Adult neurogenesis and neuronal regeneration in the brain of teleost fish

Journal of Physiology Paris

Volumn 102, Issue 4-6, 2008, Pages 357-373

  Zupanc, Günther K H ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

Apteronotus leptorhynchus; Brain injury; Intrinsic stem cells; Proteomics; Replacement therapy; Zebrafish

Indexed keywords

CELL PROTEIN;

APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN INJURY; BRAIN REGION; CELL COUNT; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; FUNCTIONAL PROTEOMICS; GENETIC ASSOCIATION; GENOME ANALYSIS; GLIA; GLIA CELL; GROWTH RATE; GROWTH REGULATION; GYMNOTIFORMES; HIPPOCAMPUS; MAMMAL; NERVE CELL; NERVE CELL NETWORK; NERVE FIBER REGENERATION; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PHYLOGENY; SENSE ORGAN; SURVIVAL TIME; TELEOST; ZEBRA FISH;

ADULT STEM CELLS; ANIMALS; BRAIN; CELL PROLIFERATION; FISHES; NERVE REGENERATION; NEUROGENESIS;

EID: 58249125893     PISSN: 09284257     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphysparis.2008.10.007     Document Type: Article

References (139)

1. Alonso J.R., Lara J., Vecino E., Coveñas R., and Aijón J. Cell proliferation in the olfactory bulb of adult freshwater teleosts. J. Anat. 163 (1989) 155-163
2. Altman J. 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 (1969) 433-458
3. Altman J., and Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124 (1965) 319-336
4. Anderson M.J., Waxman S.G., and Laufer M. Fine structure of regenerated ependyma and spinal cord in Sternarchus albifrons. Anat. Rec. 205 (1983) 73-83
5. Anderson M.J., Waxman S.G., Lee Y.-L., and Eng L.F. Molecular differentiation of neurons from ependyma-derived cells in tissue cultures of regenerating teleost spinal cord. Mol. Brain Res. 2 (1987) 131-136
6. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 (2002) 963-970
7. Barnea A., and Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl. Acad. Sci. USA 91 (1994) 11217-11221
8. Bass A.H. Evolution of the vestibulolateral lobe of the cerebellum in electroreceptive and nonelectroreceptive teleosts. J. Morphol. 174 (1982) 335-348
9. Beattie M.S., Farooqui A.A., and Bresnahan J.C. Review of current evidence for apoptosis after spinal cord injury. J. Neurotrauma 17 (2000) 915-925
10. Becker T., Wullimann M.F., Becker C.G., Bernhardt R.R., and Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J. Comp. Neurol. 377 (1997) 577-595
11. Bédard A., and Parent A. Evidence of newly generated neurons in the human olfactory bulb. Dev. Brain Res. 151 (2004) 159-168
12. Bell C., Bodznick D., Montgomery J., and Bastian J. The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav. Evol. 50 Suppl. 1 (1997) 17-31
13. Braford M.R. Comparative aspects of forebrain organization in the ray-finned fishes: touchstones or nor?. Brain Behav. Evol. 46 (1995) 259-274
14. Brain W.R., and Walton J.N. Brain's Diseases of the Nervous System. seventh ed. (1969), Oxford University Press, London
15. Butler A.B. Topography and topology of the teleost telencephalon: a paradoxon resolved. Neurosci. Lett. 293 (2000) 95-98
16. Byrd C.A., and Brunjes P.C. Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105 (2001) 793-801
17. Caddy K.W.T., and Biscoe T.J. The number of Purkinje cells and olive neurones in the normal and lurcher mutant mouse. Brain Res. 111 (1976) 396-398
18. Cameron D.A. Cellular proliferation and neurogenesis in the injured retina of adult zebrafish. Vis. Neurosci. 17 (2000) 789-797
19. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435 (2001) 406-417
20. Candal E., Anadón R., DeGrip W.J., and Rodríguez-Moldes I. Patterns of cell proliferation and cell death in the developing retina and optic tectum of the brown trout. Dev. Brain Res. 154 (2005) 101-119
21. Carlsen J., De Olmos J., and Heimer L. Tracing of two-neuron pathways in the olfactory system by the aid of transneuronal degeneration: projections to the amygdaloid body and hippocampal formation. J. Comp. Neurol. 208 (1982) 196-208
22. Chen J., Magavi S.S.P., and Macklis J.D. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc. Natl. Acad. Sci. USA 101 (2004) 16357-16362
23. Clint S.C., and Zupanc G.K.H. Neuronal regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: guidance of migrating young cells by radial glia. Dev. Brain Res. 130 (2001) 15-23
24. Corotto F.S., Henegar J.A., and Maruniak J.A. Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci. Lett. 149 (1993) 111-114
25. Corwin J.T. Postembryonic production and aging of inner ear hair cells in sharks. J. Comp. Neurol. 201 (1981) 541-553
26. Curtis M.A., Kam M., Nannmark U., Anderson M.F., Axell M.Z., Wikkelso C., Holtas S., van Roon-Mom W.M.C., Björk-Eriksson T., Nordborg C., et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315 (2007) 1243-1249
27. Doyle L.M.F., Stafford P.P., and Roberts B.L. Recovery of locomotion correlated with axonal regeneration after a complete spinal transection in the eel. Neuroscience 107 (2001) 169-179
28. Ekström P., Johnsson C.-M., and Ohlin L.-M. 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 (2001) 92-110
29. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998) 1313-1317
30. Fontana X., Nacher J., Soriano E., and Del Rio J.A. Cell proliferation in the adult hippocampal formation of rodents and its modulation by entorhinal and fimbria-fornix afferents. Cereb. Cortex 16 (2006) 301-312
31. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., et al. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. New Engl. J. Med. 344 (2001) 710-719
32. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119 (1992) 493-501
33. Gerhard G.S., Kauffman E.J., Wang X., Stewart R., Moore J.L., Kasales C.J., Demidenko E., and Cheng K.C. Life spans and senescent phenotypes in two strains of zebrafish (Danio rerio). Exp. Gerontol. 37 (2002) 1055-1068
34. Gisselsson D., and Höglund M. Connecting mitotic instability and chromosome aberrations in cancer: can telomeres bridge the gap?. Semin. Cancer Biol. 15 (2005) 13-23
35. Gould E., Reeves A.J., Fallah M., Tanapat P., Gross C.G., and Fuchs E. Hippocampal neurogenesis in adult Old World primates. Proc. Natl. Acad. Sci. USA 96 (1999) 5263-5267
36. Grandel H., Kaslin J., Ganz J., Wenzel I., and Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 295 (2006) 263-277
37. Graziadei P.P., and Graziadei G.A. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8 (1979) 1-18
38. Han Z.-G., Zhang Q.-H., Ye M., Kan L.-X., Gu B.-W., He K.-L., Shi S.-L., Zhou J., Fu G., Mao M., et al. Molecular cloning of six novel Krüppel-like zinc finger genes from hematopoietic cells and identification of a novel transregulatory domain KRNB. J. Biol. Chem. 274 (1999) 35741-35748
39. Herculano-Houzel S., and Lent R. Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J. Neurosci. 25 (2005) 2518-2521
40. Hinsch K., and Zupanc G.K.H. Isolation, cultivation, and differentiation of neural stem cells from adult fish brain. J. Neurosci. Meth. 158 (2006) 75-88
41. Hinsch K., and Zupanc G.K.H. Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis. Neuroscience 146 (2007) 679-696
42. Hitchcock P.F., Lindsey Myhr K.J., Easter Jr. S.S., Mangione-Smith R., and Jones D.D. Local regeneration in the retina of the goldfish. J. Neurobiol. 23 (1992) 187-203
43. Insausti R., Marcos P., Arroyo-Jimenez M.M., Blaizot X., and Martinez-Marcos A. Comparative aspects of the olfactory portion of the entorhinal cortex and its projection to the hippocampus in rodents, nonhuman primates, and the human brain. Brain Res. Bull. 57 (2002) 557-560
44. Johns P.R., and Easter S.S.J. Growth of the adult goldfish eye: II. Increase in retinal cell number. J. Comp. Neurol. 176 (1977) 331-342
45. Kaplan M.S., and Bell D.H. Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J. Neurosci. 4 (1984) 1429-1441
46. Kaplan M.S., McNelly N.A., and Hinds J.W. Population dynamics of adult-formed granule neurons of the rat olfactory bulb. J. Comp. Neurol. 239 (1985) 117-125
47. Kaushal D., Contos J.J.A., Treuner K., Yang A.H., Kingsbury M.A., Rehen S.K., McConnell M.J., Okabe M., Barlow C., and Chun J. Alteration of gene expression by chromosome loss in the postnatal mouse brain. J. Neurosci. 23 (2003) 5599-5606
48. Kempermann G., Gast D., Kronenberg G., Yamaguchi M., and Gage F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130 (2003) 391-399
49. Kerr J.F.R., Gobé G.C., Winterford C.M., and Harmon B.V. Anatomical methods in cell death. In: Schwartz L.M., and Osborne B.A. (Eds). Cell Death (1995), Academic Press, San Diego 1-27
50. Kingsbury M.A., Friedman B., McConnell M.J., Rehen S.K., Yang A.H., Kaushal D., and Chun J. Aneuploid neurons are functionally active and integrated into brain circuitry. Proc. Natl. Acad. Sci. USA 102 (2005) 6143-6147
51. Kornack D.R., and Rakic P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. USA 96 (1999) 5768-5773
52. Koumans J.T.M., and Akster H.A. Myogenic cells in development and growth of fish. Comp. Biochem. Physiol. 110A (1995) 3-20
53. Kranz D., and Richter W. Autoradiographische Untersuchungen über die Lokalisation der Matrixzonen des Diencephalons von juvenilen und adulten Lebistes reticulatus (Teleostei). Z. Mikrosk-anat Forsch. 82 (1970) 42-66
54. Kranz D., and Richter W. Autoradiographische Untersuchungen zur DNS-Synthese im Cerebellum und in der Medulla oblongata von Teleostiern verschiedenen Lebensalters. Z. Mikrosk-anat Forsch. 82 (1970) 264-292
55. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19 (1996) 312-318
56. Lee T.H., Lwu S., Kim J., and Pelletier J. Inhibition of Wilms tumor 1 transactivation by bone marrow zinc finger 2, a novel transcriptional repressor. J. Biol. Chem. 277 (2002) 44826-44837
57. Liou A.K.F., Clark R.S., Henshall D.C., Yin X.-M., and Chen J. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog. Neurobiol. 69 (2003) 103-142
58. Lois C., and Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 264 (1994) 1145-1148
59. Lois C., Garcia-Verdugo J.M., and Alvarez-Buylla A. Chain migration of neuronal precursors. Science 271 (1996) 978-981
60. López-García C., Molowny A., García-Verdugo J.M., and Ferrer I. Delayed postnatal neurogenesis in the cerebral cortex of lizards. Dev. Brain Res. 471 (1988) 167-174
61. Lund L.M., and McQuarrie I.G. Axonal regrowth upregulates β-actin and Jun D mRNA expression. J. Neurobiol. 31 (1996) 476-486
62. Lund L.M., Machado V.M., and McQuarrie I.G. Increased β-actin and tubulin polymerization in regrowing axons: relationship to the conditioning lesion effect. Exp. Neurol. 178 (2002) 306-312
63. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons from the forebrain subventricular zone. Neuron 11 (1993) 173-189
64. Magavi S.S., Leavitt B.R., and Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 405 (2000) 951-955
65. Magrassi L., and Graziadei P.P. Cell death in the olfactory epithelium. Anat. Embryol. 192 (1995) 77-87
66. Maler L., Sas E., Johnston S., and Ellis W. An atlas of the brain of the electric fish Apteronotus leptorhynchus. J. Chem. Neuroanat. 4 (1991) 1-38
67. Matsukawa T., Arai K., Koriyama Y., Liu Z., and Kato S. Axonal regeneration of fish optic nerve after injury. Biol. Pharm. Bull. 27 (2004) 445-451
68. Meyer R.L., Sakurai K., and Schauwecker E. Topography of regenerating optic fibers in goldfish traced with local wheat germ injections into retina: evidence for discontinuous microtopography in the retinotectal projection. J. Comp. Neurol. 239 (1985) 27-43
69. Modak S.P., and Bollum F.J. Detection and measurement of single-strand breaks in nuclear DNA in fixed lens sections. Exp. Cell. Res. 75 (1972) 307-313
70. Moore S., and Thanos S. The concept of microglia in relation to central nervous system disease and regeneration. Prog. Neurobiol. 48 (1996) 441-460
71. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., Tamura A., Kirino T., and Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110 (2002) 429-441
72. Nieuwenhuys R., and Meek J. The telencephalon of actinopterygian fishes. In: Jones E.G., and Peters A. (Eds). Comparative Structure and Evolution of the Cerebral Cortex (1990), Plenum, New York 31-73
73. Northcutt R.G. The forebrain of gnathostomes: in search of a morphotype. Brain Behav. Evol. 46 (1995) 275-318
74. Northcutt R.G., and Braford M.R. New observations on the organization and evolution of the telencephalon of actinopterygian fishes. In: Ebbesson S.O.E. (Ed). Comparative Neurology of the Telencephalon (1980), Plenum, New York 41-98
75. Osada T., Kusakabe H., Akutsu H., Yagi T., and Yanagimachi R. Adult murine neurons: their chromatin and chromosome changes and failure to support embryonic development as revealed by nuclear transfer. Cytogenet. Genome Res. 97 (2002) 7-12
76. Ott R., Zupanc G.K.H., and Horschke I. Long-term survival of postembryonically born cells in the cerebellum of gymnotiform fish, Apteronotus leptorhynchus. Neurosci. Lett. 221 (1997) 185-188
77. Otteson D.C., and Hitchcock P.F. Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res. 43 (2003) 927-936
78. Paulin M.G. The role of the cerebellum in motor control and perception. Brain Behav. Evol. 41 (1993) 39-50
79. Pencea V., Bingaman K.D., Freedman L.J., and Luskin M.B. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 172 (2001) 1-16
80. Portavella M., Torres B., and Salas C. Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J. Neurosci. 24 (2004) 2335-2342
81. Pouwels E. On the development of the cerebellum of the trout, Salmo gairdneri: I. Patterns of cell migration. Anat. Embryol. 152 (1978) 291-308
82. Pouwels E. On the development of the cerebellum of the trout, Salmo gairdneri: III. Development of neuronal elements. Anat. Embryol. 153 (1978) 37-54
83. Raff M.C. Social controls on cell survival and cell death. Nature 356 (1992) 397-400
84. Raff M.C., Barres B.A., Burne J.F., Coles H.S., Ishizaki Y., and Jacobson M.D. Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262 (1993) 695-700
85. Rajendran R.S., Zupanc M.M., Lösche A., Westra J., Chun J., and Zupanc G.K.H. Numerical chromosome variation and mitotic segregation defect in the adult brain of teleost fish. Dev. Neurobiol. 67 (2007) 1334-1347
86. Rakic P. Limits of neurogenesis in primates. Science 227 (1985) 1054-1056
87. Raymond P., Easter S., Burnham J., and Powers M. Postembryonic growth of the optic tectum in goldfish. II. Modulation of cell proliferation by retinal fiber input. J. Neurosci. 3 (1983) 1092-1099
88. Rehen S.K., McConnell M.J., Kaushal D., Kingsbury M.A., Yang A.H., and Chun J. Chromosomal variation in neurons of the developing and adult mammalian nervous system. Proc. Natl. Acad. Sci. USA 98 (2001) 13361-13366
89. Rehen S.K., Yung Y.C., McCreight M.P., Kaushal D., Yang A.H., Almeida B.S.V., Kingsbury M.A., Cabral K.M.S., McConnell M.J., Anliker B., et al. Constitutional aneuploidy in the normal human brain. J. Neurosci. 25 (2005) 2176-2180
90. Reier P.J., Stensaas L.J., and Guth L. The astrocytic scar as an impediment to regeneration in the central nervous system. In: Kao C.C., Bunge R.P., and Reier P.J. (Eds). Spinal Cord Reconstruction (1983), Raven Press, New York 163-195
91. 3H-Thymidin-Index vom Lebensalter in den Matrixzonen des Telencephalons von Lebistes reticulatus (Teleostei). Z. Mikrosk-anat Forsch. 81 (1970) 530-554
92. Richter W., and Kranz D. Die Abhängigkeit der DNS-Synthese in den Matrixzonen des Mesencephalons vom Lebensalter der Versuchstiere (Lebistes reticulatus - Teleostei): Autoradiographische Untersuchungen. Z. Mikrosk-anat Forsch. 82 (1970) 76-92
93. Rodríguez F., López J.C., Vargas J.P., Gómez Y., Broglio C., and Salas C. Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J. Neurosci. 22 (2002) 2894-2903
94. Rowe R.W.D., and Goldspink G. Muscle fibre growth in five different muscles in both sexes of mice. J. Anat. 104 (1969) 519-530
95. Rowlerson A., and Veggetti A. Cellular mechanisms of post-embryonic muscle growth in aquaculture species. In: Johnston I.A. (Ed). Muscle Development and Growth (2001), Academic Press, San Diego 103-140
96. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., García-Verdugo J.M., et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 (2004) 740-744
97. Schwenk F., Zevnik B., Brüning J., Röhl M., Willuweit A., Rode A., Hennek T., Kauselmann G., Jaenisch R., and Kühn R. Hybrid embryonic stem cell-derived tetraploid mice show apparently normal morphological, physiological, and neurological characteristics. Mol. Cell. Biol. 23 (2003) 3982-3989
98. Seri B., García-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
99. Song H.-j., Stevens C.F., and Gage F.H. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat. Neurosci. 5 (2002) 438-445
100. Soutschek J., and Zupanc G.K.H. Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Dev. Brain Res. 97 (1996) 279-286
101. Stewénius Y., Gorunova L., Jonson T., Larsson N., Höglund M., Mandahl N., Mertens F., Mitelman F., and Gisselsson D. Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc. Natl. Acad. Sci. USA 102 (2005) 5541-5546
102. Streit W.J., Walter S.A., and Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 57 (1999) 563-581
103. Stuermer C.A.O., Bastmeyer M., Bähr M., Strobel G., and Paschke K. Trying to understand axonal regeneration in the CNS of fish. J. Neurobiol. 23 (1992) 537-550
104. Surh C.D., and Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372 (1994) 100-103
105. Swisher D.A., and Wilson D.B. Cerebellar histogenesis in the lurcher (Lc) mutant mouse. J. Comp. Neurol. 173 (1977) 1038-1041
106. Tetzlaff W., Alexander S.W., Miller F.D., and Bisby M.A. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J Neurosci 11 (1991) 2528-2544
107. Vajda F.J. Neuroprotection and neurodegenerative disease. J. Clin. Neurosci. 9 (2002) 4-8
108. van Groen T., Kadish I., and Wyss J.M. Species differences in the projections from the entorhinal cortex to the hippocampus. Brain Res. Bull. 57 (2002) 553-556
109. van Groen T., Miettinen P., and Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 13 (2003) 133-149
110. Vargas J.P., Rodríguez F., López J.C., Arias J.L., and Salas C. Spatial learning-induced increase in the argyophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish. Brain Res. 865 (2000) 77-84
111. Voigt T. Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289 (1989) 74-88
112. Waxman S.G., and Anderson M.J. Regeneration of central nervous structures: Apteronotus spinal cord as a model system. In: Bullock T.H., and Heiligenberg W. (Eds). Electroreception (1986), John Wiley & Sons, New York 183-208
113. Weatherley A.H., and Gill H.S. Dynamics of increase in muscle fibres in fishes in relation to size and growth. Experientia 41 (1985) 353-354
114. Wetts R., and Herrup K. Direct correlation between Purkinje and granule cell number in the cerebella of lurcher chimeras and wild-type mice. Brain Res. 312 (1983) 41-47
115. Williams R.W. Mapping genes that modulate brain development: a quantitative genetic approach. In: Goffinet A.F., and Rakic P. (Eds). Mouse Brain Development (2000), Springer-Verlag, New York 21-49
116. Winner B., Cooper-Kuhn C.M., Aigner R., Winkler J., and Kuhn H.G. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci. 16 (2002) 1681-1689
117. Yang A.H., Kaushal D., Rehen S.K., Kriedt K., Kingsbury M.A., McConnell M.J., and Chun J. Chromosome segregation defects contribute to aneuploidy in normal neural progenitor cells. J. Neurosci. 23 (2003) 10454-10462
118. Yurov Y.B., Iourov I.Y., Monakhov V.V., Soloviev I.V., Vostrikov V.M., and Vorsanova S.G. The variation of aneuploidy frequency in the developing and adult human brain revealed by an interphase FISH study. J. Histochem. Cytochem. 53 (2005) 385-390
119. Zakon H.H. Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age. J. Comp. Neurol. 228 (1984) 557-570
120. Zhang Z., Krebs C.J., and Guth L. Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143 (1997) 141-152
121. Zikopoulos B., Kentouri M., and Dermon C.R. Proliferation zones in the adult brain of a sequential hermaphrodite teleost species (Sparus aurata). Brain Behav. Evol. 56 (2000) 310-322
122. Zimmerman A.M., and Lowery M.S. Hyperplastic development and hypertrophic growth of muscle fibers in the white seabass (Atractoscion nobilis). J. Exp. Zool. 284 (1999) 299-308
123. Zupanc G.K.H. Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J. Exp. Biol. 202 (1999) 1435-1446
124. Zupanc G.K.H. Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav. Evol. 58 (2001) 250-275
125. Zupanc G.K.H. Neurogenesis and neuronal regeneration in the adult fish brain. J. Comp. Physiol. A 192 (2006) 649-670
126. Zupanc G.K.H. Adult neurogenesis and neuronal regeneration in the teleost fish brain: implications for the evolution of a primitive vertebrate trait. In: Bullock T.H., and Rubenstein L.R. (Eds). The Evolution of Nervous Systems in Non-Mammalian Vertebrates (2006), Academic Press, Oxford 485-520
127. Zupanc G.K.H. Proteomics of traumatic brain injury and regeneration. Proteomics Clin. Appl. 1 (2007) 1362-1372
128. Zupanc G.K.H. Adult neurogenesis in teleost fish. In: Gage F.H., Kempermann G., and Song H. (Eds). Adult Neurogenesis (2008), Cold Spring Harbor Laboratory Press, New York 571-592
129. Zupanc G.K.H., and Clint S.C. Potential role of radial glia in adult neurogenesis of teleost fish. Glia 43 (2003) 77-86
130. Zupanc G.K.H., and Horschke I. Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J. Comp. Neurol. 353 (1995) 213-233
131. Zupanc G.K.H., and Ott R. Cell proliferation after lesions in the cerebellum of adult teleost fish: time course, origin, and type of new cells produced. Exp. Neurol. 160 (1999) 78-87
132. Zupanc G.K.H., and Zupanc M.M. Birth and migration of neurons in the central posterior/prepacemaker nucleus during adulthood in weakly electric knifefish (Eigenmannia sp.). Proc. Natl. Acad. Sci. USA 89 (1992) 9539-9543
133. Zupanc G.K.H., and Zupanc M.M. New neurons for the injured brain: mechanisms of neuronal regeneration in adult teleost fish. Regenerative Med. 1 (2006) 207-216
134. 28k expression during regeneration in the adult fish cerebellum. Brain Res. 1095 (2006) 26-34
135. Zupanc G.K.H., Horschke I., Ott R., and Rascher G.B. Postembryonic development of the cerebellum in gymnotiform fish. J. Comp. Neurol. 370 (1996) 443-464
136. Zupanc G.K.H., Kompass K.S., Horschke I., Ott R., and Schwarz H. Apoptosis after injuries in the cerebellum of adult teleost fish. Exp. Neurol. 152 (1998) 221-230
137. Zupanc G.K.H., Clint S.C., Takimoto N., Hughes A.T.L., Wellbrock U.M., and Meissner D. Spatio-temporal distribution of microglia/macrophages during regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: a quantitative analysis. Brain Behav. Evol. 62 (2003) 31-42
138. Zupanc G.K.H., Hinsch K., and Gage F.H. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J. Comp. Neurol. 488 (2005) 290-319
139. Zupanc M.M., Wellbrock U.M., and Zupanc G.K.H. Proteome analysis identifies novel protein candidates involved in regeneration of the cerebellum of teleost fish. Proteomics 6 (2006) 677-696