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Frontiers in Biology

Front. Biol.    2016, Vol. 11 Issue (4) : 261-284     DOI: 10.1007/s11515-016-1407-1
Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone
Gabrielle Rushing1,Rebecca A. Ihrie2,*()
1. Program in Neuroscience, Vanderbilt University, Nashville, TN 37232, USA
2. Departments of Cancer Biology and Neurological Surgery, Vanderbilt University, Nashville, TN 37232, USA
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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.

Keywords ventricular-subventricular zone      neural stem cells      positional identity      single-cell      heterogeneity     
Corresponding Authors: Rebecca A. Ihrie   
Just Accepted Date: 17 June 2016   Online First Date: 08 July 2016    Issue Date: 30 August 2016
 Cite this article:   
Gabrielle Rushing,Rebecca A. Ihrie. Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone[J]. Front. Biol., 2016, 11(4): 261-284.
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Gabrielle Rushing
Rebecca A. Ihrie
Marker Cell type labeled Source
Alpha 6 integrin Activated B1 cells C cells Ramalho-Santos et al., 2002; Kokovay et al., 2010
Brain lipid binding protein (BLBP) Radial glia Activated B1 cells Feng et al., 1994; Doetsch, 2003; Kriegstein and Gotz, 2003Giachino et al., 2014
CD44 Astrocyte-restricted precursor cells Liu et al., 2004
Dlx2 C cells A cells Doetsch et al., 2002
Doublecortin (DCX) A cells Doetsch et al., 1999a; Gleeson et al., 1999
E-NCAM Neuronal-restricted precursors Chuong and Edelman, 1984
Epidermal growth factor receptor (EGFR) Activated B1 cells C cells Doetsch et al., 2002; Pastrana et al., 2009; Codega et al., 2014
GD3 Oligodendrocyte precursor cells LeVine and Goldman, 1988a, 1988b
Glial fibrillary acidic protein (GFAP) Neuroepithelial cells Radial glia B1 cells Mature astrocytes Bignami et al., 1972
Glutamate aspartate transporter (GLAST) Radial glia Shibata et al., 1997; Hartfuss et al., 2001; Doetsch, 2003; Kriegstein and Gotz, 2003
Mature astrocytes Shibata et al., 1997; Ullensvang et al., 1997
Activated B1 cells C cells Pastrana et al., 2009
ITGA6/CD49f B1 cells C cells Ramalho-Santos et al., 2002; Shen et al., 2008; Kokovay et al., 2010
LeX (CD15) B1 cells Capela and Temple, 2002
MAG Mature oligodendrocytes Quarles and Trapp, 1984
MAP2 Mature neurons Garner et al., 1988
Mash1 (Ascl1) Activated B cells Pastrana et al., 2009
C cells Parras et al., 2004; Pastrana et al., 2009
mCD24 (aka heat-stable antigen, HSA) E cells Calaora et al., 1996
A cells (transiently) Rougon et al., 1991; Nedelec et al., 1992; Calaora et al., 1996
Myelin basic protein (MBP) Mature oligodendrocytes Poduslo and Braun, 1975; Golds and Braun, 1976; Omlin et al., 1982
Nestin Neuroepithelial cells Lendahl et al., 1990
Ependymal cells Lendahl et al., 1990; Doetsch et al., 1997
Radial glia Hockfield and McKay, 1985
Activated B1 cells Codega et al., 2014
Neuronal nuclear antigen (NeuN) Mature neurons Mullen et al., 1992
Neuron-specific enolase (NSE) Mature neurons Kirino et al., 1983
NG2 Oligodendrocyte precursor cells Stallcup and Beasley, 1987; Nishiyama et al., 1996; Ong and Levine, 1999
O4 Mature oligodendrocytes Sommer and Schachner, 1981
Pax6 Cortical radial glia Gotz et al., 1998; Englund et al., 2005
Polysialylated neural cell adhesion molecule (PSA-NCAM) A cells Doetsch et al., 1997
Prominin-1 (CD133) Ependymal cells Coskun et al., 2008
Primary cilia of B1 cells Uchida et al., 2000; Marzesco et al., 2005; Pinto et al., 2008; Beckervordersandforth et al., 2010
Platelet-derived growth factor receptor α (PDGFRα) Oligodendrocyte precursor cells Hart et al., 1989; Pringle et al., 1992; Hall et al., 1996
RC1 Neuroepithelial cells Radial glia Edwards et al., 1990
RC2 Neuroepithelial cells Radial glia Misson et al., 1988; Chanas-Sacre et al., 2000; Hartfuss et al., 2001
SOX2 (SRY-Box 2) Embryonic NSCs (radial glia) Zappone et al., 2000
B1 cells Ellis et al., 2004; Ferri et al., 2004
S100-β Mature astrocytes (Not all astrocytes express it) Wang and Bordey, 2008
Ependymal cells Didier et al., 1986
Tbr1 Intermediate progenitor cells Englund et al., 2005; Hevner, 2006; Hevner et al., 2006
Tbr2 Mature neurons (cortex) Englund et al., 2005; Hevner, 2006; Hevner et al., 2006
Tuj1 (βIII Tubulin) A cells Doetsch et al., 1997; Pastrana et al., 2009
VCAM-1 Quiescent B1 cells Kokovay et al., 2012; Codega et al., 2014
Vimentin Radial glia Schnitzer and Schachner, 1981; Zecevic, 2004
Ependymal cells
Tab.1  Marker expression on cell types within the V-SVZ and its precursor regions
Fig.1  Development of the mouse ventricular-subventricular zone. Representative coronal sections of mouse brain at indicated developmental times are shown at top. Colors in the coronal sections represent domains of transcription factor expression within the developing V-SVZ. At bottom, representative schematics of developing V-SVZ corresponding to red box within the coronal section above. Note that the size of coronal sections and corresponding representative images of cell types are not to scale. (A) Neuroepithelial cells (NECs; dark blue) fold in to form the neural tube. These cells contact both the pial and ventricular surfaces of the developing brain (below) and divide to form a densely packed VZ. (B) In developing telencephalon, NECs give rise to radial glia (RG; light blue), which retain properties of NECs (see text), including contact with the ventricular and pial surfaces. At this stage, the RG divide asymmetrically, producing a daughter RG and a daughter intermediate progenitor cell (IPC; green) located away from the ventricular surface in a subventricular zone (SVZ). Newborn neurons (red) use the RG processes as a scaffold for migration to their final destinations. (C) In the neonatal brain, the RG are retained until approximately postnatal day 7. After postnatal day 2, they begin to retract their basal (pial) processes and will give rise to ependymal (E) cells (grey; shown in (D)), B1 cells (teal; shown in (D)) and B2 cells (yellow; shown in (D)) in the mature brain. (D) In the adult brain, B1 cells are the NSCs. They have basal processes that wrap around blood vessels (dark red) and a single primary cilium that extends between the tightly connected E cells. The multiple motile cilia of E cells push CSF through the ventricles. Note the presence of transit-amplifying C cells (green), migrating neuroblasts (A cells, red) and parenchymal astrocytes (B2 cells, orange). This structure in the adult is termed the ventricular-subventricular zone (V-SVZ). Note that other cell types exist in the region that are not discussed within this review including microglia and local and distant innervating neurons.
Fig.2  Embryonic neural cell lineage and marker expression profiles. Neuroepithelial cells (NECs) are the earliest neural progenitors discussed here. These cells produce neurons but also give rise to radial glia cells (RG), which in turn act as the primary progenitors during cortical development. These cells can produce oligodendrocytes, astrocytes and neurons. While precursors for oligodendrocytes and neurons have been characterized, it is still debated whether an astrocyte-restricted precursor cell exists. RG cells also produce pre-B1 cells between E13.5-15.5 that remain relatively quiescent until postnatal reactivation (see text).
Fig.3  Postnatal neural cell lineage and marker expression profiles. *Radial glia persist only during the first postnatal week and are non-self-renewing during this time. They retract their processes after postnatal day 2 in the mouse and give rise to parenchymal astrocytes (orange), ependymal cells (grey), oligodendrocytes (purple) and astrocyte-like adult neural stem cells (B1 cells, teal). B1 cells are self-renewing and also give rise to transit amplifying progenitors (green), which in turn produce neuroblasts (red) that will mature into neurons (yellow). **These markers are primarily expressed by activated B1 cells. ***CD133 is present on the primary cilia of B1 cells, as well as ependymal cells. ****VCAM-1 is expressed on quiescent B1 cells. # Note that Nestin is not expressed on all RG and B1 cells but rather, is dynamically regulated (see text).
Persisting Questions
• Is regional transcription factor expression controlled in the same manner throughout development and in the postnatal brain?
• Which transcription factors are permissive for multiple fates vs. instructive for a specific one?
• How is regional identity maintained postnatally?
• Is there a signaling or transcriptional threshold to induce plasticity of NSCs?
• Is there a ‘gradient of identity” or sharp cutoffs within the V-SVZ?
• How do signals within the developing V-SVZ affect specific TFs to determine the ultimate fate of an NSC?
• Can we mathematically model the input of signals experienced by NSCs that drive fate determination?
• Do SGZ NSCs have a positional identity?
• Does positional identity exist in the human brain?
1 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
doi: 10.1038/nature09347 pmid: 20844536
2 Ahn S, Joyner A L (2005). In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature, 437(7060): 894–897
doi: 10.1038/nature03994 pmid: 16208373
3 Altman J (1962). Autoradiographic study of degenerative and regenerative proliferation of neuroglia cells with tritiated thymidine. Exp Neurol, 5(4): 302–318
doi: 10.1016/0014-4886(62)90040-7 pmid: 13860749
4 Altman J, Das G D (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol, 124(3): 319–335
doi: 10.1002/cne.901240303 pmid: 5861717
5 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
doi: 10.1038/35067582 pmid: 11283751
6 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
doi: 10.1016/S0361-9230(01)00770-5 pmid: 12031271
7 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
doi: 10.1016/S0896-6273(04)00140-0 pmid: 15046721
8 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
doi: 10.1093/cercor/bhs085 pmid: 22473896
9 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
doi: 10.1016/j.neubiorev.2004.03.004 pmid: 15225971
10 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
doi: 10.1111/j.1460-9568.2005.04352.x pmid: 16197496
11 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
doi: 10.1016/j.stem.2010.11.017 pmid: 21112568
12 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
doi: 10.1016/j.cell.2014.04.005 pmid: 24766814
13 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
doi: 10.1038/nature12069 pmid: 23615612
14 Bentivoglio M, Mazzarello P (1999). The history of radial glia. Brain Res Bull, 49(5): 305–315
doi: 10.1016/S0361-9230(99)00065-9 pmid: 10452351
15 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
doi: 10.1016/j.neuron.2012.03.030 pmid: 22632721
16 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
doi: 10.1073/pnas.172403999 pmid: 12177450
17 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
doi: 10.1073/pnas.0605177103 pmid: 16901981
18 Bignami A, Dahl D (1974). Astrocyte-specific protein and radial glia in the cerebral cortex of newborn rat. Nature, 252(5478): 55–56
doi: 10.1038/252055a0 pmid: 4610404
19 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
doi: 10.1016/0006-8993(72)90398-8 pmid: 4559710
20 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
doi: 10.1523/JNEUROSCI.3606-09.2009 pmid: 19955377
21 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
doi: 10.1038/19315 pmid: 10217145
22 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
doi: 10.1126/science.1208884 pmid: 22034427
23 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
doi: 10.1002/cne.23169 pmid: 22700217
24 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
doi: 10.1093/cercor/bhl164 pmid: 17259645
25 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
doi: 10.1016/0306-4522(96)00042-5 pmid: 8783272
26 Calzolari F, Michel J, Baumgart E V, Theis F, Götz M, Ninkovic J (2015). Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nat Neurosci, 18(4): 490–492
doi: 10.1038/nn.3963 pmid: 25730673
27 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
doi: 10.1002/cne.1040 pmid: 11406822
28 Cameron R S, Rakic P (1991). Glial cell lineage in the cerebral cortex: a review and synthesis. Glia, 4(2): 124–137
doi: 10.1002/glia.440040204 pmid: 1827774
29 Campbell K (2003). Dorsal-ventral patterning in the mammalian telencephalon. Curr Opin Neurobiol, 13(1): 50–56
doi: 10.1016/S0959-4388(03)00009-6 pmid: 12593982
30 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
doi: 10.1016/S0896-6273(02)00835-8 pmid: 12372282
31 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
doi: 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1078>3.0.CO;2-0 pmid: 11084651
32 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
doi: 10.1371/journal.pone.0031547 pmid: 22348101
33 Christian K M, Song H, Ming G L (2014). Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci, 37(1): 243–262
doi: 10.1146/annurev-neuro-071013-014134 pmid: 24905596
34 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
pmid: 6481452
35 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
doi: 10.1016/j.neuron.2014.02.039 pmid: 24811379
36 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
doi: 10.1016/j.expneurol.2007.03.021 pmid: 17466977
37 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
doi: 10.1073/pnas.0710000105 pmid: 18195354
38 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
doi: 10.1126/science.1136281 pmid: 17303719
39 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
pmid: 7285936
40 Davis A A, Temple S (1994). A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature, 372(6503): 263–266
doi: 10.1038/372263a0 pmid: 7969470
41 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
doi: 10.1083/jcb.200407053 pmid: 15684031
42 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)
pmid: 26436641
43 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
doi: 10.1523/JNEUROSCI.2870-06.2007 pmid: 17234597
44 Delgado R N, Lim D A (2015). Embryonic Nkx2.1-expressing neural precursor cells contribute to the regional heterogeneity of adult V-SVZ neural stem cells. Dev Biol, 407(2): 265–274
doi: 10.1016/j.ydbio.2015.09.008 pmid: 26387477
45 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
doi: 10.1038/nrn2822 pmid: 20354534
46 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
doi: 10.1007/BF00213941 pmid: 2874885
47 Doetsch F (2003). The glial identity of neural stem cells. Nat Neurosci, 6(11): 1127–1134
doi: 10.1038/nn1144 pmid: 14583753
48 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
doi: 10.1073/pnas.93.25.14895 pmid: 8962152
49 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
doi: 10.1016/S0092-8674(00)80783-7 pmid: 10380923
50 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
pmid: 9185542
51 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
doi: 10.1073/pnas.96.20.11619 pmid: 10500226
52 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
doi: 10.1016/S0896-6273(02)01133-9 pmid: 12495619
53 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
doi: 10.1016/0306-4522(90)90356-9 pmid: 2215915
54 Egger V, Urban N N (2006). Dynamic connectivity in the mitral cell-granule cell microcircuit. Semin Cell Dev Biol, 17(4): 424–432
doi: 10.1016/j.semcdb.2006.04.006 pmid: 16889994
55 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
doi: 10.1093/cercor/13.8.845 pmid: 12853371
56 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
doi: 10.1159/000082134 pmid: 15711057
57 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
doi: 10.1523/JNEUROSCI.2899-04.2005 pmid: 15634788
58 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
doi: 10.1523/JNEUROSCI.2751-04.2004 pmid: 15385618
59 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
doi: 10.1101/SQB.1997.062.01.053 pmid: 9598380
60 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
doi: 10.1016/S0092-8674(00)80323-2 pmid: 9230312
61 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
doi: 10.1038/3305 pmid: 9809557
62 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
doi: 10.1016/j.cell.2014.01.044 pmid: 24561062
63 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
doi: 10.1242/dev.01912 pmid: 16014513
64 Fanselow M S, Dong H W (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1): 7–19
doi: 10.1016/j.neuron.2009.11.031 pmid: 20152109
65 Feliciano D M, Bordey A (2013). Newborn cortical neurons: only for neonates? Trends Neurosci, 36(1): 51–61
doi: 10.1016/j.tins.2012.09.004 pmid: 23062965
66 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
doi: 10.1016/0896-6273(94)90341-7 pmid: 8161459
67 Ferri A L, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi P P, Sala M, DeBiasi S, Nicolis S K (2004). Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development, 131(15): 3805–3819
doi: 10.1242/dev.01204 pmid: 15240551
68 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
doi: 10.1126/science.aaa1975 pmid: 25721503
69 Frantz G D, McConnell S K (1996). Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron, 17(1): 55–61
doi: 10.1016/S0896-6273(00)80280-9 pmid: 8755478
70 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
doi: 10.1038/nrn1990 pmid: 16988653
71 Fuentealba L C, Obernier K, Alvarez-Buylla A (2012). Adult neural stem cells bridge their niche. Cell Stem Cell, 10(6): 698–708
doi: 10.1016/j.stem.2012.05.012 pmid: 22704510
72 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
doi: 10.1016/j.cell.2015.05.041 pmid: 26091041
73 Gage F H (2002). Neurogenesis in the adult brain. J Neurosci, 22(3): 612–613
pmid: 11826087
74 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
doi: 10.1073/pnas.87.1.458 pmid: 2104984
75 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
doi: 10.1038/nn1340 pmid: 15494728
76 Garner C C, Brugg B, Matus A (1988). A 70-kilodalton microtubule-associated protein (MAP2c), related to MAP2. J Neurochem, 50(2): 609–615
doi: 10.1111/j.1471-4159.1988.tb02954.x pmid: 3121794
77 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
doi: 10.1002/stem.1520 pmid: 23964022
78 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.)
pmid: 19552108
79 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
doi: 10.1016/S0896-6273(00)80778-3 pmid: 10399933
80 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
doi: 10.1073/pnas.80.8.2390 pmid: 6572982
81 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
pmid: 947907
82 Gonzales-Roybal G, Lim D A (2013). Chromatin-based epigenetics of adult subventricular zone neural stem cells. Front Genet, 4: 194
doi: 10.3389/fgene.2013.00194 pmid: 24115953
83 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
doi: 10.1016/j.brainresrev.2011.01.001 pmid: 21236296
84 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
pmid: 20187143
85 Götz M, Stoykova A, Gruss P (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron, 21(5): 1031–1044
doi: 10.1016/S0896-6273(00)80621-2 pmid: 9856459
86 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
doi: 10.1073/pnas.181354698 pmid: 11526209
87 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
doi: 10.1002/cne.22566 pmid: 21344407
88 Guillemot F (2005). Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol, 17(6): 639–647
doi: 10.1016/ pmid: 16226447
89 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
doi: 10.1038/nn1479 pmid: 15951811
90 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
pmid: 9012528
91 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
doi: 10.1038/nature08845 pmid: 20154730
92 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
pmid: 2558873
93 Hartfuss E, Galli R, Heins N, Götz M (2001). Characterization of CNS precursor subtypes and radial glia. Dev Biol, 229(1): 15–30
doi: 10.1006/dbio.2000.9962 pmid: 11133151
94 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
doi: 10.1016/j.neuron.2015.07.030 pmid: 26299474
95 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
doi: 10.1073/pnas.0308600100 pmid: 14963232
96 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
doi: 10.1038/nn1440 pmid: 15852015
97 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
98 Herrera D G, Garcia-Verdugo J M, Alvarez-Buylla A (1999). Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol, 46(6): 867–877
doi: 10.1002/1531-8249(199912)46:6<867::AID-ANA9>3.0.CO;2-Z pmid: 10589539
99 Hevner R F (2006). From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol, 33(1): 33–50
doi: 10.1385/MN:33:1:033 pmid: 16388109
100 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
doi: 10.1016/j.neures.2006.03.004 pmid: 16621079
101 His W (1904). Die Entwickelung des menschlichen Gehirns wahrend der esten Monte.Leipzig: Hirzel
102 Hochstim C, Deneen B, Lukaszewicz A, Zhou Q, Anderson D J (2008). Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell, 133(3): 510–522
doi: 10.1016/j.cell.2008.02.046 pmid: 18455991
103 Hockfield S, McKay R D (1985). Identification of major cell classes in the developing mammalian nervous system. J Neurosci, 5(12): 3310–3328
pmid: 4078630
104 Huang L, DeVries 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
doi: 10.1002/(SICI)1097-4695(19980905)36:3<410::AID-NEU8>3.0.CO;2-Z pmid: 9733075
105 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
doi: 10.1016/j.neuron.2011.05.018 pmid: 21791285
106 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
107 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
doi: 10.1126/science.1242366 pmid: 24179156
108 Imayoshi I, Sakamoto M, Kageyama R (2011). Genetic methods to identify and manipulate newly born neurons in the adult brain. Front Neurosci, 5: 64
doi: 10.3389/fnins.2011.00064 pmid: 21562606
109 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
doi: 10.1523/JNEUROSCI.4987-09.2010 pmid: 20203209
110 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
pmid: 12684469
111 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
doi: 10.1073/pnas.0807059105 pmid: 19095802
112 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
doi: 10.1002/jnr.10843 pmid: 14743446
113 Isaacson J S, Strowbridge B W (1998). Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron, 20(4): 749–761
doi: 10.1016/S0896-6273(00)81013-2 pmid: 9581766
114 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
doi: 10.1159/000114541 pmid: 18223308
115 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
doi: 10.1101/gad.10.24.3129 pmid: 8985182
116 Kaplan M S, Hinds J W (1977). Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science, 197(4308): 1092–1094
doi: 10.1126/science.887941 pmid: 887941
117 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 self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci, 17(2): 259–273
doi: 10.1006/mcne.2000.0925 pmid: 11178865
118 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
pmid: 6842284
119 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
pmid: 10066270
120 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
doi: 10.1523/JNEUROSCI.1435-05.2005 pmid: 16049175
121 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
doi: 10.1523/JNEUROSCI.0254-07.2007 pmid: 17596436
122 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
doi: 10.1016/j.stem.2010.05.019 pmid: 20682445
123 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
doi: 10.1016/j.stem.2012.06.016 pmid: 22862947
124 Kopan R, Ilagan M X G (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell, 137(2): 216–233
doi: 10.1016/j.cell.2009.03.045 pmid: 19379690
125 Kornack D R, Rakic P (2001a). Cell proliferation without neurogenesis in adult primate neocortex. Science, 294(5549): 2127–2130
doi: 10.1126/science.1065467 pmid: 11739948
126 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
doi: 10.1073/pnas.081074998 pmid: 11296302
127 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
doi: 10.1016/0168-0102(95)90017-9 pmid: 7501303
128 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
doi: 10.1111/j.1447-073x.2005.00092.x pmid: 15960313
129 Kriegstein A, Alvarez-Buylla A (2009). The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci, 32(1): 149–184
doi: 10.1146/annurev.neuro.051508.135600 pmid: 19555289
130 Kriegstein A R, Götz M (2003). Radial glia diversity: a matter of cell fate. Glia, 43(1): 37–43
doi: 10.1002/glia.10250 pmid: 12761864
131 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
doi: 10.1073/pnas.250471697 pmid: 11095732
132 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
doi: 10.1371/journal.pone.0007017 pmid: 19753118
133 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, LaMantia A S, Walsh C A (2011). The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron, 69(5): 893–905
doi: 10.1016/j.neuron.2011.01.023 pmid: 21382550
134 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
doi: 10.1016/0092-8674(90)90662-X pmid: 1689217
135 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
doi: 10.1146/annurev-physiol-030212-183731 pmid: 23190074
136 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
doi: 10.1016/j.cell.2015.05.047 pmid: 26095251
137 LeVine S M, Goldman J E (1988a). Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci, 8(11): 3992–4006
pmid: 3054008
138 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
doi: 10.1002/cne.902770310 pmid: 3198802
139 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
pmid: 7050307
140 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
doi: 10.1016/j.neuron.2013.03.019 pmid: 23643936
141 Li L, Clevers H (2010). Coexistence of quiescent and active adult stem cells in mammals. Science, 327(5965): 542–545
doi: 10.1126/science.1180794 pmid: 20110496
142 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
doi: 10.1523/JNEUROSCI.0939-11.2011 pmid: 21653849
143 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
doi: 10.1073/pnas.96.13.7526 pmid: 10377448
144 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
doi: 10.1101/cshperspect.a018820 pmid: 27048191
145 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
doi: 10.1038/nature07726 pmid: 19212323
146 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
doi: 10.1523/JNEUROSCI.0201-09.2009 pmid: 19386903
147 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 astrocyte-restricted precursor cells. Dev Biol, 276(1): 31–46
doi: 10.1016/j.ydbio.2004.08.018 pmid: 15531362
148 Livneh Y, Adam Y, Mizrahi A (2014). Odor processing by adult-born neurons. Neuron, 81(5): 1097–1110
doi: 10.1016/j.neuron.2014.01.007 pmid: 24508384
149 Lledo P M, Alonso M, Grubb M S (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci, 7(3): 179–193
doi: 10.1038/nrn1867 pmid: 16495940
150 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
doi: 10.1016/j.stem.2015.07.002 pmid: 26235341
151 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
doi: 10.1073/pnas.90.5.2074 pmid: 8446631
152 Lois C, García-Verdugo J M, Alvarez-Buylla A (1996). Chain migration of neuronal precursors. Science, 271(5251): 978–981
doi: 10.1126/science.271.5251.978 pmid: 8584933
153 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
doi: 10.1523/JNEUROSCI.5265-06.2007 pmid: 17376983
154 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
doi: 10.1162/jocn.2009.21012 pmid: 18476765
155 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
doi: 10.1016/j.neuroscience.2013.04.006 pmid: 23587842
156 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
doi: 10.1111/j.1474-9726.2006.00197.x pmid: 16626393
157 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, deVellis 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
doi: 10.1016/j.cell.2015.04.001 pmid: 26000486
158 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
doi: 10.1073/pnas.1735482100 pmid: 14559968
159 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
doi: 10.1242/jcs.02439 pmid: 15976444
160 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
doi: 10.1523/JNEUROSCI.4608-03.2004 pmid: 14973255
161 Maurice A (2007). Response to Comment on “Human Neuroblasts Migrate to the Olfactory Bulb via a Lateral Ventricular Extension”. Science, 318(5849): 393c
doi: 10.1126/science.1145164
162 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
doi: 10.1016/j.neuron.2015.07.011 pmid: 26299473
163 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
pmid: 11517265
164 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
doi: 10.1016/0165-3806(89)90036-9 pmid: 2496940
165 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
doi: 10.1016/0165-3806(90)90053-2 pmid: 2073725
166 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
doi: 10.1016/S0070-2153(03)53002-2 pmid: 12509125
167 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
doi: 10.1523/JNEUROSCI.1299-06.2006 pmid: 16870736
168 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
doi: 10.1038/nn.3610 pmid: 24362763
169 Merkle F T, Mirzadeh Z, Alvarez-Buylla A (2007). Mosaic organization of neural stem cells in the adult brain. Science, 317(5836): 381–384
doi: 10.1126/science.1144914 pmid: 17615304
170 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
doi: 10.1073/pnas.0407893101 pmid: 15574494
171 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
doi: 10.7554/eLife.02669 pmid: 24843006
172 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
doi: 10.1016/j.mcn.2008.07.015 pmid: 18718868
173 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
doi: 10.1016/j.stem.2008.07.004 pmid: 18786414
174 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
doi: 10.1016/0165-3806(88)90121-6 pmid: 3069243
175 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
doi: 10.1038/nature05091 pmid: 16957738
176 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
doi: 10.1038/nrn2151 pmid: 17514196
177 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
doi: 10.1073/pnas.0907063106 pmid: 19815505
178 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
doi: 10.1016/S0070-2153(05)69004-7 pmid: 16243597
179 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
doi: 10.1046/j.1460-9568.2003.02727.x pmid: 12859339
180 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
doi: 10.1016/0896-6273(94)90046-9 pmid: 7946346
181 Mullen R J, Buck C R, Smith A M (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116(1): 201–211
pmid: 1483388
182 Nedelec J, Pierres M, Moreau H, Barbet J, Naquet P, Faivre-Sarrailh C, Rougon G (1992). Isolation and characterization of a novel glycosyl-phosphatidylinositol-anchored glycoconjugate expressed by developing neurons. Eur J Biochem, 203(3): 433–442
183 Nishiyama A, Lin X H, Giese N, Heldin C H, Stallcup W B (1996). Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res, 43(3): 299–314
doi: 10.1002/(SICI)1097-4547(19960201)43:3<299::AID-JNR5>3.0.CO;2-E pmid: 8714519
184 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
doi: 10.1038/nn.2298 pmid: 19412168
185 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
doi: 10.1038/ncb2843 pmid: 24056302
186 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
pmid: 11943818
187 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
doi: 10.1038/nn1172 pmid: 14703572
188 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
189 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
doi: 10.1002/cne.21669 pmid: 18288691
190 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
doi: 10.1083/jcb.95.1.242 pmid: 6183269
191 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
doi: 10.1016/S0306-4522(98)00751-9 pmid: 10392832
192 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
doi: 10.1016/j.neuron.2011.05.029 pmid: 21745638
193 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
doi: 10.1002/cne.23896 pmid: 26417888
194 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
doi: 10.1038/sj.emboj.7600447 pmid: 15496983
195 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
doi: 10.1073/pnas.0810407106 pmid: 19332781
196 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
doi: 10.1006/exnr.2001.7768 pmid: 11681836
197 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
doi: 10.1016/S0361-9230(96)00116-5 pmid: 8978930
198 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
doi: 10.1046/j.1460-9568.2003.02432.x pmid: 12542656
199 Petreanu L, Alvarez-Buylla A (2002). Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci, 22(14): 6106–6113
pmid: 12122071
200 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
doi: 10.1073/pnas.192314199 pmid: 12235363
201 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
doi: 10.1016/j.neuron.2015.12.007 pmid: 26748089
202 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
doi: 10.1016/j.mcn.2008.01.012 pmid: 18372191
203 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
doi: 10.1016/0165-3806(84)90097-X pmid: 6383523
204 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
pmid: 1112791
205 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
doi: 10.1073/pnas.1219563110 pmid: 23431204
206 Price J L, Powell T P (1970). The mitral and short axon cells of the olfactory bulb. J Cell Sci, 7(3): 631–651
pmid: 5492279
207 Pringle N P, Mudhar H S, Collarini E J, Richardson W D (1992). PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development, 115(2): 535–551
pmid: 1425339
208 Puelles L, Rubenstein J L (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci, 26(9): 469–476
doi: 10.1016/S0166-2236(03)00234-0 pmid: 12948657
209 Purves D (2012). Neuroscience, 5th edn (Sunderland, Mass.: Sinauer Associates)
210 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
pmid: 9671587
211 Quarles R H, Trapp B D (1984). Localization of myelin-associated glycoprotein. J Neurochem, 43(6): 1773–1777
doi: 10.1111/j.1471-4159.1984.tb06110.x pmid: 6208341
212 Rakic P (1988). Specification of cerebral cortical areas. Science, 241(4862): 170–176
doi: 10.1126/science.3291116 pmid: 3291116
213 Rakic P (2006). A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex, 16(Suppl 1): i3–i17
doi: 10.1093/cercor/bhk036 pmid: 16766705
214 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
doi: 10.1126/science.1072530 pmid: 12228720
215 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
doi: 10.1016/j.stem.2015.02.007 pmid: 25800779
216 Reid C B, Liang I, Walsh C (1995). Systematic widespread clonal organization in cerebral cortex. Neuron, 15(2): 299–310
doi: 10.1016/0896-6273(95)90035-7 pmid: 7646887
217 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
doi: 10.1126/science.1553558 pmid: 1553558
218 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
doi: 10.1242/dev.086215 pmid: 23193167
219 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
pmid: 11923433
220 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
doi: 10.1007/s00441-003-0794-1 pmid: 14513354
221 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
doi: 10.1002/eji.1830210611 pmid: 2044653
222 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
doi: 10.1523/JNEUROSCI.0674-14.2014 pmid: 24760839
223 Sakamoto M, Kageyama R, Imayoshi I (2014b). The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci, 8: 121
doi: 10.3389/fnins.2014.00121 pmid: 24904263
224 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
doi: 10.1038/nature14957 pmid: 26416758
225 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
doi: 10.1126/science.1145011 pmid: 17947566
226 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
doi: 10.1038/nature10487 pmid: 21964341
227 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
doi: 10.1038/nature02301 pmid: 14973487
228 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
doi: 10.1002/cne.22543 pmid: 21246550
229 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
doi: 10.1126/science.1119133 pmid: 16410488
230 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
231 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
doi: 10.1007/BF00300010 pmid: 111580
232 Schnitzer J, Schachner M (1981). Characterization of isolated mouse cerebellar cell populations in vitro. J Neuroimmunol, 1(4): 457–470
doi: 10.1016/0165-5728(81)90023-0 pmid: 7050171
233 Shen Q, Goderie S K, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science, 304(5675): 1338–1340
doi: 10.1126/science.1095505 pmid: 15060285
234 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
doi: 10.1016/j.stem.2008.07.026 pmid: 18786416
235 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
pmid: 9364068
236 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
doi: 10.1016/j.stem.2015.07.013 pmid: 26299571
237 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
doi: 10.1016/0014-4886(59)90024-X pmid: 14446424
238 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
doi: 10.1523/JNEUROSCI.3454-14.2015 pmid: 25740506
239 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
doi: 10.1016/0012-1606(81)90477-2 pmid: 6786942
240 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
doi: 10.1016/j.cell.2013.05.002 pmid: 23746839
241 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
doi: 10.1523/JNEUROSCI.1108-04.2005 pmid: 15634762
242 Stallcup W B, Beasley L (1987). Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci, 7(9): 2737–2744
pmid: 3305800
243 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
doi: 10.1093/cercor/12.1.75 pmid: 11734534
244 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. doi: 10.1096/fj.09-151456
245 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
doi: 10.1242/jcs.025064 pmid: 18349072
246 Szatkowska I, Szymańska O, Grabowska A (2004). The role of the human ventromedial prefrontal cortex in memory for contextual information. Neurosci Lett, 364(2): 71–75
doi: 10.1016/j.neulet.2004.03.084 pmid: 15196680
247 Temple S (2001). The development of neural stem cells. Nature, 414(6859): 112–117
doi: 10.1038/35102174 pmid: 11689956
248 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 SHH-Dependent Domain in the V-SVZ Produces Large Numbers of Oligodendroglial Lineage Cells in the Postnatal Brain. Stem Cell Rep, 5(4): 461–470
doi: 10.1016/j.stemcr.2015.08.013 pmid: 26411905
249 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
doi: 10.1073/pnas.97.26.14720 pmid: 11121071
250 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
doi: 10.1111/j.1460-9568.1997.tb01522.x pmid: 9283819
251 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
doi: 10.1523/JNEUROSCI.0399-07.2007 pmid: 17442813
252 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
doi: 10.1002/cne.902890106 pmid: 2808761
253 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
doi: 10.1016/j.neuron.2006.01.018 pmid: 16476661
254 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
doi: 10.1155/2010/894374 pmid: 21527990
255 Walsh C, Cepko C L (1988). Clonally related cortical cells show several migration patterns. Science, 241(4871): 1342–1345
doi: 10.1126/science.3137660 pmid: 3137660
256 Walsh C, Cepko C L (1992). Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science, 255(5043): 434–440
doi: 10.1126/science.1734520 pmid: 1734520
257 Walsh C, Cepko C L (1993). Clonal dispersion in proliferative layers of developing cerebral cortex. Nature, 362(6421): 632–635
doi: 10.1038/362632a0 pmid: 8464513
258 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
doi: 10.1038/cr.2011.83 pmid: 21577236
259 Wang D D, Bordey A (2008). The astrocyte odyssey. Prog Neurobiol, 86(4): 342–367
pmid: 18948166
260 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
doi: 10.1093/cercor/9.6.636 pmid: 10498282
261 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
pmid: 8922416
262 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
doi: 10.1038/8131 pmid: 10321251
263 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
doi: 10.1083/jcb.200604123 pmid: 17030986
264 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
doi: 10.1523/JNEUROSCI.0476-07.2007 pmid: 17670975
265 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
doi: 10.1021/pr070247w pmid: 17696520
266 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
pmid: 10804179
267 Zecevic N (2004). Specific characteristic of radial glia in the human fetal telencephalon. Glia, 48(1): 27–35
doi: 10.1002/glia.20044 pmid: 15326612
268 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
doi: 10.1002/cne.20714 pmid: 16127688
269 Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660
doi: 10.1016/j.cell.2008.01.033 pmid: 18295581
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