Sex differences in adult cell proliferation within the zebrafish (Danio rerio) cerebellum

European Journal of Neuroscience

Volumn 25, Issue 4, 2007, Pages 1030-1040

  Ampatzis, Konstantinos ^a   Dermon, Catherine R ^a,b  

^a UNIVERSITY OF CRETE   (Greece)

^b UNIVERSITY OF PATRAS   (Greece)

Author keywords

Apoptosis; Chain migration like; Neurogenesis; Neuronal plasticity; Parvalbumin

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; FEMALE; GRANULE CELL; IMMUNOHISTOCHEMISTRY; MALE; MITOSIS; MOTOR PERFORMANCE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; SEX DIFFERENTIATION; SURVIVAL; TELEOST; ZEBRA FISH;

ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CEREBELLUM; FEMALE; IN SITU NICK-END LABELING; MALE; NERVE TISSUE PROTEINS; NEURONS; SEX CHARACTERISTICS; SEX FACTORS; TIME FACTORS; ZEBRAFISH;

EID: 33847176278     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05366.x     Document Type: Article

References (114)

1. Abizaid, A., Mezei, G., Sotonyi, P. & Horvath, T.L. (2004) Sex differences in adult suprachiasmatic nucleus neurons emerging late prenatally in rats. Eur. J. Neurosci., 19, 2488-2496.
2. Abramoff, M.D. & Viergever, M.A. (2002) Computation and visualization of three-dimensional soft tissue motion in the orbit. IEEE T. Med. Imaging, 21, 296-304.
3. Alder, J., Cho, N.K. & Hatten, M.E. (1996) Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron, 17, 389-399.
4. Allen, G., Buxton, R.B., Wong, C. & Courchesne, E. (1997) Attentional activation of the cerebellum independent of motor involvement. Science, 275, 1940-1943.
5. Alonso, J.R., Arevalo, R., Brinon, G.J., Lara, J., Weruaga, E. & Aijon, J. (1992) Parvalbumin immunoreactive neurons and fibers in the teleost cerebellum. Anat. Embryol., 184, 355-361.
6. Altman, J. (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layers. J. Comp. Neurol., 145, 399-464.
7. Alvarez Otero, R., Sotelo, C. & Alvarado-Mallart, R.M. (1993) Chick?quail chimeras with partial cerebellar grafts: an analysis of the origin and migration of cerebellar cells. J. Comp. Neurol., 333, 597-615.
8. Alvarez-Buylla, A. (1990) Mechanism of neurogenesis in adult avian brain. Experientia, 46, 948-955.
9. Aronson, L.R. & Herberman, R. (1960) Persistence of a conditioned response in the cichlid fish, Tilapia macrocephala, after forebrain and cerebellar ablations. Anat. Rec., 138, 332.
10. Beyer, C. (1999) Estrogen and the developing mammalian brain. Anat. Embryol., 199, 379-390.
11. Bodega, G., Suarez, I., Rubio, M. & Fernandez, B. (1990) Distribution and characteristics of the different astroglial cell types in the adult lizard (Lacerta lepida) spinal cord. Anat. Embryol., 181, 567-575.
12. Bodega, G., Suarez, I., Rubio, M. & Fernandez, B. (1994) Ependyma: phylogenetic evolution of glial fibrillary acidic protein (GFAP) and vimentin expression in vertebrate spinal cord. Histochemistry, 102, 113-122.
13. Bodega, G., Suarez, I., Rubio, M., Villaba, R.M. & Fernandez, B. (1993) Astroglial pattern in the spinal cord of the adult barbel (Barbus comiza). Anat. Embryol., 187, 385-395.
14. Bu, J., Sathyendra, V., Nagykery, N. & Geula, C. (2003) Age-related changes in calbindin-D28k, calretinin, and parvalbumin immunoreactive neurons in the human cerebral cortex. Exp. Neurol., 182, 220-231.
15. Byrd, C.A. & Brunjes, P.C. (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience, 105, 793-801.
16. Callard, G.V., Schlinger, B.A. & Pasmanik, M. (1990) Nonmammalian vertebrate models in studies of brain-steroid interactions. J. Exp. Zool. Suppl., 4, 6-16.
17. Candal, E., Anadon, R., DeGrip, W.J. & Rodriguez-Moldes, I. (2005) Patterns of cell proliferation and cell death in the developing retina and optic tectum of the brown trout. Dev. Brain Res., 154, 101-119.
18. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375-475.
19. Celio, M.R., Baier, W., de Viragh, P., Scharer, L. & Gerday, C. (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium, 9, 81-86.
20. Clemente, D., Porteros, A., Weruaga, E., Alonso, J.R., Arenzana, F.J., Aijon, J. & Arevalo, R. (2004) Cholinergic elements in the zebrafish central nervous system: Histochemical and immunohistochemical analysis. J. Comp. Neurol., 474, 75-107.
21. Clint, S.C. & Zupanc, G.K.H. (2001) Neuronal regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: guidance of migrating young cells by radial glia. Dev. Brain Res., 130, 15-23.
22. Contestabile, A., Villani, L. & Ciani, F. (1977) Ultrastructural analysis on acetylcholinesterase localization in the cerebellar cortex of teleosts. Anat. Embryol., 152, 15-27.
23. Crespo, C., Porteros, A., Arevalo, R., Brinon, J.G., Aijon, J. & Alonso, J.R. (1999) Distribution of parvalbumin immunoreactivity in the brain of tench (Tinca tinca L., 1758). J. Comp. Neurol., 413, 549-571.
24. Dawley, E.M., Fingerlin, A., Hwang, D., John, S.S. & Stankiewicz, C.A. (2000) Seasonal cell proliferation in the chemosensory epithelium and brain of red-backed salamanders, Plethodon cinereus. Brain Behav. Evol., 56, 1-13.
25. De Zeeuw, C.I., Wylie, D.R., Digiorgi, P.L. & Simpson, J.I. (1994) Morphological evidence for interzonal inhibition by Golgi cells in the rabbit vestibulocerebellum. Soc. Neurosci. Abstr., 20, 1745-1745.
26. Ekström, P., Johnsson, C.M. & Ohlin, L.M. (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, 92-110.
27. Eng, L.F., Ghirnikar, R.S. & Lee, Y.L. (2000) Glial fibrillary acidic protein: GFAP-thirty one years (1969-2000). Neurochem. Res., 25, 1439-1451.
28. Falconer, E.M. & Galea, L.A.M. (2003) Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res., 975, 22-36.
29. Fine, M.L., Chen, F.A. & Keefer, D.A. (1996) Autoradiographic localization of dihydrotestosterone and testosterone concentrating neurons in the brain of the oyster toadfish. Brain Res., 709, 65-80.
30. Forlano, P.M., Deitcher, D.L., Myers, D.A. & Bass, A.H. (2001) Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J. Neurosci., 21, 8943-8955.
31. Galea, L.A.M. & McEwen, B.S. (1999) Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience, 89, 955-964.
32. Galea, L.A., Spritzer, M.D., Barker, J.M. & Pawluski, J.L. (2006) Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus, 16, 225-232.
33. Gao, W.-Q. & Hatten, M.E. (1994) Immortalizing oncogenes subvert the establishment of granule cell identity in developing cerebellum. Development, 120, 1059-1070.
34. Gelinas, D. & Callard, G.V. (1997) Immunolocalization of aromatase- and androgen receptor-positive neurons in the goldfish brain. Gen. Comp. Endocrinol., 106, 155-168.
35. Gelinas, D., Pitoc, G.A. & Callard, G.V. (1998) Isolation of a goldfish brain cytochrome P450 aromatase cDNA: mRNA expression during the seasonal cycle and after steroid treatment. Mol. Cell. Endocrinol., 138, 81-93.
36. Ghelarducci, B. & Sebastiani, L. (1996) Contribution of the cerebellar vermis to cardiovascular control. J. Auton. Nerv. Syst., 56, 149-156.
37. Goldman, S.A. & Nottebohm, F. (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. USA, 80, 2390-2394.
38. Gould, E., Reeves, A.J., Fallah, M., Tanapat, P., Gross, C.G. & Fuchs, E. (1999) Hippocampal neurogenesis in adult Old World primates. Proc. Natl. Acad. Sci. USA, 96, 5263-5267.
39. Gould, E., Vail, N., Wagers, M. & Gross, C.G. (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc. Natl. Acad. Sci. USA, 98, 0910-10917.
40. 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, 263-277.
41. Hallonet, M.E.R., Teillet, M.-A. & Le Douarin, N.M. (1990) A new approach to the development of the cerebellum provided by the quail-chick marker system. Development, 108, 19-31.
42. Han, V.Z., Meek, J., Campbell, H.R. & Bell, C.C. (2006) Cell morphology and circuitry in the central lobes of the mormyrid cerebellum. J. Comp. Neurol., 497, 309-325.
43. Hayes, N.L. & Nowakowski, R.S. (2002) Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res. Dev. Brain Res., 134, 77-85.
44. Herrup, K. & Kuemerle, B. (1997) The compartmentalization of the cerebellum. Annu. Rev. Neurosci., 20, 61-90.
45. Hidalgo, A., Barami, K., Iversen, K. & Goldman, S.A. (1995) Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J. Neurobiol., 27, 470-487.
46. Ito, H. (1978) A catalogue of histological preparations of the teleost brains. Med. J. Osaka University, 28, 219-228.
47. Ito, M. (2000) Internal model visualized. Nature, 403, 153-154.
48. Ito, M., Sakurai, M. & Tongroach, P. (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. (Lond.), 324, 113-134.
49. Jankovski, A., Rosi, F. & Sotelo, C. (1996) Neuronal precursors in the postnatal mouse cerebellum are fully committed cells: evidence from heterochronic transplantations. Eur. J. Neurosci., 8, 2308-2319.
50. King, C., Lacey, R., Rodger, J., Bartlett, C., Dunlop, S. & Beazlea, L. (2004) Characterisation of tectal ephrin-A2 expression during optic nerve regeneration in goldfish: implications for restoration of topography. Exp. Neurol., 187, 380-387.
51. Kirn, J.R. & DeVoogd, T.J. (1989) sexual differentiation in the zebra finch. J. Neurosci., 9, 3176-3187.
52. Kirn, J.R. & Schwabl, H. (1997) Photoperiod regulation of neuron death in the adult canary. J. Neurobiol., 33, 223-231.
53. Kotchabhakdi, N. (1976) Functional circuitry of the goldfish cerebellum. J. Comp. Physiol., 112, 47-73.
54. Lalonde, R. & Botez, M.I. (1990) The cerebellum and learning processes in animals. Brain Res. Rev., 15, 325-332.
55. Leiner, H.C., Leiner, A.L. & Dow, R.S. (1993) Cognitive and language functions of the human cerebellum. Trends Neurosci., 16, 444-447.
56. Levine, E.M., Hitchcock, P.F., Glasgow, E. & Schechter, N. (1994) Restricted expression of a new paired-class homeobox gene in normal and regenerating adult goldfish retina. J. Comp. Neurol., 348, 596-606.
57. Levitt, P. & Rakic, P. (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J. Comp. Neurol., 193, 815-840.
58. Li, Z., Hu, M., Ochocinska, M.J., Joseph, N.M. & Easter, S.S. Jr (2000) Modulation of cell proliferation in the embryonic retina of zebrafish (Danio rerio). Dev. Dyn., 219, 391-401.
59. Lois, C., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. (1996) Chain migration of neuronal precursors. Science, 271, 978-981.
60. Lossi, L. & Merighi, A. (2003) In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Prog. Neurobiol., 69, 287-312.
61. Lossi, L., Mioletti, S. & Merighi, A. (2002) Synapse-independent and synapse-dependent apoptosis of cerebellar granule cells in postnatal rabbits occur at two subsequent but partly overlapping developmental stages. Neuroscience, 112, 509-523.
62. Marusich, M.F., Furneaux, H.M., Henion, P.D. & Weston, J.A. (1994) Hu neuronal proteins are expressed in proliferating neurogenic cells. J. Neurobiol., 25, 143-155.
63. Meek, J. & Nieuwenhuys, R. (1998) Holosteans and teleosts. In Nieuwenhuys, R., Ten Donkelaar, H.J. & Nicholson, C. (eds), The Central Nervous System of Vertebrates, Vol. 2. Springer-Verlag, Berlin, pp. 759-937.
64. Miller, M.W. & Nowakowski, R.S. (1988) Use of bromodeoxyuridine- immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res., 457, 44-52.
65. Miyamura, Y. & Nakayasu, H. (2001) Zonal distribution of Purkinje cells in the zebrafish cerebellum: analysis by means of a specific monoclonal antibody. Cell Tissue Res., 30, 299-305.
66. Mueller, T. & Wullimann, M.F. (2002) BrdU-, neuroD (nrd)- and Hu-studies reveal unusual non-ventricular neurogenesis in the postembryonic zebrafish forebrain. Mech. Devel., 117, 123-135.
67. Mullen, R.J., Buck, C.R. & Smith, A.M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116, 201-211.
68. Nikolakopoulou, A.M., Parpas, A., Panagis, L., Zikopoulos, B. & Dermon, C.R. (2006) Early post-hatching sex differences in cell proliferation and survival in the quail telencephalic ventricular zone and intermediate medial mesopallium. Brain Res. Bull., 70, 107-116.
69. Nordeen, E.J. & Nordeen, K.W. (1989) Estrogen stimulates the incorporation of new neurons into avian song nuclei during adolescence. Brain Res. Dev. Brain Res., 49, 27-32.
70. Nordeen, K.W., Nordeen, E.J. & Arnold, A.P. (1987) Estrogen accumulation in zebra finch song control nuclei: implications for sexual differentiation and adult activation of song behavior. J. Neurobiol., 18, 569-582.
71. Nowakowski, R.S., Caviness, V.S. Jr, Takahashi, T. & Hayes, N.L. (2002) Related population dynamics during cell proliferation and neuronogenesis in the developing murine neocortex. Results Probl. Cell Differ., 39, 1-25.
72. Oppenheim, R.W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci., 14, 453-501.
73. Paul, D.H. & Roberts, B.L. (1979) The significance of cerebellar function for a reflex movement of the dogfish. J. Comp. Physiol., 134, 69-74.
74. Peretto, P., Giachino, C., Panzica, G. & Fasolo, A. (2001) Sexually dimorphic neurogenesis is topographically matched with the anterior accessory olfactory bulb of the adult rat. Cell Tissue Res., 306, 385-389.
75. Porteros, A., Arevalo, R., Brinon, G.J., Crespo, C., Aijon, J. & Alonso, R.J. (1998) Parvalbumin immunoreactivity during the development of the cerebellum of rainbow trout. Dev. Brain Res., 109, 221-227.
76. Rakic, P. (1973) Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J. Comp. Neurol., 47, 523-546.
77. Rasband, W.S. (2004) ImageJ. National institutes of Health, Bethesda, MD, USA.
78. Rasika, S., Nottebohm, F. & Alvarez-Buylla, A. (1994) Testosterone increases the recruitment and?or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. USA, 91, 7854-7858.
79. Raymond, P.A. & Easter, S.S. Jr (1983) Postembryonic growth of the optic tectum in goldfish. I. Location of germinal cells and numbers of neurons produced. J. Neurosci., 3, 1077-1091.
80. Roberts, B.L., van Rossem, A. & De Jager, S. (1992) The influence of cerebellar lesions on the swimming performance of the trout. J. Exp. Biol., 167, 171-178.
81. Rodriguez, F., Duran, E., Gomez, A., Ocana, F.M., Alvarez, E., Jimenez-Moya, F., Broglio, C. & Salas, C. (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Res. Bull., 66, 365-370.
82. Sawyer, S.J., Gerstner, K.A. & Callard, G.V. (2006) Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: Gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen. Comp. Endoc., 147, 108-117.
83. Somogyi, P., Eshhar, N., Teichberg, V.I. & Roberts, J.D. (1990) Subcellular localization of a putative kainate reseptor in Bergmann glial cells using a monoclonal antibody in the chick and fish cerebellar cortex. Neuroscience, 35, 9-30.
84. Soutschek, J. & Zupanc, G.K.H. (1996) Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Dev. Brain Res., 97, 279-286.
85. Stamatakis, A., Barbas, H. & Dermon, C.R. (2004) Late granule cell genesis in quail cerebellum. J. Comp. Neurol., 474, 173-189.
86. Stokes, E.A., Lonergan, W., Weber, L.P., Janz, D.M., Poznanski, A.A., Balch, G.C., Metcalfe, C.D. & Grober, M.S. (2004) Decreased apoptosis in the forebrain of adult male medaka (Oryzias latipes) after aqueous exposure to ethinylestradiol. Comp. Biochem. Physiol. C., 138, 163-167.
87. Stuermer, C.A. (1988) Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J. Neurosci., 8, 4513-4530.
88. Supple, W.F. Jr & Kapp, B.S. (1993) The anterior cerebellar vermis: essential involvement in classically conditioned bradycardia in the rabbit. J. Neurosci., 13, 3705-3711.
89. Tanapat, P., Hastings, N.B., Reeves, A.J. & Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 19, 5792-5801.
90. Thomaidou. D., Mione, M.C., Cavanagh, J.F. & Parnavelas, J.G. (1997) Apoptosis and its relation to the cell cycle in the developing cerebral cortex. Neuroscience, 17, 1075-1085.
91. Thompson, R.F., Bao, S., Chen, L., Cipriano, B.J., Grethe, J.S., Kim, J.J., Thompson, J.K., Tracy, J.A., Weninger, M.S. & Krupa, D.J. (1997) Associative learning. In Schmahmann, J.D. (ed.), The Cerebellum and Cognition. Academic Press, San Diego, CA, pp. 152-189.
92. Tomizawa, K., Inoue, Y. & Nakayasu, H.A. (2000) Monoclonal antibody stains radial glia in the adult zebrafish (Danio rerio) CNS. J. Neurocytol., 29, 119-128.
93. Tsukahara, S., Inami, K., Maekawa, F., Kakeyama, M., Yokoyama, T., Yuji, M., Kitagawa, H., Kannan, Y. & Yamanouchi, K. (2004) Postnatal apoptosis, development, and sex difference in the lateral septum of rats. J. Comp. Neurol., 475, 177-187.
94. Vankirk, A.M. & Byrd, C.A. (2003) Apoptosis following peripheral sensory deafferentation in the olfactory bulb of adult zebrafish. J. Comp. Neurol., 455, 488-498.
95. Westerfield, M. (1995) The Zebrafish Book. University of Oregon Press, Eugene, OR.
96. Wild, J.M., Williams, N.M., Howie, J.G. & Mooney, R. (2005) Calcium-binding proteins define interneurons in HVC of the Zebra Finch (Taeniopygia guttata). J. Comp. Neurol., 483, 76-90.
97. Wise, P.M., Dubal, D.B., Wilson, M.E., Rau, S.W. & Liu, Y. (2001) Estrogens: trophic and protective factors in the adult brain. Front. Neuroendocrinol., 22, 33-66.
98. Wullimann, M.F., Rupp, B. & Reichert, H. (1996) Neuroanatomy of the Zebrafish Brain: a Topological Atlas. Birkhaeuser Verlag, Basel.
99. Wullimann, M.F. & Knipp, S. (2000) Proliferation pattern changes in the zebrafish brain from embryonic through early postembryonic stages. Anat. Embryol., 202, 385-400.
100. Wyllie, A.H. (1997) Apoptosis: an overview. Br. Med. Bull., 53, 451-465.
101. Yamashita, M. (2003) Apoptosis in zebrafish development. Comp. Biochem. Physiol. B, 136, 731-742.
102. Yoon, M.G. (1975) Effects of post-operative visual environments on reorganization of retinotectal projection in goldfish. J. Physiol. (Lond.), 246, 673-694.
103. Yoshida, M., Okamura, I. & Uematsu, K. (2004) Involvement of the cerebellum in classical fear conditioning in goldfish. Behav. Brain Res., 153, 143-148.
104. Zhang, L. & Goldman, J.E. (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron, 16, 47-54.
105. Zikopoulos, B., Kentouri, M. & Dermon, C.R. (2000) Proliferation zones in the adult brain of sequential hermaphrodite teleost species (Sparus aurata). Brain Behav. Evol., 56, 310-322.
106. Zikopoulos, B., Kentouri, M. & Dermon, C.R. (2001) Cell genesis in the hypothalamus is associated to the sexual phase of a hermaphrodite teleost. Neuroreport, 12, 2477-2481.
107. Zupanc, G.K. (1999) Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J. Exp. Biol., 202, 1435-1446.
108. Zupanc, G.K.H. (2001) Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav. Evol., 58, 250-275.
109. Zupanc, G.K.H. & Clint, S.C. (2003) Potential role of radial glia in adult neurogenesis of teleost fish. Glia, 43, 77-86.
110. Zupanc, G.K.H., Hinsch, K. & Gagr, F.H. (2005) Proliferation, migration, neuronal differentiation and long-term survival of new cells in the adult zebrafish brain. J. Comp. Neurol., 488, 290-319.
111. Zupanc, G.K.H. & Horschke, I. (1995) Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J. Comp. Neurol., 353, 213-233.
112. Zupanc, G.K.H., Horschke, I., Ott, R. & Rascher, G.B. (1996) Postembryonic development of the cerebellum in gymnotiform fish. J. Comp. Neurol., 370, 443-464.
113. Zupanc, G.K.H., Kompass, K.S., Horschke, I., Ott, R. & Schwarz, H. (1998) Apoptosis after injuries in the cerebellum of adult teleost fish. Exp. Neurol., 152, 221-230.
114. Zupanc, G.K.H. & Ott, R. (1999) Cell proliferation after lesions in the cerebellum of adult teleost fish: time course, origin, and type of new cells produced. Exp. Neurol., 160, 78-87.