Generacja komórek w mózgu dorosłych zwierząt historia badań nad neurogenezą

• Authors: Katarzyna Bartkowska

Title variants

EN

Neurogenesis in the brain of adult animals

• Languages of publication: PL EN

Abstracts

EN

Summary Traditional views maintain that the generation of neurons in the brain is restricted to a discrete developmental period. However, it is now commonly known that stem cells remain in the adult central nervous system and that adult vertebrates as well as adult invertebrates are adding new cells in some structures of their central nervous system. The progenitor cells may differentiate into neurons, astrocytes and oligodendrocytes. In some invertebrates (insects) neurogenesis occurs in the mushroom bodies, which are functional analogues of the hippocampus, brain structures involved in learning and memory. In vertebrates, the subventricular zone and the dentate gyrus of the hippocampus are sites of neuronal precursor proliferation. The production and survival of new neurons in the adult brain is regulating by hormones, transmitters, growth factors and environmental factors (stress, season, environmental complexity and experience). The role of newly formed neurons in adult brain remains still questionable. It seems that function of adult generated neurons is related to the brain regions into which new neurons are incorporated. Some experimental data suggest that adult generated neurons play a role in learning andmemory. It is also postulated that neural precursors may be use to achieve repair after brain injury or neurodegenerational diseases.

• Journal: Kosmos
• Year: 2004
• Volume: 53
• Issue: 2
• Pages: 167-181

Dates

published

2004

Contributors

author

Katarzyna Bartkowska

• Pracownia Neurobiologii Rozwoju i Ewolucji Zakład Neurobiologii Molekularnej i Komórkowej Instytut Biologii Doświadczalnej im. M. Nenckiego PAN, Pasteura 3, 02-093 Warszawa, Polska

References

• ABERG M. A., ABERG N. D., HEDBACKER H., OSKARSSON J., ERIKSSON P. S., 2000. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 20, 2896-2903.
• AHMED S., REYNOLDS B. A., WEISS S., 1995. BDNF enhances the differentiation but not the survival of CNS stem cell- derived neuronal precursor. J. Neurosci. 15, 5765-5778.
• ALTMAN J., 1963. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Postnatal growth and differentiation of themammalian brain, with implications for a morphological theory ofmemory. Anat. Rec. 145, 573-591.
• ALTMAN J., DAS G. D., 1967. Postnatal neurogenesis in the guinea-pig. Nature 214, 1098-1101.
• ALVAREZ-BUYLLA A., KIRN J. R., 1997. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol. 33, 585-601.
• ALVAREZ-BUYLLA A., GARCIA-VERDUGO J. M., 2002. Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634.
• ARSENIJEVIC Y.,WEISS S., 1998. Insulin-like growth factor- I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors: distinct actions from those of brain-derived neurotrophic factor. J. Neurosci. 18, 2118-2128.
• BANASR M., HERY M., BREZUN J. M., DASZUTA A., 2001. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur. J. Neurosci. 14, 1417-1424.
• BEHL C., 2002. Oestrogen as a neuroprotective hormone. Nature Rev. 3, 433-442.
• BENRAISS A., CHMIELNICKI E., LERNER K., ROH D., GOLDMAN S. A., 2001. Adenoviral Brain-Derived Neurotrophic Factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J. Neurosci. 21, 6718-6731.
• BERNIER P. J., BEDARD A., VINET J., LEVESQUE M., PARENT A., 2002. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc.Natl. Acad. Sci. USA 99, 11464-11469.
• BIEBL M., COOPER C. M., WINKLER J., KUHN H. G., 2000. Analysis of neurogenesis and programmed cell death reveals a self- renewing capacity in the adult rat brain. Neurosci. Lett. 291, 17-20.
• BREDY T. W., GRANT R. J., CHAMPAGNE D. L., MEANEY M. J., 2003. Maternal care influences neuronal survival in the hippocampus of the rat. Eur. J. Neurosci. 18, 2903-2909.
• BREZUN J. M., DASZUTA A., 1999. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 89, 999-1002.
• CAMERON H. A., GOULD E., 1994. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61, 203-209.
• CAMERON H. A.,MCKAY R. D. G., 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435, 406-417.
• CAMERON H. A., MCEWEN B. S., GOULD E., 1995. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15, 4687-4692.
• CARLETON A., ROCHEFORT C., MORANTE-ORIA J., DESMAISONS D., VINCENT J. D., GHEUSI G., LIEDO P. M., 2002. Making scents of olfactory neurogenesis. J. Physiol. Paris 96, 115-122.
• CARLETON A., PETREANU L. T., LANSFORD R., ALVAREZ-BUYLLA A., LLEDO P. M., 2003. Becoming a new neuron in the adult olfactory bulb. Nature Neurosci. 6, 507-518.
• CAYRE M.,MALATERRE J., SCOTTO-LOMASSESE S., STRAMBI C., STRAMBI A., 2002. The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates. Com. Bioch. Physiol. Part 13, 132, 1-15.
• CHEN X. H., IWATA A.,NONAKA M., BROWNE K. D., SMITH D. H., 2003. Neurogenesis and glial proliferation persist for at least one year in the subventricular zone following brain trauma in rats. J. Neurotrauma 20, 623-631.
• CHIASSON B. J., TROPEPE V., MORSHEAD C. M., VAN DER KOOY D., 1999. Adultmammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J. Neurosci. 19, 4462-4471.
• CID E., VELASCO A., CIUDAD J., ORFAO A., AIJON J., LARA J. M., 2002. Quantitative evaluation of the distribution of proliferating cells in the adult retina in three cyprinid species. Cell Tissue Res. 308, 47-59.
• CLAYTON N. S., 1995. Development of memory and the hippocampus: comparison of food- storing and nonstoring birds on a one- trial associative memory task. J. Neurosci. 15, 2797-2807.
• CLAYTON N. S., KREBS J. R., 1994. Hippocampal growth and attrition in birds affected by experience. Proc. Natl. Acad. Sci. USA 91, 7410-7414.
• COROTTO F. S., HENEGAR J. R., MARUNIAK J. A., 1993. Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci. Lett. 149, 111-114.
• COROTTO F. S., HENEGAR J. R.,MARUNIAK J. A., 1994. Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61, 739-744.
• ERIKSSON P. S., PERFILIEVA E., BJORK-ERIKSSON T., ALBORN A. M., NORDBORG C., PETERSON D. A., GAGE F. H., 1998. Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1207.
• FABEL K., FABEL K., TAM B., KAUFER D., BAIKER A., SIMMONS N., KUO C. J., PALMER T. D., 2003. VEGF is necessary for exercise- induced adult hippocampal neurogenesis. Eur. J. Neurosci. 18, 2803-2812.
• FELLING R. J., LEVISON S. W., 2003. Enhanced neurogenesis following stroke. J.Neurosci. Res. 73, 277-283.
• FUCHS E., GOULD E., 2000. In vitro neurogenesis in the adult brain: regulation and functional implication. Eur. J. Neurosci. 12, 2211-2214.
• GAGE F. H., 2000. Mammalian neural stem cells. Science 287, 1433-1438.
• 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.
• GOULD E., 1994. The effects of adrenal steroids and excitatory input on neuronal birth and survival. Ann. NY Acad. Sci. 743, 73-93.
• GOULD E., 1999. Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 21, 46S-51S.
• GOULD E., GROSS C. G., 2002. Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22, 619-623.
• GOULD E., CAMERON H. A., DANIELS D. C., WOOLLEY C. S., MCEWEN B. S., 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci. 12, 3642-3650.
• GOULD E., MCEWEN B. S., TANAPAT P., GALEA L. A. M., 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, 2492-2498.
• GOULD E., TANAPAT P.,MCEWEN B. S., FLUGGE 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, 3168-3171.
• GOULD E., BEYLIN A., TANAPAT P., REEVES A., SHORS T. J., 1999a. Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265.
• GOULD E., REEVES A. J., GRAZIANO M. S. A., GROSS C. G., 1999b. Neurogenesis in the neocortex of adult primates. Science 286, 548-552.
• GOULD E., TANAPAT P., HASTINGS N., 2000. Regulation of hippocampal neurogenesis in adulthood. Biol. Psychiatry 48, 715-720.
• GREGG C. T., CHOJNACKI A. K.,WEISS S., 2002. Radial glia cells as neuronal precursors: the next generation? J. Neurosci. Res. 69, 708-713.
• GRITTI A., BONFANTI L., DOETSCH F., CAILLE I., ALVAREZ-BUYLLA A., LIM D. A.,GALLI R., VERDUGO J. M. G., HERRERA D. G., VESCOVI A. L., 2002a. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J. Neurosci. 22, 437-445.
• GRITTI A., VESCOVI A. L., GATI R., 2002b. Adult neural stem cells: plasticity and developmental potential. J. Physiol. Paris 96, 81-90.
• HASTINGS N. B., TANAPAT P., GOULD E., 2000. Comparative views of adult neurogenesis. TheNeuroscientist 6, 315-325.
• HUANG L., DEVRIES G. J., BITTMAN E. L., 1998. Photoperiod regulates neural bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J. Neurobiol. 36, 410-420.
• JIN K.,MINAMI M., LAN J. Q.,MAO X. O., BATTEUR S., SIMON R. P., GREENBERG D. A., 2001. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. USA 98, 4710-4715.
• JIN K., ZHU Y., SUN Y.,MAO X. O., XIE L., GREENBERG D. A., 2002. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. USA 99, 11946-11950.
• JOHANSSON C. B., MOMMA S., CARKE D. L., RISLING M., LENDAHL U., FRISEN J., 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 96, 25-34.
• KAPLAN M. S., HINDS J. W., 1997. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197, 1092-1094.
• KEMPERMANN G., KUHN H. G., GAGE F. H., 1997. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc. Natl. Acad. Sci. USA 94, 10409-10414.
• KEMPERMANN G., GAST D., KRONENBERG G., YAMAGUCHI M., GAGE F. H., 2003. Early determination and long- term persistence of adult- generated new neurons in the hippocampus of mice. Development 130, 391-399.
• KERNIE S. G., ERWIN T. M., PARADA L.F., 2001. Brain remodeling due to neuronal and astrocytic proliferation after controlled cortical injury in mice. J. Neurosci. Res. 66, 317-326.
• KIM J. J., DIAMOND D. M., 2002. The stressed hippocampus, synaptic plasticity and lost memories. Neuroscience 3, 453-462.
• KIRSCHENBAUM B., GOLDMAN S. A., 1995. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl. Acad. Sci. USA 92, 210-214.
• KORNACK D. R., RAKIC P., 1999. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. USA 96, 5768-5773.
• KORNACK D. R., RAKIC P., 2001a. The generation,migration, and differentiation of olfactory neurons in the adult primate brain. Proc.Natl. Acad. Sci.USA 98, 4752-4757.
• KORNACK D. R., RAKIC P., 2001b. Cell proliferation without neurogenesis in adult primate neocortex. Science 294, 2127-2130.
• KOZOROVITSKIY Y., GOULD E., 2003. Adult neurogenesis: a mechanism for brain repair? J. Clin. Exp. Neuropsychol. 25, 721-732.
• KUHN H. G., DICKINSON-ANSON H., GAGE F. H., 1996. Neurogenesis in the dentate gyrus of the adult rat: agerelated decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033.
• KUHN H. G.,WINKLER J., KEMPERMANN G., THAL L. J., GAGE F. H., 1997. Epidermal Growth Factor and Fibroblast Growth Factor-2 Have Different Effects on Neural Progenitors in the Adult Rat Brain. J. Neurosci. 17, 5820-5829.
• LAVENEX P., STEELE M. A., JACOBS L. F., 2000. The seasonal pattern of cell proliferation and neuron number in the dentate gyrus ofwild adult eastern grey squirrels. Eur. J. Neurosci. 12, 643-648.
• LING C., ZUO M., ALVAREZ-BUYLLA A., CHENG M. F., 1997. Neurogenesis in juvenile and adult ring doves. J. Comp. Neurol. 379, 300-312.
• LIU J., SOLWAY K.,MESSING R. O., SHARP F. R., 1998. Increased neurogenesis in theDGafter transient global ischemia in gerbils. J. Neurosci. 18, 7768-7778.
• LIU S. H.,WANG J., ZHU D. Y., FU Y. P., LUKOWIAK K., LU Y. M., 2003. Generation of functional inhibitory neurons in the adult rat hippocampus. J. Neurosci. 23, 732-736.
• LIU Z., MARTIN L. J., 2003. Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J. Comp. Neurol. 459, 368-391.
• 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, 2074-2077.
• LUCASSEN P. J., VOLLMANN-HONSDORF G. K., GLEIBERG M., CZEH B.,DEKLOET E. R., FUCHS E., 2001. Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur. J. Neurosci. 14, 161-166.
• MADSEN T. M., KRISTJANSEN P. E. G., BOLWIG T. G., WORTWEIN G., 2003. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119, 635-642.
• MAGAVI S. S., LEAVITT B. R., MACKLIS J. D., 2000. Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951-955.
• MAGAVI S. S., MACKLIS J. D., 2001. Manipulation of neural precursors in situ: induction of neurogenesis in the neocortex of adultmice. Neuropsychopharmacology 25, 816-835.
• MARKAKIS E. A., GAGE F. H., 1999. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol. 406, 449-460.
• MARTENS D. J., TROPEPE V., VAN DER KOOY D., 2000. Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J. Neurosci. 20, 1085-1095.
• MASLOV A., BARONE T. A., PLUNKETT R. J., PRUITT S. C., 2004. Neural stem cell detection, characterization and age related changes in the subventricular zone of mice. J. Neurosci. 24, 1726-1733.
• MERRILL D. A., KARIM R., SARRAQ M., CHIBA A. A., TUSZYNSKI M. H., 2003. Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol. 459, 201-207.
• 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.
• MOMMA S., JOHANSSON C. B., FRISEN J., 2000. Get to know your stem cells. Curr. Opin.Neurobiol. 10, 45-49.
• MONTARON M. F., PIAZZA P. V., AUROUSSEAU C., URANI A., LEMOAL M., ABROUS D. N., 2003. Implication of corticosteroid receptors in the regulation of hippocampal structural plasticity. Eur. J. Neurosci. 18, 3105-3111.
• MORSHEAD C. M., VAN DER KOOY D., 2004. Disguising adult neural stem cells. Curr. Opin. Nurobiol. 14, 125-131.
• MUSKHELISHVILI L., LATENDRESSE J. R., KODEL R. L., HENDERSON E. B., 2003. Evaluation of cell proliferation in rat tissues with BrdU, PCNA, Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. J. Histochem. Cytochem. 51, 1681-1688.
• NACHER J., ROSELL D. R., ALONSO-LLOSA G., MCEWEN B. S., 2001. NMDA receptor antagonist treatment induces a long- lasting increase in the number of proliferating cells, PSA- NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur. J. Neurosci. 13, 512-520.
• NILSSON M., PERFILIEVA E., JOHANSSON U., ORWAR O., ERIKSSON P. S., 1999. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 39, 569-578.
• PALMER T. D., RAY J., GAGE F. H., 1995. FGF-2- responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell. Neurosci. 6, 474-486.
• PARENT J. M., 2003. Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 9, 261-271.
• PARENT J. M., VALENTIN V. V., LOWENSTEIN D. H., 2002. Prolonged seizures increase proliferating neuroblast in the adult rat subventricular zone- olfactory bulb pathway. J. Neurosci. 22, 3174-3188.
• PENCEA V., BINGAMAN K. D., WIEGAND S. J., LUSKIN M. B., 2001. Infusion of Brain-Derived Neurotrophic Factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus and hypothalamus. J. Neurosci. 21, 6706-6717.
• PEREZ-MARTIN M., AZCOITIA I., TREJO J. L., SIERRA A., GARCIA-SEGURA L. M., 2003. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur. J. Neurosci. 18, 923-930.
• QIAN X.,DAVIS A. A.,GODERIE S. K., TEMPLE S., 1997. FGF2 concentration regulates the generation of neurons and glia frommultipotent cortical stem cells. Neuron 18, 81-93.
• RA S. M., KIM H., JANG M. H., SHIN M. C., LEE T. H., LIM B. V., KIM C. J., KIM E. H., KIM K. M., KIM S. S., 2002. Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci. Lett. 333, 123-126.
• RADLEY J. J., JACOBS B. L., 2002. 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res. 955, 264-267.
• RAKIC P., 1985. Limits of neurogenesis in primates. Science 1054-1056.
• RAKIC P., 2002a. Neurogenesis in adult primates. Progress Brain Res. 138, 3-14.
• RAKIC P., 2002b. Adult neurogenesis in mammals: an identity crisis. J. Neurosci. 22, 614-618.
• RAMIREZ C.,NACHER J.,MOLOWNY A., SANCHEZ-SANCHEZ F., IRURZUN A., LOPEZ-IRURZUN GARCIA C., 1997. Photoperiod- temperature and neuroblast proliferation- migration in the adult lizard cortex. Neuroreport 8, 2337-2342.
• REBOREDA J. C., CLAYTON N. S., KACELNIK A., 1996. Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport 7, 505-508.
• RIETZE R. L., VALCANIS H., BROOKER G. F., THOMAS T., VOSS A. K., BARTLETT P. F., 2001. Purification of a pluripotent Nature 412, 736-739.
• ROCHEFORT C.,GHEUSI G., VINCENT J.D., LIEDO P.M., 2002. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689.
• SANTARELLI L., SAXE M., GROSS C., SURGET A., BATTAGLIA F., DULAWA S., WEISSTAUB N., LEE J., DUMAN R., ARANCIO O., BELZUNG C., HEN R., 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809.
• SEABERG R. M., VAN DER KOOY D., 2002. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22, 1784-1793.
• SEABERG R. M., VAN DER KOOY D., 2003. Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci. 26, 125-131.
• SEKI T., ARAI Y., 1995. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6, 2479-2482.
• SERI B., GARCIA-VERDUGO J. M., MCEWEN B. S., ALVAREZ-BUYLLA A., 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21, 7153-7160.
• SHORS T. J., MIESEGAES G., BEYLIN A., ZHAO M., RYDEL T., GOULD E., 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-375.
• SHORS T. J., TOWNSEND D. A., ZHAO M., KOZOROVITSKY Y., GOULD E., 2002. Neurogenesis may relate to some but not all types of hippocampal- dependent learning. Hippocampus 12, 578-584.
• SIDMAN R. L., MIALE I. L., FEDER N., 1959. Cell proliferation and migration in the primitive ependymal zone; an autoradiographic study of histogenesis in the nervous system. Exp. Neurol. 1, 322-333.
• SUHONEN J. O., PETERSON D. A., RAY J., GAGE F. H., 1996. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383, 624-627.
• 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.
• TANAPAT P., HASTINGS N. B., RYDEL T. A., GALEA L. A. M., GOULD E., 2001. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone- dependent mechanism. J. Comp. Neurol. 437, 496-504.
• TAUPIN P., GAGE F. H., 2002. Adult neurogenesis and neural stem cells of the Central Nervous System in mammals. J. Neurosci. Res. 69, 745-749.
• TONCHEV A. B., YAMASCHIMA T., ZHAO L.,OKANO H., 2003. Differential proliferative response in the postischemic hippocampus, temporal cortex, and olfactory bulb of young adult macaque monkeys. Glia 42, 209-224.
• TRAMONTIN A. D., BRENOWITZ E. A., 2000. Seasonal plasticity in the adult brain. Trends Neurosci. 23, 251-258.
• TREJO J. L., CARRO E., TORRES-ALEMAN I., 2001. Circulating insulin-like growth factor I mediates exercise- induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21, 1628-1634.
• TURLEJSKI K., DJAVADIAN R., 2002. Life-long stability of neurons: a century of research on neurogenesis, neuronal death and neuron quantification in adult CNS. Prog. Brain Res. 136, 39-65.
• WINNER B., COOPER-KUHN C. M., AIGNER R., WINKLER J., KUHN H. G., 2002. Long- term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci. 16, 1681-1689.
• VAN PRAAG H., KEMPERMANN G., GAGE F. H., 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neurosci. 2, 266-270.
• VAN PRAAG H., KEMPERMANN G., GAGE F. H., 2000. Neural consequences of environmental enrichment. Neuroscience 1, 191-198.
• VAN PRAAG H., SCHINDER A. F., CHRISTIE B. R., TONI N., PALMER T. D.,GAGE F. H., 2002. Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034.
• VICARIO-ABEJON C., COLLIN C., TSOULFAS P., MCKAY R., D. G., 2000. Hippocampal stem cells differentiate into excitatory and inhibitory neurons. Eur. J. Neurosci. 12, 677-688.
• ZHAMG L., CHANG Y. H., BARKER J. L., HU Q., ZHAMG L., MARIC D., LI B., RUBINOW D. R., 2000. Testosterone and estrogen effect neuronal differentiation but not proliferation in early embryonic cortex of the rat: the possible roles of androgen and estrogen receptors. Neurosci. Lett. 281, 57-60.
• ZHAO M., MOMMA S., DELFANI K., CARLEN M., CASSIDY R. M., JOHANSSON C. B., BRISMAR H., SHUPLIAKOV O., FRISEN J., JANSON A. M., 2003. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. USA 100, 7925-7930.
• ZIGOVA T., PENCEA V., WIEGAND S. I., LUSKIN M. B., 1998. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci. 11, 234-45.
• ZITNIK G., MARTIN G. M., 2002. Age-related decline in neurogenesis: old cells or old environment? J. Neurosci. Res. 70, 258-263.