Stem Cells, 32(1): 70–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gil-Perotín S, Alvarez-Buylla A, García-Verdugo J M (2009). Identification and characterization of neural progenitor cells in the adult mammalian brain. Adv Anat Embryol Cell Biol, 203: 1–101, ix (ix.)

    Article  PubMed  Google Scholar 

  • Gleeson J G, Lin P T, Flanagan L A, Walsh C A (1999). Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23(2): 257–271

    Article  CAS  PubMed  Google Scholar 

  • Goldman S A, Nottebohm F (1983). Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA, 80(8): 2390–2394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golds E E, Braun P E (1976). Organization of membrane proteins in the intact myelin sheath. Pyridoxal phosphate and salicylaldehyde as probes of myelin structure. J Biol Chem, 251(15): 4729–4735

    CAS  PubMed  Google Scholar 

  • Gonzales-Roybal G, Lim D A (2013). Chromatin-based epigenetics of adult subventricular zone neural stem cells. Front Genet, 4: 194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonzalez-Perez O, Alvarez-Buylla A (2011). Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Brain Res Rev, 67(1-2): 147–156

    Article  CAS  Google Scholar 

  • Gonzalez-Perez O, Quiñones-Hinojosa A (2010). Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia, 58(8): 975–983

    PubMed  PubMed Central  Google Scholar 

  • Götz M, Stoykova A, Gruss P (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron, 21(5): 1031–1044

    Article  PubMed  Google Scholar 

  • Gould E, Vail N, Wagers M, Gross C G (2001). Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA, 98(19): 10910–10917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerrero-Cázares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, García-Verdugo J M, Quinoñes-Hinojosa A (2011). Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol, 519(6): 1165–1180

    Article  PubMed  Google Scholar 

  • Guillemot F (2005). Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol, 17(6): 639–647

    Article  CAS  PubMed  Google Scholar 

  • Hack M A, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo P M, Götz M (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci, 8(7): 865–872

    Article  CAS  PubMed  Google Scholar 

  • Hall A, Giese N A, Richardson W D (1996). Spinal cord oligodendrocytes develop from ventrally derived progenitor cells that express PDGF alpha-receptors. Development, 122(12): 4085–4094

    CAS  PubMed  Google Scholar 

  • Hansen D V, Lui J H, Parker P R, Kriegstein A R (2010). Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature, 464(7288): 554–561

    Article  CAS  PubMed  Google Scholar 

  • Hart I K, Richardson W D, Heldin C H, Westermark B, Raff M C (1989). PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development, 105(3): 595–603

    CAS  PubMed  Google Scholar 

  • Hartfuss E, Galli R, Heins N, Götz M (2001). Characterization of CNS precursor subtypes and radial glia. Dev Biol, 229(1): 15–30

    Article  CAS  PubMed  Google Scholar 

  • Harwell C C, Fuentealba L C, Gonzalez-Cerrillo A, Parker P R, Gertz C C, Mazzola E, Garcia M T, Alvarez-Buylla A, Cepko C L, Kriegstein A R (2015). Wide Dispersion and Diversity of Clonally Related Inhibitory Interneurons. Neuron, 87(5): 999–1007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haubensak W, Attardo A, Denk W, Huttner W B (2004). Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA, 101(9): 3196–3201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G, de Vellis J, Sun Y E (2005). A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci, 8(5): 616–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herholz K, Schopphoff H, Schmidt M, Mielke R, Eschner W, Scheidhauer K, Schicha H, Heiss W D, Ebmeier K (2002). Direct comparison of spatially normalized PET and SPECT scans in Alzheimer's disease. J Nucl Med, 43(1): 21–26

    PubMed  Google Scholar 

  • Herrera D G, Garcia-Verdugo J M, Alvarez-Buylla A (1999). Adultderived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol, 46(6): 867–877

    Article  CAS  PubMed  Google Scholar 

  • Hevner R F (2006). From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol, 33(1): 33–50

    Article  CAS  PubMed  Google Scholar 

  • Hevner R F, Hodge R D, Daza R A, Englund C (2006). Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res, 55 (3): 223–233

    Article  CAS  PubMed  Google Scholar 

  • His W (1904). Die Entwickelung des menschlichen Gehirns wahrend der esten Monte. Leipzig: Hirzel

    Google Scholar 

  • Hochstim C, Deneen B, Lukaszewicz A, Zhou Q, Anderson D J (2008). dentification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell, 133(3): 510–522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hockfield S, McKay R D (1985). Identification of major cell classes in the developing mammalian nervous system. J Neurosci, 5(12): 3310–3328

    CAS  PubMed  Google Scholar 

  • Huang L, De Vries G J, Bittman E L (1998). Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J Neurobiol, 36(3): 410–420

    Article  CAS  PubMed  Google Scholar 

  • Ihrie R A, Shah J K, Harwell C C, Levine J H, Guinto C D, Lezameta M, Kriegstein A R, Alvarez-Buylla A (2011). Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron, 71(2): 250–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ihrie R A, Alvarez-Buylla A (2009). Neural Stem Cells Disguised as Astrocytes. In: Astrocytes in (Patho)Physiology of the Nervous System, Parpura V, Haydon P G (Eds.). (Springer US), pp. 27–47

    Chapter  Google Scholar 

  • Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H, Miyachi H, Fujiwara T, Ishidate F, Kageyama R (2013). Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science, 342(6163): 1203–1208

    Article  CAS  PubMed  Google Scholar 

  • Imayoshi I, Sakamoto M, Kageyama R (2011). Genetic methods to identify and manipulate newly born neurons in the adult brain. Front Neurosci, 5: 64

    Article  PubMed  PubMed Central  Google Scholar 

  • Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci, 30(9): 3489–3498

    Article  CAS  PubMed  Google Scholar 

  • Imura T, Kornblum H I, Sofroniew M V (2003). The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci, 23(7): 2824–2832

    CAS  PubMed  Google Scholar 

  • Inta D, Alfonso J, von Engelhardt J, Kreuzberg M M, Meyer A H, van Hooft J A, Monyer H (2008). Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA, 105(52): 20994–20999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irvin D K, Nakano I, Paucar A, Kornblum H I (2004). Patterns of Jagged1, Jagged2, Delta-like 1 and Delta-like 3 expression during late embryonic and postnatal brain development suggest multiple functional roles in progenitors and differentiated cells. J Neurosci Res, 75(3): 330–343

    Article  CAS  PubMed  Google Scholar 

  • Isaacson J S, Strowbridge B W (1998). Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron, 20(4): 749–761

    Article  CAS  PubMed  Google Scholar 

  • Jackson E L, Alvarez-Buylla A (2008). Characterization of adult neural stem cells and their relation to brain tumors. Cells Tissues Organs, 188(1-2): 212–224

    Article  PubMed  Google Scholar 

  • Johe K K, Hazel T G, Muller T, Dugich-Djordjevic M M, McKay R D (1996). Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev, 10(24): 3129–3140

    Article  CAS  PubMed  Google Scholar 

  • Kaplan M S, Hinds J W (1977). Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science, 197(4308): 1092–1094

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, Akamatsu W, Ogawa M, Okabe M, Tano Y, Goldman S A, Okano H (2001). Nestin-EGFP transgenic mice: visualization of the selfrenewal and multipotency of CNS stem cells. Mol Cell Neurosci, 17 (2): 259–273

    Article  CAS  PubMed  Google Scholar 

  • Kirino T, Brightman M W, Oertel W H, Schmechel D E, Marangos P J (1983). Neuron-specific enolase as an index of neuronal regeneration and reinnervation. J Neurosci, 3(5): 915–923

    CAS  PubMed  Google Scholar 

  • Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A (1999). Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci, 19(6): 2171–2180

    CAS  PubMed  Google Scholar 

  • Kohwi M, Osumi N, Rubenstein J L, Alvarez-Buylla A (2005). Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci, 25(30): 6997–7003

    Article  CAS  PubMed  Google Scholar 

  • Kohwi M, Petryniak M A, Long J E, Ekker M, Obata K, Yanagawa Y, Rubenstein J L, Alvarez-Buylla A (2007). A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci, 27(26): 6878–6891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kokovay E, Goderie S, Wang Y, Lotz S, Lin G, Sun Y, Roysam B, Shen Q, Temple S (2010). Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell, 7(2): 163–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kokovay E, Wang Y, Kusek G, Wurster R, Lederman P, Lowry N, Shen Q, Temple S (2012). VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. Cell Stem Cell, 11(2): 220–230

    Article  CAS  PubMed  Google Scholar 

  • Kopan R, Ilagan M X G (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell, 137(2): 216–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornack D R, Rakic P (2001a). Cell proliferation without neurogenesis in adult primate neocortex. Science, 294(5549): 2127–2130

    Article  CAS  PubMed  Google Scholar 

  • Kornack D R, Rakic P (2001b). The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA, 98(8): 4752–4757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosaka K, Aika Y, Toida K, Heizmann C W, Hunziker W, Jacobowitz D M, Nagatsu I, Streit P, Visser T J, Kosaka T (1995). Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res, 23(1): 73–88

    Article  CAS  PubMed  Google Scholar 

  • Kosaka K, Kosaka T (2005). synaptic organization of the glomerulus in the main olfactory bulb: compartments of the glomerulus and heterogeneity of the periglomerular cells. Anat Sci Int, 80(2): 80–90

    Article  PubMed  Google Scholar 

  • Kriegstein A, Alvarez-Buylla A (2009). The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci, 32(1): 149–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kriegstein A R, Götz M (2003). Radial glia diversity: a matter of cell fate. Glia, 43(1): 37–43

    Article  PubMed  Google Scholar 

  • Laywell E D, Rakic P, Kukekov V G, Holland E C, Steindler D A (2000). Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA, 97(25): 13883–13888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazarini F, Mouthon M A, Gheusi G, de Chaumont F, Olivo-Marin J C, Lamarque S, Abrous D N, Boussin F D, Lledo P M (2009). Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS ONE, 4(9): e7017

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lehtinen M K, Zappaterra M W, Chen X, Yang Y J, Hill A D, Lun M, Maynard T, Gonzalez D, Kim S, Ye P, D’Ercole A J, Wong E T, La Mantia A S, Walsh C A (2011). The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron, 69(5): 893–905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lendahl U, Zimmerman L B, McKay R D (1990). CNS stem cells express a new class of intermediate filament protein. Cell, 60(4): 585–595

    Article  CAS  PubMed  Google Scholar 

  • Lepousez G, Valley M T, Lledo P M (2013). The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol, 75(1): 339–363

    Article  CAS  PubMed  Google Scholar 

  • Levine J H, Simonds E F, Bendall S C, Davis K L, Amir A D, Tadmor M D, Litvin O, Fienberg H G, Jager A, Zunder E R, Finck R, Gedman A L, Radtke I, Downing J R, Pe’er D, Nolan G P (2015). Data-Driven Phenotypic Dissection of AML Reveals Progenitor-like Cells that Correlate with Prognosis. Cell, 162(1): 184–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeVine S M, Goldman J E (1988a). Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci, 8(11): 3992–4006

    CAS  PubMed  Google Scholar 

  • LeVine S M, Goldman J E (1988b). Ultrastructural characteristics of GD3 ganglioside-positive immature glia in rat forebrain white matter. J Comp Neurol, 277(3): 456–464

    Article  CAS  PubMed  Google Scholar 

  • Levitt P, Cooper M L, Rakic P (1981). Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J Neurosci, 1(1): 27–39

    CAS  PubMed  Google Scholar 

  • Li G, Fang L, Fernández G, Pleasure S J (2013). The ventral hippocampus is the embryonic origin for adult neural stem cells in the dentate gyrus. Neuron, 78(4): 658–672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Clevers H (2010). Coexistence of quiescent and active adult stem cells in mammals. Science, 327(5965): 542–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Sun C, Lin C, Ma T, Madhavan M C, Campbell K, Yang Z (2011). The transcription factor Sp8 is required for the production of parvalbumin-expressing interneurons in the olfactory bulb. J Neurosci, 31(23): 8450–8455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim D A, Alvarez-Buylla A (1999). Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci USA, 96(13): 7526–7531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim D A, Alvarez-Buylla A (2016). The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis. Cold Spring Harb Perspect Biol, 8(5): 8

    Article  Google Scholar 

  • Lim D A, Huang Y C, Swigut T, Mirick A L, Garcia-Verdugo J M, Wysocka J, Ernst P, Alvarez-Buylla A (2009). Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature, 458(7237): 529–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu F, You Y, Li X, Ma T, Nie Y, Wei B, Li T, Lin H, Yang Z (2009). Brain injury does not alter the intrinsic differentiation potential of adult neuroblasts. J Neurosci, 29(16): 5075–5087

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Han S S, Wu Y, Tuohy T M, Xue H, Cai J, Back S A, Sherman L S, Fischer I, Rao M S (2004). CD44 expression identifies astrocyterestricted precursor cells. Dev Biol, 276(1): 31–46

    Article  CAS  PubMed  Google Scholar 

  • Livneh Y, Adam Y, Mizrahi A (2014). Odor processing by adult-born neurons. Neuron, 81(5): 1097–1110

    Article  CAS  PubMed  Google Scholar 

  • Lledo P M, Alonso M, Grubb M S (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci, 7(3): 179–193

    Article  CAS  PubMed  Google Scholar 

  • Llorens-Bobadilla E, Zhao S, Baser A, Saiz-Castro G, Zwadlo K, Martin-Villalba A (2015). Single-Cell Transcriptomics Reveals a Population of Dormant Neural Stem Cells that Become Activated upon Brain Injury. Cell Stem Cell, 17(3): 329–340

    Article  CAS  PubMed  Google Scholar 

  • Lois C, Alvarez-Buylla A (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA, 90(5): 2074–2077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lois C, García-Verdugo J M, Alvarez-Buylla A (1996). Chain migration of neuronal precursors. Science, 271(5251): 978–981

    Article  CAS  PubMed  Google Scholar 

  • Long J E, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein J L (2007). Dlx-dependent and-independent regulation of olfactory bulb interneuron differentiation. J Neurosci, 27(12): 3230–3243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Longe O, Senior C, Rippon G (2009). The lateral and ventromedial prefrontal cortex work as a dynamic integrated system: evidence from FMRI connectivity analysis. J Cogn Neurosci, 21(1): 141–154

    Article  PubMed  Google Scholar 

  • Low V F, Faull R L, Bennet L, Gunn A J, Curtis M A (2013). Neurogenesis and progenitor cell distribution in the subgranular zone and subventricular zone of the adult sheep brain. Neuroscience, 244: 173–187

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Daniels S B, Lennington J B, Notti R Q, Conover J C (2006). The aging neurogenic subventricular zone. Aging Cell, 5(2): 139–152

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Coskun V, Liang A, Yu J, Cheng L, Ge W, Shi Z, Zhang K, Li C, Cui Y, Lin H, Luo D, Wang J, Lin C, Dai Z, Zhu H, Zhang J, Liu J, Liu H, de Vellis J, Horvath S, Sun Y E, Li S (2015). Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells. Cell, 161(5): 1175–1186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luzzati F, Peretto P, Aimar P, Ponti G, Fasolo A, Bonfanti L (2003). Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci USA, 100(22): 13036–13041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marzesco A M, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner W B (2005). Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci, 118(Pt 13): 2849–2858

    Article  CAS  PubMed  Google Scholar 

  • Maslov A Y, Barone T A, Plunkett R J, Pruitt S C (2004). Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci, 24(7): 1726–1733

    Article  CAS  PubMed  Google Scholar 

  • Maurice A (2007). Response to Comment on “Human Neuroblasts Migrate to the Olfactory Bulb via a Lateral Ventricular Extension”. Science, 318(5849): 393c

    Article  CAS  Google Scholar 

  • Mayer C, Jaglin X H, Cobbs L V, Bandler R C, Streicher C, Cepko C L, Hippenmeyer S, Fishell G (2015). Clonally Related Forebrain Interneurons Disperse Broadly across Both Functional Areas and Structural Boundaries. Neuron, 87(5): 989–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCarthy M, Turnbull D H, Walsh C A, Fishell G (2001). Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci, 21(17): 6772–6781

    CAS  PubMed  Google Scholar 

  • McDermott K W, Lantos P L (1989). The distribution of glial fibrillary acidic protein and vimentin in postnatal marmoset (Callithrix jacchus) brain. Brain Res Dev Brain Res, 45(2): 169–177

    Article  CAS  PubMed  Google Scholar 

  • McDermott K W, Lantos P L (1990). Cell proliferation in the subependymal layer of the postnatal marmoset, Callithrix jacchus. Brain Res Dev Brain Res, 57(2): 269–277

    Article  CAS  PubMed  Google Scholar 

  • McMahon A P, Ingham P W, Tabin C J (2003). Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol, 53: 1–114

    Article  CAS  PubMed  Google Scholar 

  • Menn B, Garcia-Verdugo J M, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006). Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci, 26(30): 7907–7918

    Article  CAS  PubMed  Google Scholar 

  • Merkle F T, Fuentealba L C, Sanders T A, Magno L, Kessaris N, Alvarez-Buylla A (2014). Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci, 17(2): 207–214

    Article  CAS  PubMed  Google Scholar 

  • Merkle F T, Mirzadeh Z, Alvarez-Buylla A (2007). Mosaic organization of neural stem cells in the adult brain. Science, 317(5836): 381–384

    Article  CAS  PubMed  Google Scholar 

  • Merkle F T, Tramontin A D, García-Verdugo J M, Alvarez-Buylla A (2004). Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA, 101(50): 17528–17532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mich J K, Signer R A, Nakada D, Pineda A, Burgess R J, Vue T Y, Johnson J E, Morrison S J (2014). Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. eLife, 3: e02669

    Article  PubMed  PubMed Central  Google Scholar 

  • Milosevic A, Noctor S C, Martinez-Cerdeno V, Kriegstein A R, Goldman J E (2008). Progenitors from the postnatal forebrain subventricular zone differentiate into cerebellar-like interneurons and cerebellar-specific astrocytes upon transplantation. Mol Cell Neurosci, 39(3): 324–334

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mirzadeh Z, Merkle F T, Soriano-Navarro M, Garcia-Verdugo J M, Alvarez-Buylla A (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell, 3(3): 265–278

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Misson J P, Edwards M A, Yamamoto M, Caviness V S Jr (1988). Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Brain Res Dev Brain Res, 44(1): 95–108

    Article  CAS  PubMed  Google Scholar 

  • Molofsky A V, Slutsky S G, Joseph N M, He S, Pardal R, Krishnamurthy J, Sharpless N E, Morrison S J (2006). Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature, 443(7110): 448–452

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Molyneaux B J, Arlotta P, Menezes J R, Macklis J D (2007). Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci, 8(6): 427–437

    Article  CAS  PubMed  Google Scholar 

  • Moreno M M, Linster C, Escanilla O, Sacquet J, Didier A, Mandairon N (2009). Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci USA, 106(42): 17980–17985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori T, Buffo A, Götz M (2005). The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol, 69: 67–99

    Article  CAS  PubMed  Google Scholar 

  • Morshead C M, Garcia A D, Sofroniew M V, van Der Kooy D (2003). The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur J Neurosci, 18(1): 76–84

    Article  PubMed  Google Scholar 

  • Morshead C M, Reynolds B A, Craig C G, McBurney M W, Staines W A, Morassutti D, Weiss S, van der Kooy D (1994). Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron, 13(5): 1071–1082

    Article  CAS  PubMed  Google Scholar 

  • Mullen R J, Buck C R, Smith A M (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116(1): 201–211

    CAS  PubMed  Google Scholar 

  • Nedelec J, Pierres M, Moreau H, Barbet J, Naquet P, Faivre-Sarrailh C, Rougon G (1992). Isolation and characterization of a novel glycosylphosphatidylinositol- anchored glycoconjugate expressed by developing neurons. Eur J Biochem, 203(3): 433–442

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama A, Lin X H, Giese N, Heldin C H, Stallcup W B (1996). Colocalization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res, 43(3): 299–314

    Article  CAS  PubMed  Google Scholar 

  • Nissant A, Bardy C, Katagiri H, Murray K, Lledo P M (2009). Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci, 12(6): 728–730

    Article  CAS  PubMed  Google Scholar 

  • Niu W, Zang T, Zou Y, Fang S, Smith D K, Bachoo R, Zhang C L (2013). In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol, 15(10): 1164–1175

    Article  CAS  PubMed  Google Scholar 

  • Noctor S C, Flint A C, Weissman T A, Wong W S, Clinton B K, Kriegstein A R (2002). Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci, 22(8): 3161–3173

    CAS  PubMed  Google Scholar 

  • Noctor S C, Martínez-Cerdeño V, Ivic L, Kriegstein A R (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci, 7(2): 136–144

    Article  CAS  PubMed  Google Scholar 

  • Noctor S C, Martinez-Cerdeno, V, Kriegstein A R (2007). Neural stem and progenitor cells in cortical development. Novartis Found Symp, 288: 59–73; discussion 73–58, 96–58

    Article  CAS  PubMed  Google Scholar 

  • Noctor S C, Martínez-Cerdeño V, Kriegstein A R (2008). Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol, 508(1): 28–44

    Article  PubMed  PubMed Central  Google Scholar 

  • Omlin F X, Webster H D, Palkovits C G, Cohen S R (1982). Immunocytochemical localization of basic protein in major dense line regions of central and peripheral myelin. J Cell Biol, 95(1): 242–248

    Article  CAS  PubMed  Google Scholar 

  • Ong W Y, Levine J M (1999). A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience, 92(1): 83–95

    Article  CAS  PubMed  Google Scholar 

  • Paez-Gonzalez P, Abdi K, Luciano D, Liu Y, Soriano-Navarro M, Rawlins E, Bennett V, Garcia-Verdugo J M, Kuo C T (2011). Ank3- dependent SVZ niche assembly is required for the continued production of new neurons. Neuron, 71(1): 61–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paredes M F, Sorrells S F, Garcia-Verdugo J M, Alvarez-Buylla A (2016). Brain size and limits to adult neurogenesis. J Comp Neurol, 524(3): 646–664

    Article  PubMed  Google Scholar 

  • Parras C M, Galli R, Britz O, Soares S, Galichet C, Battiste J, Johnson J E, Nakafuku M, Vescovi A, Guillemot F (2004). Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J, 23 (22): 4495–4505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pastrana E, Cheng L C, Doetsch F (2009). Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA, 106(15): 6387–6392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pencea V, Bingaman K D, Freedman L J, Luskin M B (2001). Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol, 172(1): 1–16

    Article  CAS  PubMed  Google Scholar 

  • Peretto P, Merighi A, Fasolo A, Bonfanti L (1997). Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull, 42(1): 9–21

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Martín M, Cifuentes M, Grondona J M, Bermúdez-Silva F J, Arrabal P M, Pérez-Fígares J M, Jiménez A J, García-Segura L M, Férnandez-Llebrez P, Fernandez-Llebrez P, the P. Fernández-Llebrez (2003). Neurogenesis in explants from the walls of the lateral ventricle of adult bovine brain: role of endogenous IGF-1 as a survival factor. Eur J Neurosci, 17(2): 205–211

    Article  PubMed  Google Scholar 

  • Petreanu L, Alvarez-Buylla A (2002). Maturation and death of adultborn olfactory bulb granule neurons: role of olfaction. J Neurosci, 22 (14): 6106–6113

    CAS  PubMed  Google Scholar 

  • Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, Liblau R, Pham-Dinh D, Baron-Van Evercooren A (2002). Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci USA, 99(20): 13211–13216

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pilaz L J, McMahon J J, Miller E E, Lennox A L, Suzuki A, Salmon E, Silver D L (2016). Prolonged Mitosis of Neural Progenitors Alters Cell Fate in the Developing Brain. Neuron, 89(1): 83–99

    Article  CAS  PubMed  Google Scholar 

  • Pinto L, Mader M T, Irmler M, Gentilini M, Santoni F, Drechsel D, Blum R, Stahl R, Bulfone A, Malatesta P, Beckers J, Götz M (2008). Prospective isolation of functionally distinct radial glial subtypes— lineage and transcriptome analysis. Mol Cell Neurosci, 38(1): 15–42

    Article  CAS  PubMed  Google Scholar 

  • Pixley S K, de Vellis J (1984). Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res, 317(2): 201–209

    Article  CAS  PubMed  Google Scholar 

  • Poduslo J F, Braun P E (1975). Topographical arrangement of membrane proteins in the intact myelin sheath. Lactoperoxidase incorproation of iodine into myelin surface proteins. J Biol Chem, 250(3): 1099–1105

    CAS  PubMed  Google Scholar 

  • Ponti G, Obernier K, Guinto C, Jose L, Bonfanti L, Alvarez-Buylla A (2013). Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc Natl Acad Sci USA, 110(11): E1045–E1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price J L, Powell T P (1970). The mitral and short axon cells of the olfactory bulb. J Cell Sci, 7(3): 631–651

    CAS  PubMed  Google Scholar 

  • Pringle N P, Mudhar H S, Collarini E J, Richardson W D (1992). PDGF receptors in the rat CNS: during late neurogenesis, PDGF alphareceptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development, 115(2): 535–551

    CAS  PubMed  Google Scholar 

  • Puelles L, Rubenstein J L (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci, 26(9): 469–476

    Article  CAS  PubMed  Google Scholar 

  • Purves D (2012). Neuroscience, 5th edn (Sunderland, Mass.: Sinauer Associates)

    Google Scholar 

  • Qian X, Goderie S K, Shen Q, Stern J H, Temple S (1998). Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development, 125(16): 3143–3152

    CAS  PubMed  Google Scholar 

  • Quarles R H, Trapp B D (1984). Localization of myelin-associated glycoprotein. J Neurochem, 43(6): 1773–1777

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1988). Specification of cerebral cortical areas. Science, 241 (4862). 170–176

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (2006). A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex, 16(Suppl 1): i3–i17

    Article  PubMed  Google Scholar 

  • Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan R C, Melton D A (2002). “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science, 298(5593): 597–600

    Article  CAS  PubMed  Google Scholar 

  • Ramos A D, Andersen R E, Liu S J, Nowakowski T J, Hong S J, Gertz C C, Salinas R D, Zarabi H, Kriegstein A R, Lim D A (2015). The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell, 16(4): 439–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid C B, Liang I, Walsh C (1995). Systematic widespread clonal organization in cerebral cortex. Neuron, 15(2): 299–310

    Article  CAS  PubMed  Google Scholar 

  • Reynolds B A, Weiss S (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255(5052): 1707–1710

    Article  CAS  PubMed  Google Scholar 

  • Roccio M, Schmitter D, Knobloch M, Okawa Y, Sage D, Lutolf M P (2013). Predicting stem cell fate changes by differential cell cycle progression patterns. Development, 140(2): 459–470

    Article  CAS  PubMed  Google Scholar 

  • Rochefort C, Gheusi G, Vincent J D, Lledo P M (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci, 22(7): 2679–2689

    CAS  PubMed  Google Scholar 

  • Rodríguez-Pérez L M, Pérez-Martín M, Jiménez A J, Fernández-Llebrez P (2003). Immunocytochemical characterisation of the wall of the bovine lateral ventricle. Cell Tissue Res, 314(3): 325–335

    Article  CAS  PubMed  Google Scholar 

  • Rougon G, Alterman L A, Dennis K, Guo X J, Kinnon C (1991). The murine heat-stable antigen: a differentiation antigen expressed in both the hematolymphoid and neural cell lineages. Eur J Immunol, 21 (6): 1397–1402

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto M, Ieki N, Miyoshi G, Mochimaru D, Miyachi H, Imura T, Yamaguchi M, Fishell G, Mori K, Kageyama R, Imayoshi I (2014a). Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning. J Neurosci, 34(17): 5788–5799

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto M, Kageyama R, Imayoshi I (2014b). The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci, 8: 121

    PubMed  PubMed Central  Google Scholar 

  • Samanta J, Grund E M, Silva H M, Lafaille J J, Fishell G, Salzer J L (2015). Inhibition of Gli1 mobilizes endogenous neural stem cells for remyelination. Nature, 526(7573): 448–452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanai N, Berger M S, Garcia-Verdugo J M, Alvarez-Buylla A (2007). Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science, 318(5849): 393, author reply 393

    Article  CAS  PubMed  Google Scholar 

  • Sanai N, Nguyen T, Ihrie R A, Mirzadeh Z, Tsai H H, Wong M, Gupta N, Berger M S, Huang E, Garcia-Verdugo J M, Rowitch D H, Alvarez-Buylla A (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature, 478(7369): 382–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanai N, Tramontin A D, Quiñones-Hinojosa A, Barbaro N M, Gupta N, Kunwar S, Lawton M T, McDermott M W, Parsa A T, Manuel-García Verdugo J, Berger M S, Alvarez-Buylla A (2004). Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427(6976): 740–744

    Article  CAS  PubMed  Google Scholar 

  • Sawamoto K, Hirota Y, Alfaro-Cervello C, Soriano-Navarro M, He X, Hayakawa-Yano Y, Yamada M, Hikishima K, Tabata H, Iwanami A, Nakajima K, Toyama Y, Itoh T, Alvarez-Buylla A, Garcia-Verdugo J M, Okano H (2011). Cellular composition and organization of the subventricular zone and rostral migratory stream in the adult and neonatal common marmoset brain. J Comp Neurol, 519(4): 690–713

    Article  PubMed  PubMed Central  Google Scholar 

  • Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin J A, Yamada M, Spassky N, Murcia N S, Garcia-Verdugo J M, Marin O, Rubenstein J L, Tessier-Lavigne M, Okano H, Alvarez-Buylla A (2006). New neurons follow the flow of cerebrospinal fluid in the adult brain. Science, 311(5761): 629–632

    Article  CAS  PubMed  Google Scholar 

  • Schmechel D E, Marangos P J (1983). Neuron specific enolase as a marker or differentiation in neurons and neuroendocine cells. In: McKelvey J, Ba J, ed. Current Methods in Cellular Neurobiology. New York: John Wiley & Sons. pp 1–62

    Google Scholar 

  • Schmechel D E, Rakic P (1979). A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol (Berl), 156(2): 115–152

    Article  CAS  Google Scholar 

  • Schnitzer J, Schachner M (1981). Characterization of isolated mouse cerebellar cell populations in vitro. J Neuroimmunol, 1(4): 457–470

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Goderie S K, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004). Endothelial cells stimulate selfrenewal and expand neurogenesis of neural stem cells. Science, 304 (5675). 1338–1340

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Wang Y, Kokovay E, Lin G, Chuang S M, Goderie S K, Roysam B, Temple S (2008). Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell, 3(3): 289–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y (1997). Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci, 17(23): 9212–9219

    CAS  PubMed  Google Scholar 

  • Shin J, Berg D A, Zhu Y, Shin J Y, Song J, Bonaguidi M A, Enikolopov G, Nauen D W, Christian K M, Ming G L, Song H (2015). Single- Cell RNA-Seq with Waterfall Reveals Molecular Cascades underlying Adult Neurogenesis. Cell Stem Cell, 17(3): 360–372

    Article  CAS  PubMed  Google Scholar 

  • Sidman R L, Miale I L, Feder N (1959). Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol, 1(4): 322–333

    Article  CAS  PubMed  Google Scholar 

  • Sohn J, Orosco L, Guo F, Chung S H, Bannerman P, Mills Ko E, Zarbalis K, Deng W, Pleasure D (2015). The subventricular zone continues to generate corpus callosum and rostral migratory stream astroglia in normal adult mice. J Neurosci, 35(9): 3756–3763

    Article  CAS  PubMed  Google Scholar 

  • Sommer I, Schachner M (1981). Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol, 83(2): 311–327

    Article  CAS  PubMed  Google Scholar 

  • Spalding K L, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner H B, Boström E, Westerlund I, Vial C, Buchholz B A, Possnert G, Mash D C, Druid H, Frisén J (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell, 153(6): 1219–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spassky N, Merkle F T, Flames N, Tramontin A D, García-Verdugo J M, Alvarez-Buylla A (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci, 25(1): 10–18

    Article  CAS  PubMed  Google Scholar 

  • Stallcup W B, Beasley L (1987). Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci, 7(9): 2737–2744

    CAS  PubMed  Google Scholar 

  • Stühmer T, Puelles L, Ekker M, Rubenstein J L (2002). Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex, 12(1): 75–85

    Article  PubMed  Google Scholar 

  • Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A (2010). Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J, 24(7). 2355–2363.

    Article  CAS  PubMed  Google Scholar 

  • Sunabori T, Tokunaga A, Nagai T, Sawamoto K, Okabe M, Miyawaki A, Matsuzaki Y, Miyata T, Okano H (2008). Cell-cycle-specific nestin expression coordinates with morphological changes in embryonic cortical neural progenitors. J Cell Sci, 121(Pt 8): 1204–1212

    Article  CAS  PubMed  Google Scholar 

  • Szatkowska I, Szymanska O, Grabowska A (2004). The role of the human ventromedial prefrontal cortex in memory for contextual information. Neurosci Lett, 364(2): 71–75

    Article  CAS  PubMed  Google Scholar 

  • Temple S (2001). The development of neural stem cells. Nature, 414 (6859). 112–117

    Article  CAS  PubMed  Google Scholar 

  • Tong C K, Fuentealba L C, Shah J K, Lindquist R A, Ihrie R A, Guinto C D, Rodas-Rodriguez J L, Alvarez-Buylla A (2015). A Dorsal SHHDependent Domain in the V-SVZ Produces Large Numbers of Oligodendroglial Lineage Cells in the Postnatal Brain. Stem Cell Rep, 5(4): 461–470

    Article  CAS  Google Scholar 

  • Uchida N, Buck D W, He D, Reitsma M J, Masek M, Phan T V, Tsukamoto A S, Gage F H, Weissman I L (2000). Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA, 97(26): 14720–14725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullensvang K, Lehre K P, Storm-Mathisen J, Danbolt N C (1997). Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci, 9(8): 1646–1655

    Article  CAS  PubMed  Google Scholar 

  • Ventura R E, Goldman J E (2007). Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci, 27(16): 4297–4302

    Article  CAS  PubMed  Google Scholar 

  • Voigt T (1989). Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol, 289(1): 74–88

    Article  CAS  PubMed  Google Scholar 

  • Waclaw R R, Allen Z J 2nd, Bell S M, Erdélyi F, Szabó G, Potter S S, Campbell K (2006). The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron, 49(4): 503–516

    Article  CAS  PubMed  Google Scholar 

  • Walker A S, Goings G E, Kim Y, Miller R J, Chenn A, Szele F G (2010). Nestin reporter transgene labels multiple central nervous system precursor cells. Neural Plast, 2010: 894374

    PubMed  Google Scholar 

  • Walsh C, Cepko C L (1988). Clonally related cortical cells show several migration patterns. Science, 241(4871): 1342–1345

    Article  CAS  PubMed  Google Scholar 

  • Walsh C, Cepko C L (1992). Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science, 255(5043): 434–440

    Article  CAS  PubMed  Google Scholar 

  • Walsh C, Cepko C L (1993). Clonal dispersion in proliferative layers of developing cerebral cortex. Nature, 362(6421): 632–635

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Liu F, Liu Y Y, Zhao C H, You Y, Wang L, Zhang J, Wei B, Ma T, Zhang Q, Zhang Y, Chen R, Song H, Yang Z (2011). Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res, 21(11): 1534–1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D D, Bordey A (2008). The astrocyte odyssey. Prog Neurobiol, 86 (4): 342–367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ware M L, Tavazoie S F, Reid C B, Walsh C A (1999). Coexistence of widespread clones and large radial clones in early embryonic ferret cortex. Cereb Cortex, 9(6): 636–645

    Article  CAS  PubMed  Google Scholar 

  • Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson A C, Reynolds B A (1996). Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci, 16(23): 7599–7609

    CAS  PubMed  Google Scholar 

  • Wichterle H, Garcia-Verdugo J M, Herrera D G, Alvarez-Buylla A (1999). Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci, 2(5): 461–466

    Article  CAS  PubMed  Google Scholar 

  • Willaime-Morawek S, Seaberg R M, Batista C, Labbé E, Attisano L, Gorski J A, Jones K R, Kam A, Morshead C M, van der Kooy D (2006). Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells. J Cell Biol, 175(1): 159–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young K M, Fogarty M, Kessaris N, Richardson W D (2007). Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci, 27(31): 8286–8296

    Article  CAS  PubMed  Google Scholar 

  • Zappaterra M D, Lisgo S N, Lindsay S, Gygi S P, Walsh C A, Ballif B A (2007). A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J Proteome Res, 6(9): 3537–3548

    Article  CAS  PubMed  Google Scholar 

  • Zappone M V, Galli R, Catena R, Meani N, De Biasi S, Mattei E, Tiveron C, Vescovi A L, Lovell-Badge R, Ottolenghi S, Nicolis S K (2000). Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development, 127(11): 2367–2382

    CAS  PubMed  Google Scholar 

  • Zecevic N (2004). Specific characteristic of radial glia in the human fetal telencephalon. Glia, 48(1): 27–35

    Article  PubMed  Google Scholar 

  • Zecevic N, Chen Y, Filipovic R (2005). Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol, 491(2): 109–122

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rebecca A. Ihrie.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rushing, G., Ihrie, R.A. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone. Front. Biol. 11, 261–284 (2016). https://doi.org/10.1007/s11515-016-1407-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11515-016-1407-1

Keywords

Navigation