Comparative aspects of adult neural stem cell activity in vertebrates

Development Genes and Evolution

Volumn 223, Issue 1-2, 2013, Pages 131-147

  Grandel, Heiner ^a   Brand, Michael ^a  

^a CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Adult neurogenesis; Astroglia; Neural stem cell; Neuroepithelial cell; Radial glia; Regeneration; Zebrafish

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN S100B; VIMENTIN;

AMPHIBIA; BIRD; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CEREBELLUM; DENTATE GYRUS; DOPAMINERGIC NERVE CELL; FISH; GABAERGIC SYSTEM; GRANULE CELL; HIPPOCAMPUS; IMMUNOREACTIVITY; INTERNEURON; MORPHOGENESIS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM; NONHUMAN; OLFACTORY BULB; PHYLOGENY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REGENERATION; REPTILE; REVIEW; SIGNAL TRANSDUCTION; SUPERIOR COLLICULUS; TELENCEPHALON; VERTEBRATE; ZEBRA FISH;

ADULT STEM CELLS; ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; NEURAL STEM CELLS; NEUROGENESIS; REGENERATION; STEM CELL NICHE; VERTEBRATES;

AVES; DANIO RERIO; MAMMALIA; TELEOSTEI; VERTEBRATA;

EID: 84872979322     PISSN: 0949944X     EISSN: 1432041X     Source Type: Journal    
DOI: 10.1007/s00427-012-0425-5     Document Type: Review

References (174)

1. 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 (Pubitemid 44041332)
2. Airey DC, DeVoogd TJ (2000) Greater song complexity is associated with augmented song system anatomy in zebra finches. Neuroreport 11(10):2339-2344 (Pubitemid 30485588)
3. 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
4. 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
5. 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 (Pubitemid 20368500)
6. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124(3):319-335
7. 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
8. Alvarez-Buylla A, Kirn JR (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33(5):585-601 (Pubitemid 27456454)
9. 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
10. 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 (Pubitemid 20224505)
11. 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 (Pubitemid 24273426)
12. 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 (Pubitemid 28112924)
13. 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
14. 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
15. 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
16. 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
17. 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 (Pubitemid 12058817)
18. 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 (Pubitemid 32274746)
19. Becker CG, Becker T (2008) Adult zebrafish as a model for successful central nervous system regeneration. Restor Neurol Neurosci 26(2-3):71-80
20. 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 (Pubitemid 27053550)
21. 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 (Pubitemid 41316568)
22. 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
23. 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 (Pubitemid 20359193)
24. 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 (Pubitemid 36143738)
25. 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
26. Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals - a theme with many variations. Eur J Neurosci 34(6):930-950
27. 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 (Pubitemid 15012466)
28. 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 (Pubitemid 20305195)
29. 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
30. Byrd CA, Brunjes PC (1998) Addition of new cells to the olfactory bulb of adult zebrafish. Ann N Y Acad Sci 855:274-276 (Pubitemid 29109994)
31. Byrd CA, Brunjes PC (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105(4):793-801 (Pubitemid 32786793)
32. Cerveny KL, Varga M, Wilson SW (2012) Continued growth and circuit building in the anamniote visual system. Dev Neurobiol 72:328-345
33. 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
34. 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
35. 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
36. 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 (Pubitemid 23077905)
37. 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 (Pubitemid 16035934)
38. Dann JF, Beazley LD (1988) Development of the optic tecta in the frog Limnodynastes dorsalis. Brain Res Dev Brain Res 44(1):21-35
39. 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
40. 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 (Pubitemid 36528662)
41. DeVoogd TJ (2004) Neural constraints on the complexity of avian song. Brain Behav Evol 63(4):221-232 (Pubitemid 38490189)
42. 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
43. Doetsch F, Scharff C (2001) Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav Evol 58(5):306-322 (Pubitemid 34458035)
44. 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 (Pubitemid 27263818)
45. 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 (Pubitemid 29278045)
46. 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
47. 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 (Pubitemid 32591547)
48. Encinas JM, Hamani C, Lozano AM, Enikolopov G (2011) Neurogenic hippocampal targets of deep brain stimulation. J Comp Neurol 519(1):6-20
49. Endo T, Yoshino J, Kado K, Tochinai S (2007) Brain regeneration in anuran amphibians. Develop Growth Differ 49(2):121-129
50. Evans HE (1952) The correlation of brain pattern and feeding habits in four species of cyprinid fishes. J Comp Neurol 97(1):133-142
51. 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
52. Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol 209(2):294-301 (Pubitemid 351174127)
53. 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 (Pubitemid 34458033)
54. 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
55. 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
56. 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
57. 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
58. 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 (Pubitemid 13097195)
59. 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 (Pubitemid 26256774)
60. 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 (Pubitemid 41077001)
61. 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
62. Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6(10):777-788 (Pubitemid 41726116)
63. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39(5):749-765 (Pubitemid 37088088)
64. 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 (Pubitemid 44041336)
65. Hanaway J (1967) Formation and differentiation of the external granular layer of the chick cerebellum. J Comp Neurol 131(1):1-14
66. Hans S, Kaslin J, Freudenreich D, Brand M (2009) Temporally-controlled site-specific recombination in zebrafish. PLoS One 4(2):e4640
67. 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
68. Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229(1):15-30 (Pubitemid 32061711)
69. Hatten ME, Heintz N (1995) Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385-408
70. 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 (Pubitemid 46617060)
71. 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
72. Hui SP, Dutta A, Ghosh S (2010) Cellular response after crush injury in adult zebrafish spinal cord. Dev Dyn 239(11):2962-2979
73. 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
74. 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
75. 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 (Pubitemid 30098914)
76. 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 (Pubitemid 350174581)
77. 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
78. Kempermann G (2011) Adult Neurogenesis 2. Stem cells and neuronal development in the adult brain, 2nd edn. Oxford University Press, New York
79. Kempermann G (2012) New neurons for 'survival of the fittest'. Nat Rev Neurosci 13(10):727-736
80. 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 (Pubitemid 36175935)
81. Kirn JR (2010) The relationship of neurogenesis and growth of brain regions to song learning. Brain Lang 115(1):29-44
82. Kirn JR, Nottebohm F (1993) Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 13(4):1654-1663 (Pubitemid 23095407)
83. 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
84. 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 (Pubitemid 24253841)
85. 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
86. 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
87. 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
88. Kishimoto N, Shimizu K, Sawamoto K (2012) Neuronal regeneration in a zebrafish model of adult brain injury. Dis Model Mech 5(2):200-209
89. Kizil C, Kaslin J, Kroehne V, Brand M (2012a) Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol 72(3):429-61
90. 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
91. 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
92. 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
93. Koster RW, Fraser SE (2001) Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr Biol 11(23):1858-1863 (Pubitemid 33136525)
94. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184
95. Kroehne V, Brand M (2012) The cellular basis of constitutive and regenerative neurogenesis in the adult zebrafish brain. DGZ Cell News 38(1):12-16
96. 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
97. 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
98. 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
99. 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
100. 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
101. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60(4):585-595 (Pubitemid 20083815)
102. 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 (Pubitemid 8373198)
103. 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
104. 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 (Pubitemid 32098738)
105. Lindsey BW, Tropepe V (2006) A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80(6):281-307 (Pubitemid 46111018)
106. 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
107. Ling C, Zuo M, Alvarez-Buylla A, Cheng MF (1997) Neurogenesis in juvenile and adult ring doves. J Comp Neurol 379(2):300-312 (Pubitemid 27113621)
108. Lledo PM, Merkle FT, Alvarez-Buylla A (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31(8):392-400
109. 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 (Pubitemid 14010420)
110. 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
111. 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
112. 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 (Pubitemid 36288548)
113. 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 (Pubitemid 41111771)
114. 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 (Pubitemid 29245409)
115. 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 (Pubitemid 41539922)
116. 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 (Pubitemid 29494153)
117. 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
118. 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
119. 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
120. Merkle FT, Mirzadeh Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317(5836):381-384 (Pubitemid 47106379)
121. Meyer RL (1978) Evidence from thymidine labeling for continuing growth of retina and tectum in juvenile goldfish. Exp Neurol 59(1):99-111 (Pubitemid 8290042)
122. 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
123. 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
124. 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
125. Morales D, Hatten ME (2006) Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J Neurosci 26(47):12226-12236 (Pubitemid 44808389)
126. 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 (Pubitemid 29445026)
127. Northcutt RG (2011) Paleontology. Evolving large and complex brains. Science 332(6032):926-927
128. Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214(4527):1368-1370 (Pubitemid 12135127)
129. Nottebohm F (1985) Neuronal replacement in adulthood. Ann N Y Acad Sci 457:143-161 (Pubitemid 16129908)
130. 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 (Pubitemid 27049229)
131. 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 (Pubitemid 47305061)
132. Paton JA, Nottebohm FN (1984) Neurons generated in the adult brain are recruited into functional circuits. Science 225(4666):1046-1048 (Pubitemid 14066321)
133. 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 (Pubitemid 26231595)
134. 3H]thymidine autoradiographic and bromodeoxyuridine immunocytochemical study. Brain Res Dev Brain Res 93(1-2):49-61 (Pubitemid 26188233)
135. 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 (Pubitemid 27323807)
136. Platel R (1974) Poids encéphalique et indice d'encé phalisation chez les reptiles sauriens. Zool Anz 192:332-382
137. 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 (Pubitemid 23077906)
138. 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
139. 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
140. Potten CS (2004) Keratinocyte stem cells, label-retaining cells and possible genome protection mechanisms. J Investig Dermatol Symp Proc 9(3):183-195 (Pubitemid 39108121)
141. 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
142. 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 (Pubitemid 44780072)
143. 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 (Pubitemid 13135431)
144. 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 (Pubitemid 13135432)
145. 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
146. 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
147. 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
148. 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 (Pubitemid 12246277)
149. 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
150. 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 (Pubitemid 24178194)
151. 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
152. 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 (Pubitemid 32846963)
153. 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 (Pubitemid 39305128)
154. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5(2):146-156 (Pubitemid 38160289)
155. 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 (Pubitemid 351693900)
156. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32(12):638-647
157. 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 (Pubitemid 40110761)
158. Stamatakis A, Barbas H, Dermon CR (2004) Late granule cell genesis in quail cerebellum. J Comp Neurol 474(2):173-189 (Pubitemid 38702681)
159. Stensaas LJ, Stensaas SS (1968) Light microscopy of glial cells in turtles and birds. Z Zellforsch Mikrosk Anat 91(3):315-340
160. Stevenson JA, Yoon MG (1981) Mitosis of radial glial cells in the optic tectum of adult goldfish. J Neurosci 1(8):862-875 (Pubitemid 11025875)
161. Tanaka EM, Ferretti P (2009) Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci 10(10):713-723
162. 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
163. 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
164. 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 (Pubitemid 350298311)
165. 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
166. 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 (Pubitemid 35370700)
167. 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
168. 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 (Pubitemid 46073984)
169. 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 (Pubitemid 32417741)
170. Zupanc GK (2001) Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav Evol 58(5):250-275 (Pubitemid 34458032)
171. Zupanc GK, Clint SC (2003) Potential role of radial glia in adult neurogenesis of teleost fish. Glia 43(1):77-86 (Pubitemid 36781700)
172. 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
173. 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
174. 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 (Pubitemid 40934690)