Abstract
The expression of early developmental markers such as doublecortin (DCX) and the polysialylated-neural cell adhesion molecule (PSA-NCAM) has been used to identify immature neurons within canonical neurogenic niches. Additionally, DCX/PSA-NCAM+ immature neurons reside in cortical layer II of the paleocortex and in the paleo- and entorhinal cortex of mice and rats, respectively. These cells are also found in the neocortex of guinea pigs, rabbits, some afrotherian mammals, cats, dogs, non-human primates, and humans. The population of cortical DCX/PSA-NCAM+ immature neurons is generated prenatally as conclusively demonstrated in mice, rats, and guinea pigs. Thus, the majority of these cells do not appear to be the product of adult proliferative events. The immature neurons in cortical layer II are most abundant in the cortices of young individuals, while very few DCX/PSA-NCAM + cortical neurons can be detected in aged mammals. Maturation of DCX/PSA-NCAM+ cells into glutamatergic and GABAergic neurons has been proposed as an explanation for the age-dependent reduction in their population over time. In this review, we compile the recent information regarding the age-related decrease in the number of cortical DCX/PSA-NCAM+ neurons. We compare the distribution and fates of DCX/PSA-NCAM + neurons among mammalian species and speculate their impact on cognitive function. To respond to the diversity of adult neurogenesis research produced over the last number of decades, we close this review by discussing the use and precision of the term “adult non-canonical neurogenesis.”
Similar content being viewed by others
References
Abrous D N, Montaron M F, Petry K G, Rougon G, Darnaudéry M, Le Moal M, Mayo W(1997). Decrease in highly polysialylated neuronal cell adhesion molecules and in spatial learning during ageing are not correlated. Brain Res, 744(2): 285–292
Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, Ferri P, Sartini S, Del Grande P (2000). Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett, 286(1): 21–24
Bédard A, Lévesque M, Bernier P J, Parent A (2002). The rostral migratory stream in adult squirrel monkeys: contribution of new neurons to the olfactory tubercle and involvement of the antiapoptotic protein Bcl-2. Eur J Neurosci, 16(10): 1917–1924
Bekkers J M, Suzuki N (2013). Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci, 36(7): 429–438
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
Betarbet R, Zigova T, Bakay R A, Luskin M B (1996). Dopaminergic and GABAergic interneurons of the olfactory bulb are derived from the neonatal subventricular zone. Int J Dev Neurosci, 14(7-8): 921–930
Biebl M, Cooper C M, Winkler J, Kuhn H G (2000). Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett, 291(1): 17–20
Bizon J L, Gallagher M (2005). More is less: neurogenesis and agerelated cognitive decline in Long-Evans rats. Sci SAGE KE, 2005(7): re2
Bizon J L, Lee H J, Gallagher M (2004). Neurogenesis in a rat model of age-related cognitive decline. Aging Cell, 3(4): 227–234
Bloch J, Kaeser M, Sadeghi Y, Rouiller EM, Redmond D E, Brunet J F (2011). Doublecortin-positive cells in the adult primate cerebral cortex and possible role in brain plasticity and development. J Comp Neurol, 519(4): 775–789
Bondolfi L, Ermini F, Long J M, Ingram D K, Jucker M (2004). Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol Aging, 25(3): 333–340
Bonfanti L (2013). The (real) neurogenic/gliogenic potential of the postnatal and adult brain parenchyma. ISRN Neurosci, 2013: 354136
Bonfanti L, Nacher J (2012). New scenarios for neuronal structural plasticity in non-neurogenic brain parenchyma: the case of cortical layer II immature neurons. Prog Neurobiol, 98(1): 1–15
Bonfanti L, Olive S, Poulain D A, Theodosis D T (1992). Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience, 49(2): 419–436
Bonfanti L, Peretto P (2011). Adult neurogenesis in mammals—a theme with many variations. Eur J Neurosci, 34(6): 930–950
Breunig J J, Arellano J I, Macklis J D, Rakic P (2007). Everything that glitters isn’t gold: a critical review of postnatal neural precursor analyses. Cell Stem Cell, 1(6): 612–627
Brown J, Cooper-Kuhn C M, Kempermann G, van Praag H, Winkler J, Gage F H, Kuhn H G (2003). Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci, 17(10): 2042–2046
Burns K A, Ayoub A E, Breunig J J, Adhami F, Weng WL, Colbert MC, 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
Burns T C, Ortiz-González X R, Gutiérrez-Pérez M, Keene C D, Sharda R, Demorest Z L, Jiang Y, Nelson-Holte M, Soriano M, Nakagawa Y, Luquin MR, Garcia-Verdugo JM, Prósper F, Low WC, Verfaillie C M (2006). Thymidine analogs are transferred from prelabeled donor to host cells in the central nervous system after transplantation: a word of caution. Stem Cells, 24(4): 1121–1127
Butt A M, Hamilton N, Hubbard P, Pugh M, Ibrahim M (2005). Synantocytes: the fifth element. J Anat, 207(6): 695–706
Cai Y, Xiong K, Chu Y, Luo D W, Luo X G, Yuan X Y, Struble R G, Clough R W, Spencer D D, Williamson A, Kordower J H, Patrylo P R, Yan X X (2009). Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp Neurol, 216(2): 342–356
Cameron H A, McKay R D (1999). Restoring production of hippocampal neurons in old age. Nat Neurosci, 2(10): 894–897
Carleton A, Petreanu L T, Lansford R, Alvarez-Buylla A, Lledo P M (2003). Becoming a new neuron in the adult olfactory bulb. Nat Neurosci, 6(5): 507–518
Clarke L E, Young K M, Hamilton N B, Li H, Richardson W D, Attwell D (2012). Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J Neurosci, 32(24): 8173–8185
Costa M R, Kessaris N, Richardson W D, Götz M, Hedin-Pereira C (2007). The marginal zone/layer I as a novel niche for neurogenesis and gliogenesis in developing cerebral cortex. J Neurosci, 27(42): 11376–11388
Couillard-Despres S, Winner B, Karl C, Lindemann G, Schmid P, Aigner R, Laemke J, Bogdahn U, Winkler J, Bischofberger J, Aigner L (2006). Targeted transgene expression in neuronal precursors: watching young neurons in the old brain. Eur J Neurosci, 24(6): 1535–1545
Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn H G, Aigner L (2005). Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci, 21(1): 1–14
Curtis M A, Eriksson P S, Faull R L (2007). Progenitor cells and adult neurogenesis in neurodegenerative diseases and injuries of the basal ganglia. Clin Exp Pharmacol Physiol, 34(5-6): 528–532
Dawson M R, Polito A, Levine J M, Reynolds R (2003). NG2- expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci, 24(2): 476–488
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
de la Rosa-Prieto C, Saiz-Sanchez D, Ubeda-Bañon I, Argandoña-Palacios L, Garcia-Muñozguren S, Martinez-Marcos A (2010). Neurogenesis in subclasses of vomeronasal sensory neurons in adult mice. Dev Neurobiol, 70(14): 961–970
de Marchis S, Fasolo A, Puche A C (2004). Subventricular zone-derived neuronal progenitors migrate into the subcortical forebrain of postnatal mice. J Comp Neurol, 476(3): 290–300
de Nevi E, Marco-Salazar P, Fondevila D, Blasco E, Pérez L, Pumarola M (2013). Immunohistochemical study of doublecortin and nucleostemin in canine brain. Eur J Histochem, 57 (1): e9
des Portes V, Pinard J M, Billuart P, Vinet M C, Koulakoff A, Carrié A, Gelot A, Dupuis E, Motte J, Berwald-Netter Y, Catala M, Kahn A, Beldjord C, Chelly J (1998). A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell, 92(1): 51–61
Dimou L, Simon C, Kirchhoff F, Takebayashi H, Götz M (2008). Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci, 28(41): 10434–10442
Dirian L, Galant S, Coolen M, Chen W, Bedu S, Houart C, Bally-Cuif L, Foucher I (2014). Spatial regionalization and heterochrony in the formation of adult pallial neural stem cells. Dev Cell, 30(2): 123–136
Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, Schachner M (2004). Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci, 24(42): 9372–9382
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
Duque A, Rakic P (2011). Different effects of bromodeoxyuridine and [3H]thymidine incorporation into DNA on cell proliferation, position, and fate. J Neurosci, 31(42): 15205–15217
Ehninger D, Kempermann G (2008). Neurogenesis in the adult hippocampus. Cell Tissue Res, 331(1): 243–250
Ehninger D, Wang L P, Klempin F, Römer B, Kettenmann H, Kempermann G (2011). Enriched environment and physical activity reduce microglia and influence the fate of NG2 cells in the amygdala of adult mice. Cell Tissue Res, 345(1): 69–86
Ekstrand J J, Domroese M E, Feig S L, Illig K R, Haberly L B (2001). Immunocytochemical analysis of basket cells in rat piriform cortex. J Comp Neurol, 434(3): 308–328
Encinas J M, Michurina T V, Peunova N, Park J H, Tordo J, Peterson D A, Fishell G, Koulakov A, Enikolopov G (2011). Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell, 8(5): 566–579
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
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
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
Feliciano D M, Bordey A (2013). Newborn cortical neurons: only for neonates? Trends Neurosci, 36(1): 51–61
Feliciano D M, Bordey A, Bonfanti L (2015). Noncanonical Sites of Adult Neurogenesis in the Mammalian Brain. Cold Spring Harb Perspect Biol, 7(10): a018846
Fox G B, Fichera G, Barry T, O’Connell AW, Gallagher H C, Murphy K J, Regan C M (2000). Consolidation of passive avoidance learning is associated with transient increases of polysialylated neurons in layer II of the rat medial temporal cortex. J Neurobiol, 45(3): 135–141
Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet M C, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell S K, Berwald-Netter Y, Denoulet P, Chelly J (1999). Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron, 23(2): 247–256
Friocourt G, Liu J S, Antypa M, Rakic S, Walsh C A, Parnavelas J G (2007). Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci, 27(14): 3875–3883
Gage F H, Kempermann G, Song H (2008). Adult Neurogenesis, Vol 52. Cold Spring Harbor Laboratory Press
Ge S, Goh E L, Sailor K A, Kitabatake Y, Ming G L, Song H (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 439(7076): 589–593
Gómez-Climent M A, Castillo-Gómez E, Varea E, Guirado R, Blasco-Ibáñez J M, Crespo C, Martínez-Guijarro F J, Nácher J (2008). A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb Cortex, 18(10): 2229–2240
Gomez-Climent M A, Guirado R, Varea E, Nàcher J (2010). “Arrested development”. Immature, but not recently generated, neurons in the adult brain. Arch Ital Biol, 148(2): 159–172
Gottfried J A, Winston J S, Dolan R J (2006). Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron, 49 (3): 467–479
Gould E (2007).How widespread is adult neurogenesis in mammals? Nat Rev Neurosci, 8(6): 481–488
Gould E, Tanapat P, Hastings N B, Shors T J (1999). Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci, 3(5): 186–192
Gritti A, Vescovi A L, Galli R (2002). Adult neural stem cells: plasticity and developmental potential. J Physiol Paris, 96(1-2): 81–90
Guo F, Maeda Y, Ma J, Xu J, Horiuchi M, Miers L, Vaccarino F, Pleasure D (2010). Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J Neurosci, 30(36): 12036–12049
Hastings N B, Gould E (1999). Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol, 413(1): 146–154
He X, Zhang X M, Wu J, Fu J, Mou L, Lu D H, Cai Y, Luo X G, Pan A, Yan X X (2014). Olfactory experience modulates immature neuron development in postnatal and adult guinea pig piriform cortex. Neuroscience, 259: 101–112
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
Johnson C P, Fujimoto I, Rutishauser U, Leckband D E (2005). Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem, 280(1): 137–145
Kadohisa M, Wilson D A (2006a). Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol, 95(3): 1888–1896
Kadohisa M, Wilson D A (2006b). Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci USA, 103(41): 15206–15211
Kang S H, Fukaya M, Yang J K, Rothstein J D, Bergles D E (2010). NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron, 68(4): 668–681
Kaplan M S (1981). Neurogenesis in the 3-month-old rat visual cortex. J Comp Neurol, 195(2): 323–338
Kapur A, Pearce R A, Lytton W W, Haberly L B (1997). GABAAmediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J Neurophysiol, 78(5): 2531–2545
Kato T, Yokouchi K, Kawagishi K, Fukushima N, Miwa T, Moriizumi T, Kato T, Yokouchi K, Kawagishi K (2000). Fate of newly formed periglomerular cells in the olfactory bulb. Acta Otolaryngol, 120(7): 876–879
Kelsch W, Mosley C P, Lin C W, Lois C (2007). Distinct mammalian precursors are committed to generate neurons with defined dendritic projection patterns. PLoS Biol, 5 (11): e300
Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004). Milestones of neuronal development in the adult hippocampus. Trends Neurosci, 27(8): 447–452
Klempin F, Kronenberg G, Cheung G, Kettenmann H, Kempermann G (2011). Properties of doublecortin-(DCX)-expressing cells in the piriform cortex compared to the neurogenic dentate gyrus of adult mice. PLoS ONE, 6 (10): e25760
Komitova M, Zhu X, Serwanski D R, Nishiyama A (2009). NG2 cells are distinct from neurogenic cells in the postnatal mouse subventricular zone. J Comp Neurol, 512(5): 702–716
König R, Rotheneichner P, Marschallinger J, Aigner L, Couillard-Despres S (2016). Adult Neurogenesis in the Hippocampus. Elsevier, pp. 145–176
Kornack D R, Rakic P (2001). Cell proliferation without neurogenesis in adult primate neocortex. Science, 294(5549): 2127–2130
Kremer T, Jagasia R, Herrmann A, Matile H, Borroni E, Francis F, Kuhn H G, Czech C (2013). Analysis of adult neurogenesis: evidence for a prominent “non-neurogenic” DCX-protein pool in rodent brain. PLoS ONE, 8 (5): e59269
Kuan C Y, Schloemer A J, Lu A, Burns K A, WengW L, Williams M T, Strauss K I, Vorhees C V, Flavell R A, Davis R J, Sharp F R, Rakic P (2004). Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci, 24 (47): 10763–10772
Kunz B A, Kohalmi S E (1991). Modulation of mutagenesis by deoxyribonucleotide levels. Annu Rev Genet, 25(1): 339–359
Lehner B, Sandner B, Marschallinger J, Lehner C, Furtner T, Couillard- Despres S, Rivera F J, Brockhoff G, Bauer H C, Weidner N, Aigner L (2011). The dark side of BrdU in neural stem cell biology: detrimental effects on cell cycle, differentiation and survival. Cell Tissue Res, 345(3): 313–328
Lemaire V, Koehl M, Le Moal M, Abrous D N (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA, 97(20): 11032–11037
Luskin M B, Boone M S (1994). Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem Senses, 19(6): 695–714
Luzzati F, Bonfanti L, Fasolo A, Peretto P (2009). DCX and PSANCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex, 19(5): 1028–1041
Luzzati F, Nato G, Oboti L, Vigna E, Rolando C, Armentano M, Bonfanti L, Fasolo A, Peretto P (2014). Quiescent neuronal progenitors are activated in the juvenile guinea pig lateral striatum and give rise to transient neurons. Development, 141(21): 4065–4075
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
Manganas L N, Zhang X, Li Y, Hazel R D, Smith S D, Wagshul M E, Henn F, Benveniste H, Djuric P M, Enikolopov G, Maletic-Savatic M (2007). Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science, 318(5852): 980–985
Markakis E A, Gage F H (1999). Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol, 406(4): 449–460
Martí-Mengual U, Varea E, Crespo C, Blasco-Ibáñez J M, Nacher J (2013). Cells expressing markers of immature neurons in the amygdala of adult humans. Eur J Neurosci, 37(1): 10–22
Mikkonen M, Soininen H, Kälviänen R, Tapiola T, Ylinen A, Vapalahti M, Paljärvi L, Pitkänen A (1998). Remodeling of neuronal circuitries in human temporal lobe epilepsy: increased expression of highly polysialylated neural cell adhesion molecule in the hippocampus and the entorhinal cortex. Ann Neurol, 44(6): 923–934
Murphy K J, Fox G B, Foley A G, Gallagher H C, O’Connell A, Griffin A M, Nau H, Regan C M (2001). Pentyl-4-yn-valproic acid enhances both spatial and avoidance learning, and attenuates age-related NCAM-mediated neuroplastic decline within the rat medial temporal lobe. J Neurochem, 78(4): 704–714
Nacher J, Bonfanti L (2015). New neurons from old beliefs in the adult piriform cortex? A Commentary on: “Occurrence of new neurons in the piriform cortex”. Front Neuroanat, 9: 62
Nacher J, Crespo C, McEwen B S (2001). Doublecortin expression in the adult rat telencephalon. Eur J Neurosci, 14(4): 629–644
Nacher J, Lanuza E, McEwen B S (2002). Distribution of PSA-NCAM expression in the amygdala of the adult rat. Neuroscience, 113(3): 479–484
Neville K R, Haberly L B (2003). Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol, 90 (6): 3921–3930
Ní Dhúill C M, Fox G B, Pittock S J, O’Connell A W, Murphy K J, Regan C M (1999). Polysialylated neural cell adhesion molecule expression in the dentate gyrus of the human hippocampal formation from infancy to old age. J Neurosci Res, 55(1): 99–106
Nishiyama A, Komitova M, Suzuki R, Zhu X (2009). Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci, 10(1): 9–22
Nishiyama A, Suzuki R, Zhu X (2014). NG2 cells (polydendrocytes) in brain physiology and repair. Front Neurosci, 8: 133
Nowakowski R S, Hayes N L (2000). New neurons: extraordinary evidence or extraordinary conclusion? Science, 288 (5467): 771
Nowakowski R S, Lewin S B, Miller M W (1989). Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol, 18(3): 311–318
Okuda H, Tatsumi K, Makinodan M, Yamauchi T, Kishimoto T, Wanaka A (2009). Environmental enrichment stimulates progenitor cell proliferation in the amygdala. J Neurosci Res, 87(16): 3546–3553
Patzke N, Le Roy A, Ngubane N W, Bennett N C, Medger K, Gravett N, Kaswera-Kyamakya C, Gilissen E, Chawana R, Manger P R (2014). The distribution of doublecortin-immunopositive cells in the brains of four afrotherian mammals: the Hottentot golden mole (Amblysomus hottentotus), the rock hyrax (Procavia capensis), the eastern rock sengi (Elephantulus myurus) and the four-toed sengi (Petrodromus tetradactylus). Brain Behav Evol, 84(3): 227–241
Peretto P, Bonfanti L (2014). Major unsolved points in adult neurogenesis: doors open on a translational future? Front Neurosci, 8: 154
Petreanu L, Alvarez-Buylla A (2002). Maturation and death of adultborn olfactory bulb granule neurons: role of olfaction. J Neurosci, 22 (14): 6106–6113
Pierce A A, Xu A W (2010). De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J Neurosci, 30(2): 723–730
Psachoulia K, Jamen F, Young K M, Richardson W D (2009). Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biol, 5(3-4): 57–67
Purves D, Augustine G J, Flitzpatrick D, Katz L C, La Mantia A S, McNamara J O, Williams S M (2001). Neuroscience, 2nd edition. Sunderland (MA): Sinauer Associates
Richardson W D, Young K M, Tripathi R B, McKenzie I (2011). NG2- glia as multipotent neural stem cells: fact or fantasy? Neuron, 70(4): 661–673
Rivers L E, Young K M, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson W D (2008). PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci, 11(12): 1392–1401
Robins S C, Trudel E, Rotondi O, Liu X, Djogo T, Kryzskaya D, Bourque CW, KokoevaMV (2013). Evidence for NG2-glia derived, adult-born functional neurons in the hypothalamus. PLoS ONE, 8 (10): e78236
Rosselli-Austin L, Altman J (1979). The postnatal development of the main olfactory bulb of the rat. J Dev Physiol, 1(4): 295–313
Rossi S L, Mahairaki V, Zhou L, Song Y, Koliatsos V E (2014). Remodeling of the piriform cortex after lesion in adult rodents. Neuroreport, 25(13): 1006–1012
Rubio A, Belles M, Belenguer G, Vidueira S, Fariñas I, Nacher J (2015). Characterization and isolation of immature neurons of the adult mouse piriform cortex. Dev Neurobiol, doi: 10.1002/dneu.22357
Rutishauser U (2008). Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci, 9(1): 26–35
Saegusa T, Mine S, Iwasa H, Murai H, Seki T, Yamaura A, Yuasa S (2004). Involvement of highly polysialylated neural cell adhesion molecule (PSA-NCAM)-positive granule cells in the amygdaloidkindling- induced sprouting of a hippocampal mossy fiber trajectory. Neurosci Res, 48(2): 185–194
Sairanen M, O’Leary O F, Knuuttila J E, Castrén E (2007). Chronic antidepressant treatment selectively increases expression of plasticity- related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience, 144(1): 368–374
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
Seki T, Arai Y (1999). Temporal and spacial relationships between PSANCAM- expressing, newly generated granule cells, and radial glialike cells in the adult dentate gyrus. J Comp Neurol, 410(3): 503–513
Shapiro L A, Ng K, Zhou Q Y, Ribak C E (2009). Subventricular zonederived, newly generated neurons populate several olfactory and limbic forebrain regions. Epilepsy Behav, 14(Suppl 1): 74–80
Shapiro L A, Ng K L, Kinyamu R, Whitaker-Azmitia P, Geisert E E, Blurton-Jones M, Zhou Q Y, Ribak C E (2007a). Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex. Brain Struct Funct, 212(2): 133–148
Shapiro L A, Ng K L, Zhou Q Y, Ribak C E (2007b). Olfactory enrichment enhances the survival of newly born cortical neurons in adult mice. Neuroreport, 18(10): 981–985
Shechter R, Ziv Y, Schwartz M (2007). New GABAergic interneurons supported by myelin-specific T cells are formed in intact adult spinal cord. Stem Cells, 25(9): 2277–2282
Shors T J, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410(6826): 372–376
Shors T J, Townsend D A, Zhao M, Kozorovitskiy Y, Gould E (2002). Neurogenesis may relate to some but not all types of hippocampaldependent learning. Hippocampus, 12(5): 578–584
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
Suzuki N, Bekkers J M (2007). Inhibitory interneurons in the piriform cortex. Clin Exp Pharmacol Physiol, 34(10): 1064–1069
Suzuki N, Bekkers J M (2010a). Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex. Cereb Cortex, 20(12): 2971–2984
Suzuki N, Bekkers J M (2010b). Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comp Neurol, 518(10): 1670–1687
Takemura N U (2005). Evidence for neurogenesis within the white matter beneath the temporal neocortex of the adult rat brain. Neuroscience, 134(1): 121–132
Toni N, Laplagne D A, Zhao C, Lombardi G, Ribak C E, Gage F H, Schinder A F (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci, 11(8): 901–907
Toni N, Teng EM, Bushong E A, Aimone J B, Zhao C, Consiglio A, van Praag H, Martone M E, Ellisman M H, Gage F H (2007). Synapse formation on neurons born in the adult hippocampus. Nat Neurosci, 10(6): 727–734
van Praag H, Schinder A F, Christie B R, Toni N, Palmer T D, Gage F H (2002). Functional neurogenesis in the adult hippocampus. Nature, 415(6875): 1030–1034
Varea E, Belles M, Vidueira S, Blasco-Ibáñez J M, Crespo C, Pastor A M, Nacher J (2011). PSA-NCAM is Expressed in Immature, but not Recently Generated, Neurons in the Adult Cat Cerebral Cortex Layer II. Front Neurosci, 5: 17
Varea E, Castillo-Gómez E, Gómez-Climent M A, Blasco-Ibáñez J M, Crespo C, Martínez-Guijarro F J, Nàcher J (2007).PSA-NCAM expression in the human prefrontal cortex. J Chem Neuroanat, 33(4): 202–209
Varea E, Castillo-Gómez E, Gómez-Climent M A, Guirado R, Blasco-Ibáñez J M, Crespo C, Martínez-Guijarro F J, Nácher J (2009). Differential evolution of PSA-NCAM expression during aging of the rat telencephalon. Neurobiol Aging, 30(5): 808–818
Vessal M, Aycock A, Garton M T, Ciferri M, Darian-Smith C (2007). Adult neurogenesis in primate and rodent spinal cord: comparing a cervical dorsal rhizotomy with a dorsal column transection. Eur J Neurosci, 26(10): 2777–2794
Vivar C, van Praag H (2013). Functional circuits of new neurons in the dentate gyrus. Front Neural Circuits, 7: 15
Winner B, Cooper-Kuhn C M, Aigner R, Winkler J, Kuhn H G (2002). Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci, 16(9): 1681–1689
Xiong K, Cai Y, Zhang X M, Huang J F, Liu Z Y, Fu G M, Feng J C, Clough RW, Patrylo P R, Luo X G, Hu C H, Yan X X (2010). Layer I as a putative neurogenic niche in young adult guinea pig cerebrum. Mol Cell Neurosci, 45(2): 180–191
Xiong K, Luo D W, Patrylo P R, Luo X G, Struble R G, Clough R W, Yan X X (2008). Doublecortin-expressing cells are present in layer II across the adult guinea pig cerebral cortex: partial colocalization with mature interneuron markers. Exp Neurol, 211(1): 271–282
Yang Y, Geldmacher D S, Herrup K (2001). DNA replication precedes neuronal cell death in Alzheimer’s disease. J Neurosci, 21(8): 2661–2668
Yang Y, Xie M X, Li J M, Hu X, Patrylo P R, Luo X G, Cai Y, Li Z, Yan X X (2015). Prenatal genesis of layer II doublecortin expressing neurons in neonatal and young adult guinea pig cerebral cortex. Front Neuroanat, 9: 109
Yuan T F, Liang Y X, So K F (2014). Occurrence of new neurons in the piriform cortex. Front Neuroanat, 8: 167
Yuan T F, Liang Y X, So K F (2015). Response: New neurons from old beliefs in the adult piriform cortex? A Commentary on: “Occurrence of new neurons in the piriform cortex”. Front Neuroanat, 9: 79
Zhang J, Giesert F, Kloos K, Vogt Weisenhorn DM, Aigner L, Wurst W, Couillard-Despres S (2010). A powerful transgenic tool for fate mapping and functional analysis of newly generated neurons. BMC Neurosci, 11 (1): 158
Zhang X M, Cai Y, Chu Y, Chen E Y, Feng J C, Luo X G, Xiong K, Struble R G, Clough R W, Patrylo P R, Kordower J H, Yan X X (2009). Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat, 3: 17
Zhu X, Bergles D E, Nishiyama A (2008). NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development, 135(1): 145–157
Zhu X, Hill R A, Dietrich D, Komitova M, Suzuki R, Nishiyama A (2011). Age-dependent fate and lineage restriction of single NG2 cells. Development, 138(4): 745–753
Zigova T, Betarbet R, Soteres B J, Brock S, Bakay R A, Luskin M B (1996). A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotopically transplanted telencephalic ventricular zone cells. Dev Biol, 173(2): 459–474
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
König, R., Benedetti, B., Rotheneichner, P. et al. Distribution and fate of DCX/PSA-NCAM expressing cells in the adult mammalian cortex: A local reservoir for adult cortical neuroplasticity?. Front. Biol. 11, 193–213 (2016). https://doi.org/10.1007/s11515-016-1403-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-016-1403-5