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Comparative aspects of adult neural stem cell activity in vertebrates

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Abstract

At birth or after hatching from the egg, vertebrate brains still contain neural stem cells which reside in specialized niches. In some cases, these stem cells are deployed for further postnatal development of parts of the brain until the final structure is reached. In other cases, postnatal neurogenesis continues as constitutive neurogenesis into adulthood leading to a net increase of the number of neurons with age. Yet, in other cases, stem cells fuel neuronal turnover. An example is protracted development of the cerebellar granular layer in mammals and birds, where neurogenesis continues for a few weeks postnatally until the granular layer has reached its definitive size and stem cells are used up. Cerebellar growth also provides an example of continued neurogenesis during adulthood in teleosts. Again, it is the granular layer that grows as neurogenesis continues and no definite adult cerebellar size is reached. Neuronal turnover is most clearly seen in the telencephalon of male canaries, where projection neurons are replaced in nucleus high vocal centre each year before the start of a new mating season—circuitry reconstruction to achieve changes of the song repertoire in these birds? In this review, we describe these and other examples of adult neurogenesis in different vertebrate taxa. We also compare the structure of the stem cell niches to find common themes in their organization despite different functions adult neurogenesis serves in different species. Finally, we report on regeneration of the zebrafish telencephalon after injury to highlight similarities and differences of constitutive neurogenesis and neuronal regeneration.

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References

  • Adolf B, Chapouton P, Lam CS, Topp S, Tannhauser B, Strahle U, Gotz M, Bally-Cuif L (2006) Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295(1):278–293

    Article  PubMed  CAS  Google Scholar 

  • Airey DC, DeVoogd TJ (2000) Greater song complexity is associated with augmented song system anatomy in zebra finches. Neuroreport 11(10):2339–2344

    Article  PubMed  CAS  Google Scholar 

  • Altman J (1969a) Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136(3):269–293

    Article  PubMed  CAS  Google Scholar 

  • Altman J (1969b) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137(4):433–457

    Article  PubMed  CAS  Google Scholar 

  • Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301(3):365–381

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Alunni A, Hermel JM, Heuze A, Bourrat F, Jamen F, Joly JS (2010) Evidence for neural stem cells in the medaka optic tectum proliferation zones. Dev Neurobiol 70(10):693–713

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Buylla A, Kirn JR (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33(5):585–601

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Buylla A, Theelen M, Nottebohm F (1988) Mapping of radial glia and of a new cell type in adult canary brain. J Neurosci 8(8):2707–2712

    PubMed  CAS  Google Scholar 

  • Alvarez-Buylla A, Theelen M, Nottebohm F (1990) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5(1):101–109

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Buylla A, Ling CY, Yu WS (1994) Contribution of neurons born during embryonic, juvenile, and adult life to the brain of adult canaries: regional specificity and delayed birth of neurons in the song-control nuclei. J Comp Neurol 347(2):233–248

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Buylla A, Garcia-Verdugo JM, Mateo AS, Merchant-Larios H (1998) Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J Neurosci 18(3):1020–1037

    PubMed  CAS  Google Scholar 

  • Amrein I, Dechmann DK, Winter Y, Lipp HP (2007) Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS One 2(5):e455

    Article  PubMed  CAS  Google Scholar 

  • Amrein I, Isler K, Lipp HP (2011) Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage. Eur J Neurosci 34(6):978–987

    Article  PubMed  Google Scholar 

  • Barnea A, Pravosudov V (2011) Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approaches. Eur J Neurosci 34(6):884–907

    Article  PubMed  Google Scholar 

  • Baumgart EV, Barbosa JS, Bally-Cuif L, Gotz M, Ninkovic J (2012) Stab wound injury of the zebrafish telencephalon: a model for comparative analysis of reactive gliosis. Glia 60(3):343–357

    Article  PubMed  Google Scholar 

  • Bayer SA, Yackel JW, Puri PS (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216(4548):890–892

    Article  PubMed  CAS  Google Scholar 

  • Becker T, Becker CG (2001) Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish. J Comp Neurol 433(1):131–147

    Article  PubMed  CAS  Google Scholar 

  • Becker CG, Becker T (2008) Adult zebrafish as a model for successful central nervous system regeneration. Restor Neurol Neurosci 26(2–3):71–80

    PubMed  Google Scholar 

  • Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 377(4):577–595

    Article  PubMed  CAS  Google Scholar 

  • Becker T, Lieberoth BC, Becker CG, Schachner M (2005) Differences in the regenerative response of neuronal cell populations and indications for plasticity in intraspinal neurons after spinal cord transection in adult zebrafish. Mol Cell Neurosci 30(2):265–278

    Article  PubMed  CAS  Google Scholar 

  • Berg DA, Kirkham M, Beljajeva A, Knapp D, Habermann B, Ryge J, Tanaka EM, Simon A (2010) Efficient regeneration by activation of neurogenesis in homeostatically quiescent regions of the adult vertebrate brain. Development 137(24):4127–4134

    Article  PubMed  CAS  Google Scholar 

  • Bernocchi G, Scherini E, Giacometti S, Mares V (1990) Premitotic DNA synthesis in the brain of the adult frog (Rana esculenta L.): an autoradiographic 3H-thymidine study. Anat Rec 228(4):461–470

    Article  PubMed  CAS  Google Scholar 

  • Blader P, Plessy C, Strahle U (2003) Multiple regulatory elements with spatially and temporally distinct activities control neurogenin1 expression in primary neurons of the zebrafish embryo. Mech Dev 120(2):211–218

    Article  PubMed  CAS  Google Scholar 

  • Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145(7):1142–1155

    Article  PubMed  CAS  Google Scholar 

  • Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals—a theme with many variations. Eur J Neurosci 34(6):930–950

    Article  PubMed  Google Scholar 

  • Boss BD, Peterson GM, Cowan WM (1985) On the number of neurons in the dentate gyrus of the rat. Brain Res 338(1):144–150

    Article  PubMed  CAS  Google Scholar 

  • Brandstatter R, Kotrschal K (1990) Brain growth patterns in four European cyprinid fish species (Cyprinidae, Teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus). Brain Behav Evol 35(4):195–211

    Article  PubMed  CAS  Google Scholar 

  • Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascon S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner RF, Raineteau O, Gotz M (2009) Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12(12):1524–1533

    Article  PubMed  CAS  Google Scholar 

  • Byrd CA, Brunjes PC (1998) Addition of new cells to the olfactory bulb of adult zebrafish. Ann N Y Acad Sci 855:274–276

    Article  PubMed  CAS  Google Scholar 

  • Byrd CA, Brunjes PC (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105(4):793–801

    Article  PubMed  CAS  Google Scholar 

  • Cerveny KL, Varga M, Wilson SW (2012) Continued growth and circuit building in the anamniote visual system. Dev Neurobiol 72:328–345

    Google Scholar 

  • Chaplin N, Tendeng C, Wingate RJ (2010) Absence of an external germinal layer in zebrafish and shark reveals a distinct, anamniote ground plan of cerebellum development. J Neurosci 30(8):3048–3057

    Article  PubMed  CAS  Google Scholar 

  • Chapouton P, Skupien P, Hesl B, Coolen M, Moore JC, Madelaine R, Kremmer E, Faus-Kessler T, Blader P, Lawson ND, Bally-Cuif L (2010) Notch activity levels control the balance between quiescence and recruitment of adult neural stem cells. J Neurosci 30(23):7961–7974

    Article  PubMed  CAS  Google Scholar 

  • Chapouton P, Webb KJ, Stigloher C, Alunni A, Adolf B, Hesl B, Topp S, Kremmer E, Bally-Cuif L (2011) Expression of hairy/enhancer of split genes in neural progenitors and neurogenesis domains of the adult zebrafish brain. J Comp Neurol 519(9):1748–1769

    Article  PubMed  CAS  Google Scholar 

  • Chetverukhin VK, Polenov AL (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. I. Ventricular zone cell proliferation. Cell Tissue Res 271(2):341–350

    Article  PubMed  CAS  Google Scholar 

  • Crespo D, Stanfield BB, Cowan WM (1986) Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Exp Brain Res 62(3):541–548

    Article  PubMed  CAS  Google Scholar 

  • Dann JF, Beazley LD (1988) Development of the optic tecta in the frog Limnodynastes dorsalis. Brain Res Dev Brain Res 44(1):21–35

    Article  PubMed  CAS  Google Scholar 

  • Dawley EM, Fingerlin A, Hwang D, John SS, Stankiewicz CA (2000) Seasonal cell proliferation in the chemosensory epithelium and brain of red-backed salamanders, Plethodon cinereus. Brain Behav Evol 56(1):1–13

    Article  PubMed  CAS  Google Scholar 

  • Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460(4):563–572

    Article  PubMed  Google Scholar 

  • DeVoogd TJ (2004) Neural constraints on the complexity of avian song. Brain Behav Evol 63(4):221–232

    Article  PubMed  Google Scholar 

  • Diotel N, Vaillant C, Gueguen MM, Mironov S, Anglade I, Servili A, Pellegrini E, Kah O (2010) Cxcr4 and Cxcl12 expression in radial glial cells of the brain of adult zebrafish. J Comp Neurol 518(24):4855–4876

    Article  PubMed  CAS  Google Scholar 

  • Doetsch F, Scharff C (2001) Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav Evol 58(5):306–322

    Article  PubMed  CAS  Google Scholar 

  • Doetsch F, Garcia-Verdugo JM, 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

    PubMed  CAS  Google Scholar 

  • Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703–716

    Article  PubMed  CAS  Google Scholar 

  • Dong Z, Yang N, Yeo SY, Chitnis A, Guo S (2012) Intralineage directional notch signaling regulates self-renewal and differentiation of asymmetrically dividing radial glia. Neuron 74(1):65–78

    Article  PubMed  CAS  Google Scholar 

  • Ekström P, Johnsson CM, Ohlin LM (2001) Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration (secondary matrix) zones. J Comp Neurol 436(1):92–110

    Article  PubMed  Google Scholar 

  • Encinas JM, Hamani C, Lozano AM, Enikolopov G (2011) Neurogenic hippocampal targets of deep brain stimulation. J Comp Neurol 519(1):6–20

    Article  PubMed  Google Scholar 

  • Endo T, Yoshino J, Kado K, Tochinai S (2007) Brain regeneration in anuran amphibians. Develop Growth Differ 49(2):121–129

    Article  Google Scholar 

  • Evans HE (1952) The correlation of brain pattern and feeding habits in four species of cyprinid fishes. J Comp Neurol 97(1):133–142

    Article  PubMed  CAS  Google Scholar 

  • Finger TE, Drake SK, Kotrschal K, Womble M, Dockstader KC (1991) Postlarval growth of the peripheral gustatory system in the channel catfish, Ictalurus punctatus. J Comp Neurol 314(1):55–66

    Article  PubMed  CAS  Google Scholar 

  • Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 209(2):294–301

    Article  PubMed  CAS  Google Scholar 

  • Font E, Desfilis E, Perez-Canellas MM, Garcia-Verdugo JM (2001) Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav Evol 58(5):276–295

    Article  PubMed  CAS  Google Scholar 

  • Ganz J, Kaslin J, Hochmann S, Freudenreich D, Brand M (2010) Heterogeneity and Fgf dependence of adult neural progenitors in the zebrafish telencephalon. Glia 58(11):1345–1363

    PubMed  Google Scholar 

  • Ganz J, Kaslin J, Freudenreich D, Machate A, Geffarth M, Brand M (2012) Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J Comp Neurol 520(3):633–655

    Article  PubMed  CAS  Google Scholar 

  • Garcia Verdugo JM, Berbel PJ, Lopez Garcia C (1981) Golgi and electron microscopy study of cerebral ependymocytes of the lizard Lacerta galloti. Trab Inst Cajal 72(4):269–278

    PubMed  CAS  Google Scholar 

  • Garcia-Verdugo JM, Farinas I, Molowny A, Lopez-Garcia C (1986) Ultrastructure of putative migrating cells in the cerebral cortex of Lacerta galloti. J Morphol 189(2):189–197

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Goldman SA, Zukhar A, Barami K, Mikawa T, Niedzwiecki D (1996) Ependymal/subependymal zone cells of postnatal and adult songbird brain generate both neurons and nonneuronal siblings in vitro and in vivo. J Neurobiol 30(4):505–520

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Lira G, Lamas M, Romo-Parra H, Gutierrez R (2005) Programmed and induced phenotype of the hippocampal granule cells. J Neurosci 25(30):6939–6946

    Article  PubMed  CAS  Google Scholar 

  • González-Granero S, Lezameta M, García-Verdugo JM (2011) Adult neurogenesis in reptiles. In: Seki T, Sawamoto K, Parent JM, Alvarez-Buylla A (eds) Neurogenesis in the adult brain, vol I. Springer, pp. 169–189

  • Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6(10):777–788

    Article  PubMed  CAS  Google Scholar 

  • Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39(5):749–765

    Article  PubMed  CAS  Google Scholar 

  • Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295(1):263–277

    Article  PubMed  CAS  Google Scholar 

  • Hanaway J (1967) Formation and differentiation of the external granular layer of the chick cerebellum. J Comp Neurol 131(1):1–14

    Article  PubMed  CAS  Google Scholar 

  • Hans S, Kaslin J, Freudenreich D, Brand M (2009) Temporally-controlled site-specific recombination in zebrafish. PLoS One 4(2):e4640

    Article  PubMed  CAS  Google Scholar 

  • Hans S, Freudenreich D, Geffarth M, Kaslin J, Machate A, Brand M (2011) Generation of a non-leaky heat shock-inducible Cre line for conditional Cre/lox strategies in zebrafish. Dev Dyn 240(1):108–115

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hatten ME, Heintz N (1995) Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385–408

    Article  PubMed  CAS  Google Scholar 

  • Hinsch K, Zupanc GK (2007) Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis. Neuroscience 146(2):679–696

    Article  PubMed  CAS  Google Scholar 

  • Holtzman DA, Halpern M (1991) Incorporation of 3H-thymidine in telencephalic structures of the vomeronasal and olfactory systems of embryonic garter snakes. J Comp Neurol 304(3):450–466

    Article  PubMed  CAS  Google Scholar 

  • Hui SP, Dutta A, Ghosh S (2010) Cellular response after crush injury in adult zebrafish spinal cord. Dev Dyn 239(11):2962–2979

    Article  PubMed  Google Scholar 

  • Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11(10):1153–1161

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Tanaka H, Okamoto H, Ohshima T (2010) Characterization of neural stem cells and their progeny in the adult zebrafish optic tectum. Dev Biol 342(1):26–38

    Article  PubMed  CAS  Google Scholar 

  • Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H (2000) Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22(1–2):139–153

    Article  PubMed  CAS  Google Scholar 

  • Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363(1489):101–122

    Article  PubMed  Google Scholar 

  • Kaslin J, Ganz J, Geffarth M, Grandel H, Hans S, Brand M (2009) Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J Neurosci 29(19):6142–6153

    Article  PubMed  CAS  Google Scholar 

  • Kempermann G (2011) Adult Neurogenesis 2. Stem cells and neuronal development in the adult brain, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Kempermann G (2012) New neurons for ‘survival of the fittest’. Nat Rev Neurosci 13(10):727–736

    PubMed  CAS  Google Scholar 

  • Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130(2):391–399

    Article  PubMed  CAS  Google Scholar 

  • Kirn JR (2010) The relationship of neurogenesis and growth of brain regions to song learning. Brain Lang 115(1):29–44

    Article  PubMed  Google Scholar 

  • Kirn JR, Nottebohm F (1993) Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 13(4):1654–1663

    PubMed  CAS  Google Scholar 

  • Kirn JR, Alvarez-Buylla A, Nottebohm F (1991) Production and survival of projection neurons in a forebrain vocal center of adult male canaries. J Neurosci 11(6):1756–1762

    PubMed  CAS  Google Scholar 

  • Kirn J, O'Loughlin B, Kasparian S, Nottebohm F (1994) Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc Natl Acad Sci U S A 91(17):7844–7848

    Article  PubMed  CAS  Google Scholar 

  • Kirsche W (1967) On postembryonic matrix zones in the brain of various vertebrates and their relationship to the study of the brain structure. Z Mikrosk Anat Forsch 77(3):313–406

    PubMed  CAS  Google Scholar 

  • Kirsche W, Kirsche K (1961) Experimental studies on the problem of regeneration and function of the tectum opticum of Carassium carassium L. Z Mikrosk Anat Forsch 67:140–182

    PubMed  CAS  Google Scholar 

  • Kishimoto N, Alfaro-Cervello C, Shimizu K, Asakawa K, Urasaki A, Nonaka S, Kawakami K, Garcia-Verdugo JM, Sawamoto K (2011) Migration of neuronal precursors from the telencephalic ventricular zone into the olfactory bulb in adult zebrafish. J Comp Neurol 519(17):3549–3565

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto N, Shimizu K, Sawamoto K (2012) Neuronal regeneration in a zebrafish model of adult brain injury. Dis Model Mech 5(2):200–209

    Article  PubMed  CAS  Google Scholar 

  • Kizil C, Kaslin J, Kroehne V, Brand M (2012a) Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol 72(3):429–61

    Article  PubMed  Google Scholar 

  • Kizil C, Dudczig S, Kyritsis N, Machate A, Blaesche J, Kroehne V, Brand M (2012b) The chemokine receptor cxcr5 regulates the regenerative neurogenesis response in the adult zebrafish brain. Neural Dev 7(1):27

    Article  PubMed  CAS  Google Scholar 

  • Kizil C, Kyritsis N, Dudczig S, Kroehne V, Freudenreich D, Kaslin J, Brand M (2012c) Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of Gata3. Dev Cell. doi:10.1016/jdevcel.2012.10.014

  • Komada N (1994) Distribution of taste buds in the oropharyngeal cavity of larval and juvenile stages of the cyprinid fish, Tribolodon hakonensis. Jpn J Ichthyol 41:307–311

    Google Scholar 

  • Koster RW, Fraser SE (2001) Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr Biol 11(23):1858–1863

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kroehne V, Brand M (2012) The cellular basis of constitutive and regenerative neurogenesis in the adult zebrafish brain. DGZ Cell News 38(2012/1):12–16

    Google Scholar 

  • Kroehne V, Freudenreich D, Hans S, Kaslin J, Brand M (2011) Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development 138(22):4831–4841

    Article  PubMed  CAS  Google Scholar 

  • Kuroyanagi Y, Okuyama T, Suehiro Y, Imada H, Shimada A, Naruse K, Takeda H, Kubo T, Takeuchi H (2010) Proliferation zones in adult medaka (Oryzias latipes) brain. Brain Res 1323:33–40

    Article  PubMed  CAS  Google Scholar 

  • Kuscha V, Barreiro-Iglesias A, Becker CG, Becker T (2012a) Plasticity of tyrosine hydroxylase and serotonergic systems in the regenerating spinal cord of adult zebrafish. J Comp Neurol 520(5):933–951

    Article  PubMed  CAS  Google Scholar 

  • Kuscha V, Frazer SL, Dias TB, Hibi M, Becker T, Becker CG (2012b) Lesion-induced generation of interneuron cell types in specific dorsoventral domains in the spinal cord of adult zebrafish. J Comp Neurol 520(16):3604–3616

    Article  PubMed  CAS  Google Scholar 

  • Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J, Freudenreich D, Iltzsche A, Brand M (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science. doi:10.1126.science.1228773

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

    Article  PubMed  CAS  Google Scholar 

  • Leonard RB, Coggeshall RE, Willis WD (1978) A documentation of an age related increase in neuronal and axonal numbers in the stingray, Dasyatis sabina, Leseuer. J Comp Neurol 179(1):13–21

    Article  PubMed  CAS  Google Scholar 

  • Li G, Kataoka H, Coughlin SR, Pleasure SJ (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 136(2):327–335

    Article  PubMed  CAS  Google Scholar 

  • Lin JC, Cai L, Cepko CL (2001) The external granule layer of the developing chick cerebellum generates granule cells and cells of the isthmus and rostral hindbrain. J Neurosci 21(1):159–168

    PubMed  CAS  Google Scholar 

  • Lindsey BW, Tropepe V (2006) A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80(6):281–307

    Article  PubMed  CAS  Google Scholar 

  • Lindsey BW, Darabie A, Tropepe V (2012) The cellular composition of neurogenic periventricular zones in the adult zebrafish forebrain. J Comp Neurol 520(10):2275–2316

    Article  PubMed  Google Scholar 

  • Ling C, Zuo M, Alvarez-Buylla A, Cheng MF (1997) Neurogenesis in juvenile and adult ring doves. J Comp Neurol 379(2):300–312

    Article  PubMed  CAS  Google Scholar 

  • Lledo PM, Merkle FT, Alvarez-Buylla A (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31(8):392–400

    Article  PubMed  CAS  Google Scholar 

  • López-García C, Tineo PL, Del Corral J (1984) Increase of the neuron number in some cerebral cortical areas of a lizard, Podarcis hispanica, (Steind., 1870), during postnatal periods of life. J Hirnforsch 25(3):255–259

    PubMed  Google Scholar 

  • Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Martinez-Guijarro FJ, Bernabeu A (1990a) Late generated neurons in the medial cortex of adult lizards send axons that reach the Timm-reactive zones. Brain Res Dev Brain Res 57(2):249–254

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Perez-Sanchez F, Matinez-Guijarro FJ (1990b) Postnatal neurogenesis in the brain of the lizard Podarcis hispanica. Experimental Brain Research Series 19. Springer, Berlin

    Google Scholar 

  • Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Gotz M (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37(5):751–764

    Article  PubMed  CAS  Google Scholar 

  • Marchioro M, Nunes JM, Ramalho AM, Molowny A, Perez-Martinez E, Ponsoda X, Lopez-Garcia C (2005) Postnatal neurogenesis in the medial cortex of the tropical lizard Tropidurus hispidus. Neuroscience 134(2):407–413

    Article  PubMed  CAS  Google Scholar 

  • Marcus RC, Delaney CL, Easter SS Jr (1999) Neurogenesis in the visual system of embryonic and adult zebrafish (Danio rerio). off. Vis Neurosci 16(3):417–424

    Article  PubMed  CAS  Google Scholar 

  • Margotta V, Morelli A, Caronti B (2005) Expression of PCNA positivity in the brain of normal adult heterothermic vertebrates: further observations. Ital J Anat Embryol 110(2):59–74

    PubMed  Google Scholar 

  • Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41(2):281–294

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Guijarro FJ, Blasco-Ibáñez, López-García (1994) Postnatal increase of GABA and PV-IR cells in the cerebral cortex of the lizard Podacris hispanica. Brain Res 634:168–172

  • März M, Chapouton P, Diotel N, Vaillant C, Hesl B, Takamiya M, Lam CS, Kah O, Bally-Cuif L, Strahle U (2010) Heterogeneity in progenitor cell subtypes in the ventricular zone of the zebrafish adult telencephalon. Glia 58(7):870–888

    PubMed  Google Scholar 

  • März M, Schmidt R, Rastegar S, Strahle U (2011) Regenerative response following stab injury in the adult zebrafish telencephalon. Dev Dyn 240(9):2221–2231

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meyer RL (1978) Evidence from thymidine labeling for continuing growth of retina and tectum in juvenile goldfish. Exp Neurol 59(1):99–111

    Article  PubMed  CAS  Google Scholar 

  • Mezey S, Krivokuca D, Balint E, Adorjan A, Zachar G, Csillag A (2012) Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J Comp Neurol 520(1):100–116

    Article  PubMed  CAS  Google Scholar 

  • Métin C, Alvarez C, Moudoux D, Vitalis T, Pieau C, Molnár Z (2007) Conserved pattern of tangential migration during forebrain development. Development 134:2815–2827

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Morales D, Hatten ME (2006) Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J Neurosci 26(47):12226–12236

    Article  PubMed  CAS  Google Scholar 

  • Nguyen V, Deschet K, Henrich T, Godet E, Joly JS, Wittbrodt J, Chourrout D, Bourrat F (1999) Morphogenesis of the optic tectum in the medaka (Oryzias latipes): a morphological and molecular study, with special emphasis on cell proliferation. J Comp Neurol 413(3):385–404

    Article  PubMed  CAS  Google Scholar 

  • Northcutt RG (2011) Paleontology. Evolving large and complex brains. Science 332(6032):926–927

    Article  PubMed  CAS  Google Scholar 

  • Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214(4527):1368–1370

    Article  PubMed  CAS  Google Scholar 

  • Nottebohm F (1985) Neuronal replacement in adulthood. Ann N Y Acad Sci 457:143–161

    Article  PubMed  CAS  Google Scholar 

  • Ott R, Zupanc GK, Horschke I (1997) Long-term survival of postembryonically born cells in the cerebellum of gymnotiform fish, Apteronotus leptorhynchus. Neurosci Lett 221(2–3):185–188

    Article  PubMed  CAS  Google Scholar 

  • Parish CL, Beljajeva A, Arenas E, Simon A (2007) Midbrain dopaminergic neurogenesis and behavioural recovery in a salamander lesion-induced regeneration model. Development 134(15):2881–2887

    Article  PubMed  CAS  Google Scholar 

  • Paton JA, Nottebohm FN (1984) Neurons generated in the adult brain are recruited into functional circuits. Science 225(4666):1046–1048

    Article  PubMed  CAS  Google Scholar 

  • Peñafiel A, Gutierrez A, Martin R, Mar Perez-Canellas M, de la Calle A (1996) A tangential neuronal migration in the olfactory bulbs of adult lizards. Neuroreport 7(7):1257–1260

    Article  PubMed  Google Scholar 

  • Pérez-Cañellas MM, García-Verdugo JM (1996) Adult neurogenesis in the telencephalon of a lizard: a [3H]thymidine autoradiographic and bromodeoxyuridine immunocytochemical study. Brain Res Dev Brain Res 93(1–2):49–61

    Article  PubMed  Google Scholar 

  • Pérez-Cañellas MM, Font E, García-Verdugo JM (1997) Postnatal neurogenesis in the telencephalon of turtles: evidence for nonradial migration of new neurons from distant proliferative ventricular zones to the olfactory bulbs. Brain Res Dev Brain Res 101(1–2):125–137

    Article  PubMed  Google Scholar 

  • Platel R (1974) Poids encéphalique et indice d'encéphalisation chez les reptiles sauriens. Zool Anz 192:332–382

    Google Scholar 

  • Polenov AL, Chetverukhin VK (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. II. Types of neuronal cells produced. Cell Tissue Res 271(2):351–362

    Article  PubMed  CAS  Google Scholar 

  • Ponti G, Peretto P, Bonfanti L (2006) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294(1):168–180

    Article  PubMed  CAS  Google Scholar 

  • Ponti G, Peretto P, Bonfanti L (2008) Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS One 3(6):e2366

    Article  PubMed  CAS  Google Scholar 

  • Potten CS (2004) Keratinocyte stem cells, label-retaining cells and possible genome protection mechanisms. J Investig Dermatol Symp Proc 9(3):183–195

    Article  PubMed  CAS  Google Scholar 

  • Rahmann H (1968) Autoradiographic studies on the DNA metabolism (mitosis frequency) in the CNS of Brachydanio rerio Ham. Buch. (Cyprinidae, Pisces). J Hirnforsch 10(3):279–284

    PubMed  CAS  Google Scholar 

  • Raucci F, Di Fiore MM, Pinelli C, D'Aniello B, Luongo L, Polese G, Rastogi RK (2006) Proliferative activity in the frog brain: a PCNA-immunohistochemistry analysis. J Chem Neuroanat 32(2–4):127–142

    Article  PubMed  CAS  Google Scholar 

  • Raymond PA, Easter SS Jr (1983) Postembryonic growth of the optic tectum in goldfish. I. Location of germinal cells and numbers of neurons produced. J Neurosci 3(5):1077–1091

    PubMed  CAS  Google Scholar 

  • Raymond PA, Easter SS Jr, Burnham JA, Powers MK (1983) Postembryonic growth of the optic tectum in goldfish. II. Modulation of cell proliferation by retinal fiber input. J Neurosci 3(5):1092–1099

    PubMed  CAS  Google Scholar 

  • Reimer MM, Sorensen I, Kuscha V, Frank RE, Liu C, Becker CG, Becker T (2008) Motor neuron regeneration in adult zebrafish. J Neurosci 28(34):8510–8516

    Article  PubMed  CAS  Google Scholar 

  • Reimer MM, Kuscha V, Wyatt C, Sorensen I, Frank RE, Knuwer M, Becker T, Becker CG (2009) Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. J Neurosci 29(48):15073–15082

    Article  PubMed  CAS  Google Scholar 

  • Richter W, Kranz D (1981a) Autoradiographic investigations on postnatal proliferative activity of the telencephalic and diencephalic matrix-zones in the axolotl (Ambystoma mexicanum), with special references to the olfactory organ (author’s transl). Z Mikrosk Anat Forsch 95(6):883–904

    PubMed  CAS  Google Scholar 

  • Richter W, Kranz D (1981b) Autoradiographic investigations on postnatal proliferative activity of the matrix-zones of the brain in the trout (Salmo irideus) (author’s transl). Z Mikrosk Anat Forsch 95(4):491–520

    PubMed  CAS  Google Scholar 

  • Rothenaigner I, Krecsmarik M, Hayes JA, Bahn B, Lepier A, Fortin G, Gotz M, Jagasia R, Bally-Cuif L (2011) Clonal analysis by distinct viral vectors identifies bona fide neural stem cells in the adult zebrafish telencephalon and characterizes their division properties and fate. Development 138(8):1459–1469

    Article  PubMed  CAS  Google Scholar 

  • Ryder EF, Cepko CL (1994) Migration patterns of clonally related granule cells and their progenitors in the developing chick cerebellum. Neuron 12(5):1011–1028

    Article  PubMed  CAS  Google Scholar 

  • Scharff C, Kirn JR, Grossman M, Macklis JD, Nottebohm F (2000) Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25(2):481–492

    Article  PubMed  CAS  Google Scholar 

  • Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21(18):7153–7160

    PubMed  CAS  Google Scholar 

  • Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478(4):359–378

    Article  PubMed  Google Scholar 

  • Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5(2):146–156

    Article  PubMed  CAS  Google Scholar 

  • Simmons AM, Tanyu LH, Horowitz SS, Chapman JA, Brown RA (2008) Developmental and regional patterns of GAP-43 immunoreactivity in a metamorphosing brain. Brain Behav Evol 71(4):247–262

    Article  PubMed  Google Scholar 

  • Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32(12):638–647

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis A, Barbas H, Dermon CR (2004) Late granule cell genesis in quail cerebellum. J Comp Neurol 474(2):173–189

    Article  PubMed  Google Scholar 

  • Stensaas LJ, Stensaas SS (1968) Light microscopy of glial cells in turtles and birds. Z Zellforsch Mikrosk Anat 91(3):315–340

    Article  PubMed  CAS  Google Scholar 

  • Stevenson JA, Yoon MG (1981) Mitosis of radial glial cells in the optic tectum of adult goldfish. J Neurosci 1(8):862–875

    PubMed  CAS  Google Scholar 

  • Tanaka EM, Ferretti P (2009) Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci 10(10):713–723

    Article  PubMed  CAS  Google Scholar 

  • Tozzini ET, Baumgart M, Battistoni G, Cellerino A (2011) Adult neurogenesis in the short-lived teleost Nothobranchius furzeri: localization of neurogenic niches, molecular characterization and effects of aging. Aging Cell 11(2):241–251

    Article  CAS  Google Scholar 

  • Vellema M, van der Linden A, Gahr M (2010) Area-specific migration and recruitment of new neurons in the adult songbird brain. J Comp Neurol 518(9):1442–1459

    Article  PubMed  Google Scholar 

  • Volkmann K, Rieger S, Babaryka A, Koster RW (2008) The zebrafish cerebellar rhombic lip is spatially patterned in producing granule cell populations of different functional compartments. Dev Biol 313(1):167–180

    Article  PubMed  CAS  Google Scholar 

  • Walton C, Pariser E, Nottebohm F (2012) The zebra finch paradox: song is little changed, but number of neurons doubles. J Neurosci 32(3):761–774

    Article  PubMed  CAS  Google Scholar 

  • Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16(9):1681–1689

    Article  PubMed  Google Scholar 

  • Wullimann MF, Mueller T, Distel M, Babaryka A, Grothe B, Koster RW (2011) The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front Neuroanat 5:27

    Article  PubMed  Google Scholar 

  • Yeo SY, Kim M, Kim HS, Huh TL, Chitnis AB (2007) Fluorescent protein expression driven by her4 regulatory elements reveals the spatiotemporal pattern of Notch signaling in the nervous system of zebrafish embryos. Dev Biol 301(2):555–567

    Article  PubMed  CAS  Google Scholar 

  • Zikopoulos B, Kentouri M, Dermon CR (2000) Proliferation zones in the adult brain of a sequential hermaphrodite teleost species (Sparus aurata). Brain Behav Evol 56(6):310–322

    Article  PubMed  CAS  Google Scholar 

  • Zupanc GK (2001) Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav Evol 58(5):250–275

    Article  PubMed  CAS  Google Scholar 

  • Zupanc GK, Clint SC (2003) Potential role of radial glia in adult neurogenesis of teleost fish. Glia 43(1):77–86

    Article  PubMed  Google Scholar 

  • Zupanc GK, Horschke I (1995) Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J Comp Neurol 353(2):213–233

    Article  PubMed  CAS  Google Scholar 

  • Zupanc GK, Sirbulescu RF (2011) Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Eur J Neurosci 34(6):917–929

    Article  PubMed  Google Scholar 

  • Zupanc GK, Hinsch K, Gage FH (2005) Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488(3):290–319

    Article  PubMed  Google Scholar 

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Acknowledgments

The work in the Brand Laboratory is supported by research grants from the Deutsche Forschungsgemeinschaft (SFB 655), European Union (ZF Health) and a seed grant by the Center for Regenerative Therapies Dresden. The authors would like to thank Stefan Hans, Caghan Kizil and Volker Kroehne for the comments on previous versions of the manuscript.

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  1. DFG-Center for Regenerative Therapies Dresden-Cluster of Excellence, University of Technology Dresden, Fetscherstr. 105, 01307, Dresden, Germany

    Heiner Grandel & Michael Brand

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  1. Heiner Grandel
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  2. Michael Brand
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Correspondence to Michael Brand.

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Communicated by V. Hartenstein

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Grandel, H., Brand, M. Comparative aspects of adult neural stem cell activity in vertebrates. Dev Genes Evol 223, 131–147 (2013). https://doi.org/10.1007/s00427-012-0425-5

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