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Neurogenesis and neuronal regeneration in the adult fish brain

  • G. K. H. Zupanc
Review

Abstract

Fish are distinctive in their enormous potential to continuously produce new neurons in the adult brain, whereas in mammals adult neurogenesis is restricted to the olfactory bulb and the hippocampus. In fish new neurons are not only generated in structures homologous to those two regions, but also in dozens of other brain areas. In some regions of the fish brain, such as the optic tectum, the new cells remain near the proliferation zones in the course of their further development. In others, as in most subdivisions of the cerebellum, they migrate, often guided by radial glial fibers, to specific target areas. Approximately 50% of the young cells undergo apoptotic cell death, whereas the others survive for the rest of the fish’s life. A large number of the surviving cells differentiate into neurons. Two key factors enabling highly efficient brain repair in fish after injuries involve the elimination of damaged cells by apoptosis (instead of necrosis, the dominant type of cell death in mammals) and the replacement of cells lost to injury by newly generated ones. Proteome analysis has suggested well over 100 proteins, including two dozen identified ones, to be involved in the individual steps of this phenomenon of neuronal regeneration.

Keywords

Adult neurogenesis Neuronal regeneration Proteomics Apteronotus leptorhynchus Zebrafish 

Abbreviations

BrdU

5-Bromo-2′-deoxyuridine

CP/PPn

Central posterior/prepacemaker nucleus

EOD

Electric organ discharge

GFAP

Glial fibrillary acidic protein

TUNEL

Terminal deoxynucleotidyl-transferase-mediated dUTP-biotin nick end-labeling

Notes

Acknowledgments

I thank Robert C. Beason, Theodore H. Bullock, Cecilia Ubilla, and Marianne M. Zupanc for their most helpful comments on the manuscript. Part of this review was written while the author was a Visiting Scholar in the laboratory of Ted Bullock at the Department of Neurosciences of the University of California at San Diego. Financial support was provided by funds from the Wellcome Trust and the International University Bremen.

References

  1. Alonso JR, Lara J, Vecino E, Coveñas R, Aijón J (1989) Cell proliferation in the olfactory bulb of adult freshwater teleosts. J Anat 163:155–163PubMedGoogle Scholar
  2. Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135:1127–1128PubMedGoogle Scholar
  3. Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145:573–591PubMedGoogle Scholar
  4. Altman J (1969a) Autoradiographic and histological studies of postnatal neurogenesis: III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136:269–294Google Scholar
  5. 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 137:433–458Google Scholar
  6. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–336PubMedGoogle Scholar
  7. Barnea A, Nottebohm F (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217–11221PubMedGoogle Scholar
  8. Bass AH (1982) Evolution of the vestibulolateral lobe of the cerebellum in electroreceptive and nonelectroreceptive teleosts. J Morphol 174:335–348Google Scholar
  9. Bastian J (1999) Plasticity of feedback inputs in the apteronotid electrosensory system. J Exp Biol 202:1327–1337PubMedGoogle Scholar
  10. Bayer SA, Yackel JW, Puri PS (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890–892PubMedGoogle Scholar
  11. Beattie MS, Farooqui AA, Bresnahan JC (2000) Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 17:915–925PubMedGoogle Scholar
  12. Bell C, Bodznick D, Montgomery J, Bastian J (1997) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50(Suppl 1):17–31PubMedGoogle Scholar
  13. 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 228:461–470PubMedGoogle Scholar
  14. Bernstein JJ (1968) Regeneration of a peripheral nerve implant into goldfish telencephalic parenchyma. Nature 217:183–184Google Scholar
  15. Botsch D (1960) Dressur-und Transpositionsversuche bei Karauschen (Carassius, Teleostei) nach partieller Exstirpation des Tectum opticum. Z Vergl Physiol 43:173–230Google Scholar
  16. Bufalari A, Sidoni A, Ferri M, Lolli G, Alberti P (1996) Effect of octreotide on pancreatic regeneration in rats measured by bromodeoxyuridine uptake. Eur J Surg 162:223–228PubMedGoogle Scholar
  17. Bullock TH (1969) Species differences in effect of electroreceptor input on electric organ pacemakers and other aspects of behavior in electric fish. Brain Behav Evol 2:85–118Google Scholar
  18. Burd GD, Nottebohm F (1985) Ultrastructural characterization of synaptic terminals formed on newly generated neurons in a song control nucleus of the adult canary forebrain. J Comp Neurol 240:143–152PubMedGoogle Scholar
  19. Byrd CA, Brunjes PC (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105:793–801PubMedGoogle Scholar
  20. Caddy KWT, Biscoe TJ (1976) The number of Purkinje cells and olive neurones in the normal and lurcher mutant mouse. Brain Res 111:396–398PubMedGoogle Scholar
  21. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417PubMedGoogle Scholar
  22. Chetverukhin VK, Polenov AL (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus in the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus: I. Ventricular zone cell proliferation. Cell Tiss Res 271:341–350Google Scholar
  23. Clint SC, Zupanc GKH (2001) Neuronal regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: guidance of migrating young cells by radial glia. Dev Brain Res 130:15–23Google Scholar
  24. Clint SC, Zupanc GKH (2002) Up-regulation of vimentin expression during regeneration in the adult fish brain. NeuroReport 13:317–320PubMedGoogle Scholar
  25. Corotto FS, Henegar JA, Maruniak JA (1993) Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci Lett 149:111–114PubMedGoogle Scholar
  26. Corwin JT (1981) Postembryonic production and aging of inner ear hair cells in sharks. J Comp Neurol 201:541–553PubMedGoogle Scholar
  27. Doetsch F, Scharff C (2001) Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav Evol 58:306–322PubMedGoogle Scholar
  28. Dulka JG, Maler L (1994) Testosterone modulates female chirping behavior in the weakly electric fish, Apteronotus leptorhynchus. J Comp Physiol A 174:331–343Google Scholar
  29. Dunlap KD, Thomas P, Zakon HH (1998) Diversity of sexual dimorphism in electrocommunication signals and its androgen regulation in a genus of electric fish, Apteronotus. J Comp Physiol A 183:77–86PubMedGoogle Scholar
  30. 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 436:92–110PubMedGoogle Scholar
  31. Engler G, Zupanc GKH (2001) Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, Apteronotus leptorhynchus. J Comp Physiol A 187:747–756PubMedGoogle Scholar
  32. Engler G, Fogarty CM, Banks JR, Zupanc GKH (2000) Spontaneous modulations of the electric organ discharge in the weakly electric fish, Apteronotus leptorhynchus: a biophysical and behavioral analysis. J Comp Physiol A 186:645–660PubMedGoogle Scholar
  33. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317PubMedGoogle Scholar
  34. Font E, Desfilis E, Pérez-Cañellas MM, García-Verdugo JM (2001) Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav Evol 58:276–295PubMedGoogle Scholar
  35. Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22:612–613PubMedGoogle Scholar
  36. García-Verdugo JM, Llahi S, Ferrer I, López-García C (1989) Postnatal neurogenesis in the olfactory bulb of a lizard: a tritiated thymidine autoradiographic study. Neurosci Lett 98:247–252PubMedGoogle Scholar
  37. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501PubMedGoogle Scholar
  38. Gerhard GS, Kauffman EJ, Wang X, Stewart R, Moore JL, Kasales CJ, Demidenko E, Cheng KC (2002) Life spans and senescent phenotypes in two strains of zebrafish (Danio rerio). Exp Gerontol 37:1055–1068PubMedGoogle Scholar
  39. Gheteu A, Zupanc GKH (2001) Radial glia in the cerebellum of adult teleost fish: implications for guidance of migrating new neurons. 31st Annual Meeting of the Society for Neuroscience, San Diego, Society for Neuroscience, Washington, DC, Abstract 692.1Google Scholar
  40. Gheteu A, Zupanc GKH (2002) Radial glia in the central posterior/prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus: effect of sexual maturity. 32nd Annual Meeting of the Society for Neuroscience, Orlando, Society for Neuroscience. Washington, DC, Abstract 527.5Google Scholar
  41. Goldman-Rakic PS (1980) Morphological consequences of prenatal injury to the primate brain. Prog Brain Res 53:3–19Google Scholar
  42. 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 USA 80:2390–2394PubMedGoogle Scholar
  43. Gould E, McEwen BS, Tanapat P, Galea LAM, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492–2498PubMedGoogle Scholar
  44. Gould E, Tanapat P, McEwen BS, Flügge G, Fuchs E (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168–3171PubMedGoogle Scholar
  45. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E (1999) Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96:5263–5267PubMedGoogle Scholar
  46. Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475PubMedGoogle Scholar
  47. Gratzner HG, Leif RC, Ingram DJ, Castro A (1975) The use of antibody specific for bromodeoxyuridine for the immunofluorescent determination of DNA replication in single cells and chromosomes. Exp Cell Res 95:88–94PubMedGoogle Scholar
  48. Graziadei PP, Graziadei GA (1979) 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 8:1–18PubMedGoogle Scholar
  49. Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33:254–265Google Scholar
  50. Heiligenberg W, Finger T, Matsubara J, Carr C (1981) Input to the medullary pacemaker nucleus in the weakly electric fish, Eigenmannia (Sternopygidae, Gymnotiformes). Brain Res 211:418–423PubMedGoogle Scholar
  51. Herculano-Houzel S, Lent R (2005) Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J Neurosci 25:2518–2521PubMedGoogle Scholar
  52. Hopkins CD (1974) Electric communication: functions in the social behavior of Eigenmannia virescens. Behaviour 50:270–305Google Scholar
  53. Johns PR (1977) Growth of the adult goldfish eye. III. Source of the new retinal cells. J Comp Neurol 176:343–358PubMedGoogle Scholar
  54. Johns PR, Easter SSJ (1977) Growth of the adult goldfish eye: II. Increase in retinal cell number. J Comp Neurol 176:331–342PubMedGoogle Scholar
  55. Kaplan MS (1981) Neurogenesis in the 3-month-old rat visual cortex. J Comp Neurol 195:323–338PubMedGoogle Scholar
  56. Kaplan MS, Bell DH (1983) Neuronal proliferation in the 9-month-old rodent—radioautographic study of granule cells in the hippocampus. Exp Brain Res 52:1–5PubMedGoogle Scholar
  57. Kaplan MS, Bell DH (1984) Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4:1429–1441PubMedGoogle Scholar
  58. Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092–1094PubMedGoogle Scholar
  59. Kawasaki M, Maler L, Rose GJ, Heiligenberg W (1988) Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neurol 276:113–131PubMedGoogle Scholar
  60. 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 130:391–399PubMedGoogle Scholar
  61. Kerr JFR, Searle J, Harmon BV, Bishop CJ (1987) Apoptosis. In: Potten CS (eds) Perspectives on mammalian cell death. Oxford University Press, Oxford, pp 93–128Google Scholar
  62. Kerr JFR, Gobé GC, Winterford CM, Harmon BV (1995) Anatomical methods in cell death. In: Schwartz LM, Osborne BA (eds) Cell death. Academic, San Diego, pp 1–27Google Scholar
  63. Kirschbaum F (1979) Reproduction of the weakly electric fish Eigenmannia virescens (Rhamphichtyidae, Teleostei) in captivity: I. Control of gonadal recrudescence and regression by environmental factors. Behav Ecol Sociobiol 4:331–355Google Scholar
  64. Kirsche W (1950) Die regenerativen Vorgänge am Rückenmark erwachsener Teleostier nach operativer Kontinuitätstrennung. Z mikrosk.-anat Forsch 56:190–265Google Scholar
  65. Kirsche W, Kirsche K (1961) Experimentelle Untersuchungen zur Frage der Regeneration und Funktion des Tectum opticum von Carassius carassius L. Z mikrosk.-anat Forsch 67:140–182PubMedGoogle Scholar
  66. Kokudo N, Kothary PC, Eckhauser FE, Nakamura T, Raper SE (1992) Inhibition of DNA synthesis by somatostatin in rat hepatocytes stimulated by hepatocyte growth factor or epidermal growth factor. Am J Surg 163:169–173PubMedGoogle Scholar
  67. Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768–5773PubMedGoogle Scholar
  68. Koumans JTM, Akster HA (1995) Myogenic cells in development and growth of fish. Comp Biochem Physiol 110A:3–20Google Scholar
  69. Kranz D, Richter W (1970) Autoradiographische Untersuchungen zur DNS-Synthese im Cerebellum und in der Medulla oblongata von Teleostiern verschiedenen Lebensalters. Z mikrosk.-anat Forsch 82:264–292PubMedGoogle Scholar
  70. Larimer JL, MacDonald JA (1968) Sensory feedback from electroreceptors to electromotor pacemaker centers in gymnotids. Am J Physiol 214:1253–1261PubMedGoogle Scholar
  71. Lois C, Alvarez-Buylla A (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90:2074–2077PubMedGoogle Scholar
  72. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148PubMedGoogle Scholar
  73. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981PubMedGoogle Scholar
  74. López-García C, Molowny A, García-Verdugo JM, Ferrer I (1988) Delayed postnatal neurogenesis in the cerebral cortex of lizards. Dev Brain Res 471:167–174Google Scholar
  75. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons from the forebrain subventricular zone. Neuron 11:173–189PubMedGoogle Scholar
  76. Maler L, Sas E, Johnston S, Ellis W (1991) An atlas of the brain of the electric fish Apteronotus leptorhynchus. J Chem Neuroanat 4:1–38PubMedGoogle Scholar
  77. Marcus RC, Delaney CL, Easter SS (1999) Neurogenesis in the visual system of embryonic and adult zebrafish (Danio rerio). Vis Neurosci 16:417–424PubMedGoogle Scholar
  78. Mareš V, Lodin Z (1974) An autoradiographic study of DNA synthesis in adolescent and adult mouse forebrain. Brain Res 76:557–561PubMedGoogle Scholar
  79. Mascardo RN, Sherline P (1982) Somatostatin inhibits rapid centrosomal separation and cell proliferation induced by epidermal growth factor. Endocrinology 111:1394–1396PubMedGoogle Scholar
  80. Metzner W (1999) Neural circuitry for communication and jamming avoidance in gymnotiform electric fish. J Exp Biol 202:1365–1375PubMedGoogle Scholar
  81. Meyer RL (1978) Evidence from thymidine labelling for continuing growth of retina and tectum in juvenile goldfish. Exp Neurol 59:99–111PubMedGoogle Scholar
  82. Meyer RL, Sakurai K, Schauwecker E (1985) 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 239:27–43PubMedGoogle Scholar
  83. Modak SP, Bollum FJ (1972) Detection and measurement of single-strand breaks in nuclear DNA in fixed lens sections. Exp Cell Res 75:307–313PubMedGoogle Scholar
  84. Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202:1195–1203PubMedGoogle Scholar
  85. Nottebohm F (2002) Neuronal replacement in adult brain. Brain Res Bull 57:737–749PubMedGoogle Scholar
  86. Ott R, Zupanc GKH, Horschke I (1997) Long-term survival of postembryonically born cells in the cerebellum of gymnotiform fish, Apteronotus leptorhynchus. Neurosci Lett 221:185–188PubMedGoogle Scholar
  87. Paton JA, Nottebohm FN (1984) Neurons generated in the adult brain are recruited into functional circuits. Science 225:1046–1048PubMedGoogle Scholar
  88. Paton JA, O’Loughlin BE, Nottebohm F (1985) Cells born in adult canary forebrain are local interneurons. J Neurosci 5:3088–3093PubMedGoogle Scholar
  89. Paulin MG (1993) The role of the cerebellum in motor control and perception. Brain Behav Evol 41:39–50PubMedGoogle Scholar
  90. Pencea V, Bingaman KD, Freedman LJ, Luskin MB (2001) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1–16PubMedGoogle Scholar
  91. Pflugfelder O (1965) Reparative und regenerative Prozesse nach partieller Zerstörung von Fischgehirnen. Zool Jb Physiol 71:301–314Google Scholar
  92. 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 271:351–362PubMedGoogle Scholar
  93. Polenov AL, Pavlovic M (1978) The hypothalamo–hypophysial system in Acipenseridae. VII. The functional morphology of the peptidergic neurosecretory cells in the preoptic nucleus of the sturgeon, Acipenser güldenstädti Brandt: a quantitative study. Cell Tissue Res 186:559–570PubMedGoogle Scholar
  94. Pollak MN, Schally AV (1998) Mechanisms of antineoplastic action of somatostatin analogs. Proc Soc Exp Biol Med 217:143–152PubMedGoogle Scholar
  95. Pouwels E (1978a) On the development of the cerebellum of the trout, Salmo gairdneri: I. Patterns of cell migration. Anat Embryol 152:291–308Google Scholar
  96. Pouwels E (1978b) On the development of the cerebellum of the trout, Salmo gairdneri: III. Development of neuronal elements. Anat Embryol 153:37–54Google Scholar
  97. Pérez-Cañellas MM, García-Verdugo JM (1996) Adult neurogenesis in the telencephalon of a lizard: a [3H] thymidine autoradiographic and bromodeoxyuridine immunocytochemical study. Dev Brain Res 93:49–61Google Scholar
  98. Pérez-Sánchez F, Molowny A, García-Verdugo JM, López-García C (1989) Postnatal neurogenesis in the nucleus sphericus of the lizard, Podarcis hispanica. Neurosci Lett 106:71–75PubMedGoogle Scholar
  99. Raff MC (1992) Social controls on cell survival and cell death. Nature 356:397–400PubMedGoogle Scholar
  100. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262:695–700PubMedGoogle Scholar
  101. Rakic P (2002) Neurogenesis in adult primates. Prog Brain Res 138:3–14PubMedGoogle Scholar
  102. Raymond PA, Easter SS (1983) Postembryonic growth of the optic tectum in goldfish. I. Location of germinal cells and numbers of neurons produced. J Neurosci 3:1077–1091PubMedGoogle Scholar
  103. Raymond PA, Easter SS, Burnham JA, Powers MK (1983) Postembryonic growth of the optic tectum in goldfish. II. Modulation of cell proliferation by retinal fiber input. J Neurosci 3:1092–1099PubMedGoogle Scholar
  104. Reier PJ, Stensaas LJ, Guth L (1983) The astrocytic scar as an impediment to regeneration in the central nervous system. In: Kao CC, Bunge RP, Reier PJ (eds) Spinal cord reconstruction. Raven, New York, pp 163–195Google Scholar
  105. Ruben RJ (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Oto-Laryngol Suppl 220:1–44Google Scholar
  106. Sas E, Maler L (1987) The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anat Embryol 177:55–79PubMedGoogle Scholar
  107. Sas E, Maler L (1991) Somatostatin-like immunoreactivity in the brain of an electric fish (Apteronotus leptorhynchus) identified with monoclonal antibodies. J Chem Neuroanat 4:155–186PubMedGoogle Scholar
  108. Schwartz JP, Taniwaki T, Messing A, Brenner M (1996) Somatostatin as a trophic factor: analysis of transgenic mice overexpressing somatostatin in astrocytes. Ann NY Acad Sci 780:29–35PubMedGoogle Scholar
  109. Seri B, García-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160PubMedGoogle Scholar
  110. Siehler S, Zupanc GKH, Seuwen K, Hoyer D (1999) Characterisation of the fish sst3 receptor, a member of the SRIF1 receptor family: atypical pharmacological features. Neuropharmacology 38:449–462PubMedGoogle Scholar
  111. Siehler S, Nunn C, Zupanc GKH, Hoyer D (2005) Fish somatostatin sst3 receptor: comparison of radioligand and GTPγS binding, adenylate cyclase and phospholipase C activities reveals different agonist-dependent pharmacological signatures. Autonom Autacoid Pharmacol 25:1–16Google Scholar
  112. Song HJ, Stevens CF, Gage FH (2002) Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5:438–445PubMedGoogle Scholar
  113. Soutschek J, Zupanc GKH (1995) Apoptosis as a regulator of cell proliferation in the central posterior/prepacemaker nucleus of adult gymnotiform fish, Apteronotus leptorhynchus. Neurosci Lett 202:133–136PubMedGoogle Scholar
  114. Soutschek J, Zupanc GKH (1996) Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Dev Brain Res 97:279–286Google Scholar
  115. Srikant CB (1995) Cell cycle dependent induction of apoptosis by somatostatin analog SMS 201–995 in AtT-20 mouse pituitary cells. Biochem Biophys Res Commun 209:400–406PubMedGoogle Scholar
  116. Stroh T, Zupanc GKH (1993) Identification and localization of somatostatin-like immunoreactivity in the cerebellum of gymnotiform fish, Apteronotus leptorhynchus. Neurosci Lett 160:145–148PubMedGoogle Scholar
  117. Stroh T, Zupanc GKH (1995) Somatostatin in the prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus: evidence for a nonsynaptic function. Brain Res 674:1–14PubMedGoogle Scholar
  118. Stroh T, Zupanc GKH (1996) The postembryonic development of somatostatin immunoreactivity in the central posterior/prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus: a double-labelling study. Dev Brain Res 93:76–87Google Scholar
  119. Surh CD, Sprent J (1994) T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:100–103PubMedGoogle Scholar
  120. Swisher DA, Wilson DB (1977) Cerebellar histogenesis in the lurcher(Lc) mutant mouse. J Comp Neurol 173:1038–1041Google Scholar
  121. Szende B, Zalatnai A, Schally AV (1989) Programmed cell death (apoptosis) in pancreatic cancers of hamsters after treatment with analogs of both luteinizing hormone-releasing hormone and somatostatin. Proc Natl Acad Sci USA 86:1643–1647PubMedGoogle Scholar
  122. Taniwaki T, Schwartz JP (1995) Somatostatin enhances neurofilament expression and neurite outgrowth in cultured rat cerebellar granule cells. Dev Brain Res 88:109–116Google Scholar
  123. Taupin P, Gage FH (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69:745–749PubMedGoogle Scholar
  124. Temple S (2001) The development of neural stem cells. Nature 414:112–117PubMedGoogle Scholar
  125. Thompson JS, Nguyen B-LT, Harty RF (1993) Somatostatin analogue inhibits intestinal regeneration. Arch Surg 128:385–389PubMedGoogle Scholar
  126. Turner RW, Maler L (1999) Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe. J Exp Biol 202:1255–1265PubMedGoogle Scholar
  127. Vajda FJ (2002) Neuroprotection and neurodegenerative disease. J Clin Neurosci 9:4–8PubMedGoogle Scholar
  128. Voigt T (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74–88PubMedGoogle Scholar
  129. Van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034PubMedGoogle Scholar
  130. Waxman SG, Anderson MJ (1986) Regeneration of central nervous structures: Apteronotus spinal cord as a model system. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 183–208Google Scholar
  131. Weiss S, Dunne C, Hewson J, Wohl C, Wheatly M, Peterson AC, Reynolds BA (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16:7599–7609PubMedGoogle Scholar
  132. Wetts R, Herrup K (1983) Direct correlation between Purkinje and granule cell number in the cerebella of lurcher chimeras and wild-type mice. Brain Res 312:41–47PubMedGoogle Scholar
  133. Williams RW (2000) Mapping genes that modulate brain development: a quantitative genetic approach. In: Goffinet AF, Rakic P (eds) Mouse brain development. Springer, Berlin Heidelberg New York, pp 21–49Google Scholar
  134. Zakon HH (1984) Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age. J Comp Neurol 228:557–570PubMedGoogle Scholar
  135. Zakon H, Oestreich J, Tallarovic S, Triefenbach F (2002) EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips. J Physiol (Paris) 96:451–458Google Scholar
  136. Zhang Z, Krebs CJ, Guth L (1997) Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp Neurol 143:141–152PubMedGoogle Scholar
  137. Zieleniewski W, Zieleniewski J (1993) Somatostatin inhibits cell proliferation and corticosterone secretion in the early stage of adrenal regeneration. Cytobios 74:163–166PubMedGoogle Scholar
  138. Zikopoulos B, Kentouri M, Dermon CR (2000) Proliferation zones in the adult brain of a sequential hermaphrodite teleost species (Sparus aurata). Brain Behav Evol 56:310–322PubMedGoogle Scholar
  139. Zupanc GKH (1999a) Neurogenesis, cell death and regeneration in the adult gymnotiform brain. J Exp Biol 202:1435–1446Google Scholar
  140. Zupanc GKH (1999b) Up-regulation of somatostatin after lesions in the cerebellum of the teleost fish Apteronotus leptorhynchus. Neurosci Lett 268:135–138Google Scholar
  141. Zupanc GKH (2001a) Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav Evol 58:250–275Google Scholar
  142. Zupanc GKH (2001b) Distribution of radial glia in the central posterior/prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus. In: Elsner N, Kreutzberg GW (eds) In: Göttingen neurobiology report 2001. Proceedings of the 4th meeting of the German Neuroscience Society 2001; vol II. Georg Thieme Verlag, Stuttgart/New York, pp 976Google Scholar
  143. Zupanc GKH (2002) From oscillators to modulators: behavioral and neural control of modulations of the electric organ discharge in the gymnotiform fish, Apteronotus leptorhynchus. J Physiol (Paris) 96:459–472Google Scholar
  144. Zupanc GKH, Heiligenberg W (1992) The structure of the diencephalic prepacemaker nucleus revisited: light microscopic and ultrastructural studies. J Comp Neurol 323:558–569PubMedGoogle Scholar
  145. Zupanc GKH, Zupanc MM (1992) Birth and migration of neurons in the central posterior/prepacemaker nucleus during adulthood in weakly electric knifefish (Eigenmannia sp.). Proc Natl Acad Sci USA 89:9539–9543PubMedGoogle Scholar
  146. Zupanc GKH, Maler L (1993) Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can J Zool 71:2301–2310CrossRefGoogle Scholar
  147. Zupanc GKH, Horschke I (1995) Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J Comp Neurol 353:213–233PubMedGoogle Scholar
  148. Zupanc GKH, Maler L (1997) Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish. J Comp Physiol A 180:99–111Google Scholar
  149. Zupanc GKH, 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 160:78–87PubMedGoogle Scholar
  150. Zupanc GKH, Clint SC (2003) Potential role of radial glia in adult neurogenesis of teleost fish. Glia 43:77–86PubMedGoogle Scholar
  151. Zupanc GKH, Bullock TH (2005) From electrogenesis to electroreception: an overview. In: Bullock TH, Hopkins CD, Popper EN, Fay RR (eds) Electroreception. Springer, Berlin Heidelberg New York, pp 5–46Google Scholar
  152. Zupanc GKH, Maler L, Heiligenberg W (1991a) Somatostatin-like immunoreactivity in the region of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia: a quantitative analysis. Brain Res 559:249–260Google Scholar
  153. Zupanc GKH, Okawara Y, Zupanc MM, Fryer JN, Maler L (1991b) In situ hybridization of putative somatostatin mRNA in the brain of electric gymnotiform fish. NeuroReport 2:707–710Google Scholar
  154. Zupanc GKH, Cécyre D, Maler L, Zupanc MM, Quirion R (1994) The distribution of somatostatin binding sites in the brain of gymnotiform fish, Apteronotus leptorhynchus. J Chem Neuroanat 7:49–63PubMedGoogle Scholar
  155. Zupanc GKH, Horschke I, Ott R, Rascher GB (1996) Postembryonic development of the cerebellum in gymnotiform fish. J Comp Neurol 370:443–464PubMedGoogle Scholar
  156. Zupanc GKH, Kompass KS, Horschke I, Ott R, Schwarz H (1998) Apoptosis after injuries in the cerebellum of adult teleost fish. Exp Neurol 221–230Google Scholar
  157. Zupanc GKH, Siehler S, Jones EMC, Seuwen K, Furuta H, Hoyer D, Yano H (1999) Molecular cloning and pharmacological characterization of a somatostatin receptor subtype in the gymnotiform fish Apteronotus albifrons. Gen Comp Endocrinol 15:333–345Google Scholar
  158. Zupanc GKH, Clint SC, Takimoto N, Hughes ATL, Wellbrock UM, Meissner D (2003) Spatio-temporal distribution of microglia/macrophages during regeneration in the cerebellum of adult teleost fish, Apteronotus leptorhynchus: a quantitative analysis. Brain Behav Evol 62:31–42PubMedGoogle Scholar
  159. Zupanc GKH, Hinsch K, Gage FH (2005) Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488:290–319PubMedGoogle Scholar
  160. Zupanc GKH, Sîrbulescu RF, Nichols A, Ilies I (2006a) Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus. J Comp Physiol A 192:159–173Google Scholar
  161. Zupanc MM, Wellbrock UM, Zupanc GKH (2006b) Proteome analysis identifies novel protein candidates involved in regeneration of the cerebellum of teleost fish. Proteomics 6:677–696PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.School of Engineering and ScienceInternational University BremenBremenGermany
  2. 2.Department of NeurosciencesUniversity of California at San DiegoLa JollaUSA

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