DOI QR코드

DOI QR Code

Adult Neurogenesis in Insulted Brain

  • Kim, Byung-Woo (Department of Biochemistry and Molecular Biology, Hanyang University College of Medicine) ;
  • Son, Hyeon (Department of Biochemistry and Molecular Biology, Hanyang University College of Medicine)
  • Published : 2007.06.30

Abstract

Although there are some questions about the venues of adult neurogenesis, it is undoubtedly accepted that new neurons are born in adult brains. Adult neurogenesis is regulated by a wide array of factors. Insults harmful to brain, such as neurodegenerative diseases, seizure, ischemia and exposure to drugs of abuse, are intricately related to adult neurogenesis. Whereas neurodegenerative diseases are characterized by death or functional loss of specific neurons, recent studies report that they can be accompanied by neurogenesis. In addition, alcohol and drugs of abuse which have been reputed to cause irreversible damage to brain can also generate newly born cells in adult brain. As yet, however, we have little knowledge of the functional significance and roles of adult neurogenesis under pathological settings, not to mention under physiological settings. Accordingly, in this review we briefly summarize the results of studies which focus on adult neurogenesis in insulted brain, instead of trying to draw hurried conclusion regarding the relationship between adult neurogenesis and brain insults.

Keywords

References

  1. Aberg, E., Hofstetter, C.P., Olson, L. and Brene, S. (2005). Moderate ethanol consumption increases hippocampal cell proliferation and neurogenesis in the adult mouse. Int.J. europsychopharmacol., 8, 557-567 https://doi.org/10.1017/S1461145705005286
  2. Abrous, D.N., Koehl, M. and Le Moal, M. (2005). Adult neurogenesis: from precursors to network and physiology. Physiol. Rev., 85, 523-569 https://doi.org/10.1152/physrev.00055.2003
  3. Agartz, I., Momenan, R., Rawlings, R.R., Kerich, M.J. and Hommer, D.W. (1999). Hippocampal volume in patients with alcohol dependence. Arch. Gen. Psychiatry, 56, 356- 363 https://doi.org/10.1001/archpsyc.56.4.356
  4. Altman, J. and Das, G.D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol., 124, 319-335 https://doi.org/10.1002/cne.901240303
  5. Alvarez-Buylla, A. and Garcia-Verdugo, J.M. (2002). Neurogenesis in adult subventricular zone. J. Neurosci., 22, 629-634 https://doi.org/10.1523/JNEUROSCI.22-03-00629.2002
  6. Alvarez-Buylla, A., Theelen, M. and Nottebohm, F. (1988). Birth of projection neurons in the higher vocal enter of the canary forebrain before, during, and after song learning. Proc. Natl. Acad. Sci. USA, 85, 8722-87 https://doi.org/10.1073/pnas.85.22.8722
  7. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. and Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med., 8, 963-970 https://doi.org/10.1038/nm747
  8. Arvidsson, A., Kokaia, Z. and Lindvall, O. (2001). N-methyl-Daspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur. J. Neurosci., 14, 10-18 https://doi.org/10.1046/j.0953-816x.2001.01611.x
  9. Bedard, A., Cossette, M., Levesque, M. and Parent, A. (2002). Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci. Lett., 328, 213-216 https://doi.org/10.1016/S0304-3940(02)00530-X
  10. Bedard, A. and Parent, A. (2004). Evidence of newly generated neurons in the human olfactory bulb. Dev. Brain Res., 151, 159-168 https://doi.org/10.1016/j.devbrainres.2004.03.021
  11. Bengochea, O. and Gonzalo, L.M. (1990). Effect of chronic alcoholism on the human hippocampus. Histol. Histopathol., 5, 349-357
  12. Bengzon, J., Kokaia, Z., Elmer, E., Nanobashvili, A., Kokaia, M. and Lindvall, O. (1997). Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. USA, 94, 10432-10437 https://doi.org/10.1073/pnas.94.19.10432
  13. Borta, A. and Hoglinger, G.U. (2007). Dopamine and adult neurogenesis. J. Neurochem., 100, 587-595 https://doi.org/10.1111/j.1471-4159.2006.04241.x
  14. Chen, Y., Ai, Y., Slevin, J.R., Maley, B.E. and Gash, D.M. (2005). Progenitor proliferation in the adult hippocampus and substantia nigra induced by glial cell line-derived neurotrophic factor. Exp. Neurol., 196, 87-95 https://doi.org/10.1016/j.expneurol.2005.07.010
  15. Choi, Y.S., Lee, M.Y., Sung, K.W., Jeong, S.W., Choi, J.S., Park, H.J., Kim, O.N., Lee, S.B. and Kim, S.Y. (2003). Regional differences in enhanced neurogenesis in the dentate gyrus of adult rats after transient forebrain ischemia. Mol. Cells, 16, 232-238
  16. Conover, J.C. and Allen, R.L. (2002). The subventricular zone: new molecular and cellular developments. Cell Mol. Life Sci., 59, 2128-2135 https://doi.org/10.1007/s000180200012
  17. Cooper, O. and Isacson, O. (2004). Intrastriatal transforming growth factor a delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J. Neurosci., 24, 8924-8931 https://doi.org/10.1523/JNEUROSCI.2344-04.2004
  18. Crews, F.T., Mdzinarishvili, A., Kim, D., He, J. and Nixon, K. (2006). Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience, 137, 437-445 https://doi.org/10.1016/j.neuroscience.2005.08.090
  19. Crews, F.T., Miller, M.W., Ma, W., Nixon, K., Zawada, W.M. and Zakhari, S. (2003). Neural stem cells and alcohol. Alcohol Clin. Exp. Res., 27, 324-335 https://doi.org/10.1097/01.ALC.0000052581.46630.C5
  20. Curtis, M.A., Penney, E.B., Pearson, A.G., van Roon-Mom, W.M., Butterworth, N.J., Dragunow, M., Connor, B. and Faull, R.L. (2003). Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl. Acad. Sci. USA, 100, 9023-9027 https://doi.org/10.1073/pnas.1532244100
  21. Darsalia, V., Heldmann, U., Lindvall, O. and Kokaia, Z. (2005). Stroke-induced neurogenesis in aged brain. Stroke, 36, 1790-1795 https://doi.org/10.1161/01.STR.0000173151.36031.be
  22. Dayer, A.G., Cleaver, K.M., Abouantoun, T. and Cameron, H.A. (2005). New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol., 168, 415-427 https://doi.org/10.1083/jcb.200407053
  23. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M. and Cameron, H.A. (2003). Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol., 460, 563-572 https://doi.org/10.1002/cne.10675
  24. Dominguez-Escriba, L., Hernandez-Rabaza, V., Soriano-Navarro, M., Barcia, J.A., Romero, F.J., Garcia-Verdugo, J.M. and Canales, J.J. (2006). Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur. J. Neurosci., 24, 586-594 https://doi.org/10.1111/j.1460-9568.2006.04924.x
  25. Donovan, M.H., Yazdani, U., Norris, R.D., Games, D., German, D.C. and Eisch, A.J. (2006). Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J. Comp. Neurol., 495, 70-83 https://doi.org/10.1002/cne.20840
  26. Eisch, A.J. and Harburg, G.C. (2006). Opiates, psychostimulants, and adult hippocampal neurogenesis: insights for addiction and stem cell biology. Hippocampus, 16, 271- 286 https://doi.org/10.1002/hipo.20161
  27. Eisch, A.J., Barrot, M., Schad, C.A., Self, D.W. and Nestler, E.J. (2000) Opiates inhibit neurogenesis in the adult rat hippocampus: Proc. Natl. Acad. Sci. USA, 97, 7579-7584 https://doi.org/10.1073/pnas.120552597
  28. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A. and Gage, F.H. (1998). Neurogenesis in the adult human hippocampus. Nature Med., 4, 1313-1317 https://doi.org/10.1038/3305
  29. Everitt, B.J., Dickinson, A. and Robbins, T.W. (2001). The neuropsychological basis of addictive behaviour. Brain Res. Brain Res. Rev., 36, 129-138 https://doi.org/10.1016/S0165-0173(01)00088-1
  30. Frielingsdorf, H., Schwarz, K., Brundin, P. and Mohapel, P. (2004). No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. USA, 101, 10177-10182 https://doi.org/10.1073/pnas.0401229101
  31. Fuchs, E., Flugge, G. and Czeh, B. (2006). Remodeling of neuronal networks by stress. Front.Biosci., 11, 2746-2758 https://doi.org/10.2741/2004
  32. Fuchs, R.A., Evans, K.A., Ledford, C.C., Parker, M.P., Case, J.M., Mehta, R.H. and See, R.E. (2005). The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology, 30, 296-309 https://doi.org/10.1038/sj.npp.1300579
  33. Gage, F.H. (2000). Mammalian neural stem cells. Science, 287, 1433-1438 https://doi.org/10.1126/science.287.5457.1433
  34. Gil, J.M., Mohapel, P., Araujo, I.M., Popovic, N., Li, J.Y., Brundin, P. and Petersen, A. (2005). Reduced hippocampal neurogenesis in R6/2 transgenic Huntington's disease mice. Neurobiol. Dis., 20, 744-751 https://doi.org/10.1016/j.nbd.2005.05.006
  35. Gould, E. (2007). How widespread is adult neurogenesis in mammals? Nat. Rev. Neurosci., 8, 481-488 https://doi.org/10.1038/nrn2147
  36. Gould, E., Reeves, A.J., Fallah, M., Tanapat, P., Gross, C.G. and Fuchs, E. (1999a). Hippocampal neurogenesis in adult Old World primates. Proc. Natl. Acad. Sci. USA, 96, 5263-5267 https://doi.org/10.1073/pnas.96.9.5263
  37. Gould, E., Reeves, A.J., Graziano, M.S. and Gross, C.G. (1999b). Neurogenesis in the neocortex of adult primates. Science, 286, 548-552 https://doi.org/10.1126/science.286.5439.548
  38. Gray, W.P. and Sundstrom, L.E. (1998). Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res., 790, 52-59 https://doi.org/10.1016/S0006-8993(98)00030-4
  39. Hattiangady, B., Rao, M.S. and Shetty, A.K. (2004). Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus. Neurobiol. Dis., 17, 473-490 https://doi.org/10.1016/j.nbd.2004.08.008
  40. Haughey, N.J., Nath, A., Chan, S.L., Borchard, A.C., Rao, M.S., Mattson, M.P. (2002a). Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J. Neurochem., 83, 1509-1524 https://doi.org/10.1046/j.1471-4159.2002.01267.x
  41. Haughey, N.J., Liu, D., Nath, A., Borchard, A.C. and Mattson, M.P. (2002b). Disruption of neurogenesis in the subventricular zone of adult mice and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med., 1, 125-135 https://doi.org/10.1385/NMM:1:2:125
  42. He, J., Nixon, K., Shetty, A.K. and Crews, F.T. (2005). Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur. J. Neurosci., 21, 2711-2720 https://doi.org/10.1111/j.1460-9568.2005.04120.x
  43. Hernandez-Rabaza, V., Dominguez-Escriba, L., Barcia, J.A., Rosel, J.F., Romero, F.J., Garcia-Verdugo, J.M. and Canales, J.J. (2006). Binge administration of 3,4-methylenedioxymethamphetamine (''ecstasy'') impairs the survival of neural precursors in adult rat dentate gyrus. Neuropharmacology, 51, 967-973 https://doi.org/10.1016/j.neuropharm.2006.06.019
  44. Herrera, D.G., Yague, A.G, Johnsen-Soriano, S., Bosch-Morell, F., Collado-Morente, L., Muriach, M., Romero, F.J. and Garcia-Verdugo, J.M. (2003). Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc. Natl. Acad. Sci. USA, 100, 7919-7924 https://doi.org/10.1073/pnas.1230907100
  45. Hoglinger, G.U., Rizk, P., Muriel, M.P., Duyckaerts, C., Oertel, W.H., Caille, I. and Hirsch, E.C. (2004). Dopamine depletion impairs precursor cell proliferation in Parkinson's disease. Nat. Neurosci., 7, 726-735 https://doi.org/10.1038/nn1265
  46. Jakubs, K., Nanobashvili, A., Bonde, S., Ekdahl, C.T., Kokaia, Z., Kokaia, M. and Lindvall, O. (2006). Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron, 52, 1047-1059 https://doi.org/10.1016/j.neuron.2006.11.004
  47. Jang, M.H., Shin, M.C., Kim, E.H. and Kim, C.J. (2002). Acute alcohol intoxication decreases cell proliferation and nitric oxide synthase expression in dentate gyrus of rats. Toxicol. Lett., 133, 255-262 https://doi.org/10.1016/S0378-4274(02)00129-7
  48. Jin, K., Galvan, V., Xie, L., Mao, X.O., Gorostiza, O.F., Bredesen, D.E. and Greenberg, D.A. (2004a). Enhanced neurogenesis in Alzheimer's disease transgenic (PDGFAPPSw, Ind) mice. Proc. Natl. Acad. Sci. USA, 101, 13363- 13367 https://doi.org/10.1073/pnas.0403678101
  49. Jin, K., Minami, M., Lan, J.Q., Mao, X.O., Batteur, S., Simon, R.P. and 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 https://doi.org/10.1073/pnas.081011098
  50. Jin, K., Peel, A.L., Mao, X.O., Xie, L., Cottrell, B.A., Henshall, D.C. and Greenberg, D.A. (2004b). Increased hippocampal neurogenesis in Alzheimer's disease. Proc.Natl. Acad. Sci. USA, 101, 343-347 https://doi.org/10.1073/pnas.2634794100
  51. Kahn, L., Alonso, G., Normand, E. and Manzoni, O.J. (2005). Repeated morphine treatment alters polysialylated neural cell adhesion molecule, glutamate decarboxylase-67 expression and cell proliferation in the adult rat hippocampus. Eur. J. Neurosci., 21, 493-500 https://doi.org/10.1111/j.1460-9568.2005.03883.x
  52. Kokoeva, M.V., Yin, H. and Flier, J.S. (2005). Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science, 310, 679-683 https://doi.org/10.1126/science.1115360
  53. Komitova, M., Perfilieva, E., Mattsson, B., Eriksson, P.S. and Johansson, B.B. (2002). Effects of cortical ischemia and postischemic environmental enrichment on hippocampal cell genesis and differentiation in the adult rat. J. Cereb. Blood Flow Metab., 22, 852-860 https://doi.org/10.1097/00004647-200207000-00010
  54. Kornack, D.R. and Rakic, P. (1999). Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. USA, 96, 5768-5773 https://doi.org/10.1073/pnas.96.10.5768
  55. Kralic, J.E., Ledergerber, D.A. and Fritschy, J.M. (2005). Disruption of the neurogenic potential of the dentate gyrus in a mouse model of temporal lobe epilepsy with focal seizures. Eur. J. Neurosci., 22, 1916-1 https://doi.org/10.1111/j.1460-9568.2005.04386.x
  56. Laakso, M.P., Vaurio, O., Savolainen, L., Repo, E., Soininen, H., Aronen, H.J. and Tiihonen, J. (2000). A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism. Behav. Brain Res., 109, 177-186 https://doi.org/10.1016/S0166-4328(99)00172-2
  57. Lazic, S.E., Grote, H., Armstrong, R.J., Blakemore, C., Hannan, A.J., van Dellen, A. and Barker, R.A. (2004). Decreased hippocampal cell proliferation in R6/1 Huntington's mice. Neuroreport, 15, 811-813 https://doi.org/10.1097/00001756-200404090-00014
  58. Leavitt, B.R., Hernit-Grant, C.S. and Macklis, J.D. (1999). Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp. Neurol., 157, 43-57 https://doi.org/10.1006/exnr.1999.6982
  59. Lie, D.C., Song, H., Colamarino, S.A., Ming, G.L. and Gage, F.H. (2004). Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol., 44, 399-421 https://doi.org/10.1146/annurev.pharmtox.44.101802.121631
  60. Liu, J., Solway, K., Messing, R.O. and Sharp, F.R. (1998). Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci., 18, 7768- 7778 https://doi.org/10.1523/JNEUROSCI.18-19-07768.1998
  61. Lopez-Toledano, M.A. and Shelanski, M.L. (2004). Neurogenic effect of beta-amyloid peptide in the development of neural stemcells. Neurosci., 24, 5439-5444 https://doi.org/10.1523/JNEUROSCI.0974-04.2004
  62. Luo, J. and Miller, M.W. (1998). Growth factor-mediated neural proliferation: Target of ethanol toxicity. Brain Res. Rev., 27, 157-167 https://doi.org/10.1016/S0165-0173(98)00009-5
  63. Magavi, S.S., Leavitt, B.R. and Macklis, J.D. (2000). Induction of neurogenesis in the neocortex of adult mice. Nature, 405, 951-955 https://doi.org/10.1038/35016083
  64. Mandyam, C.D., Norris, R.D. and Eisch, A.J. (2004). Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone. J. Neurosci. Res., 76, 783-794 https://doi.org/10.1002/jnr.20090
  65. Mao, L., Lau, Y.S., Petroske, E. and Wan, J.Q. (2001). Profound astrogenesis in the striatum of adult mice following nigrostriatal dopaminergic lesion by repeated MPTP administration. Dev. Brain Res., 131, 57-65 https://doi.org/10.1016/S0165-3806(01)00260-7
  66. Mathern, G.W., Leiphart, J.L., De Vera, A., Adelson, P.D., Seki, T., Neder, L. and Leite, J.P. (2002). Seizures decrease postnatal neurogenesis and granule cell development in the human fascia dentata. Epilepsia, 43 Suppl 5, 68-73
  67. Nakagawa, E., Aimi, Y., Yasuhara, O., Tooyama, I., Shimada, M., McGeer, P.L. and Kimura, H. (2000). Enhancement of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epilepsy. Epilepsia, 41, 10-18
  68. Nithianantharajah, J. and Hannan, A.J. (2006). Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci., 7, 697-709 https://doi.org/10.1038/nrn1970
  69. Nixon, K. and Crews, F.T. (2004). Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J. Neurosci., 24, 9714- 9722 https://doi.org/10.1523/JNEUROSCI.3063-04.2004
  70. Nixon, K. and Crews, F.T. (2002). Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J. Neurochem., 83, 1087-1093 https://doi.org/10.1046/j.1471-4159.2002.01214.x
  71. Obernier, J.A., Bouldin, T.W. and Crews, F.T. (2002). Binge ethanol exposure in adult rats causes necrotic cell death. Alcohol Clin. Exp. Res., 26, 547-557 https://doi.org/10.1111/j.1530-0277.2002.tb02573.x
  72. Ohab, J.J., Fleming, S., Blesch, A. and Carmichael, S.T. (2006). A neurovascular niche for neurogenesis after stroke. J. Neurosci., 26, 13007-13016 https://doi.org/10.1523/JNEUROSCI.4323-06.2006
  73. Olson, A.K., Eadie, B.D., Ernst, C. and Christie, B.R. (2006). Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus, 16, 250-260 https://doi.org/10.1002/hipo.20157
  74. Overstreet-Wadiche, L.S., Bromberg, D.A., Bensen, A.L. and Westbrook, G.L. (2006). Seizures accelerate functional integration of adult-generated granule cells. J. Neurosci., 26, 4095-4103 https://doi.org/10.1523/JNEUROSCI.5508-05.2006
  75. Palmer, T.D., Willhoite, A.R. and Gage, F.H. (2000). Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol., 425, 479-494 https://doi.org/10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3
  76. Parent, J.M., Elliott, R.C., Pleasure, S.J., Barbaro, N.M. and Lowenstein, D.H. (2006). Aberrant seizure-induced neurogenesis in experimental temporal lobe epilepsy. Ann. Neurol., 59, 81-91 https://doi.org/10.1002/ana.20699
  77. Parent, J.M. and Lowenstein, D.H. (1997). Mossy fiber reorganization in the epileptic hippocampus. Curr. Opin. Neurol., 10, 103-109 https://doi.org/10.1097/00019052-199704000-00006
  78. Parent, J.M., Valentin, V.V. and Lowenstein, D.H. (2002a). Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J. Neurosci., 22, 3174-3188 https://doi.org/10.1523/JNEUROSCI.22-08-03174.2002
  79. Parent, J.M., Vexler, Z.S., Gong, C., Derugin, N. and Ferriero, D.M. (2002b). Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol., 52, 802-813 https://doi.org/10.1002/ana.10393
  80. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S. and Lowenstein, D.H. (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci., 17, 3727-37 https://doi.org/10.1523/JNEUROSCI.17-10-03727.1997
  81. Pelchat, M.L., Johnson, A., Chan, R., Valdez, J. and Ragland, J.D. (2004). Images of desire: food-craving activation during fMRI. Neuroimage, 23, 1486-1493 https://doi.org/10.1016/j.neuroimage.2004.08.023
  82. Reimers, D., Herranz, A.S., Diaz-Gil, J.J., Lobo, M.V., Paino, C.L., Alonso, R., Asensio, M.J., Gonzalo-Gobernado, R. and Bazan, E. (2006). Intrastriatal infusion of liver growth factor stimulates dopamine terminal sprouting and partially restores motor function in 6-hydroxydopamine-lesioned rats. J. Histochem. Cytochem., 54, 457-465 https://doi.org/10.1369/jhc.5A6805.2005
  83. Rice, A.C., Bullock, M.R. and Shelton, K.L. (2004). Chronic ethanol consumption transiently reduces adult neural progenitor cell proliferation. Brain Res., 1011, 94-98 https://doi.org/10.1016/j.brainres.2004.01.091
  84. Rosas, H.D., Koroshetz, W.J., Chen, Y.I., Skeuse, C., Vangel, M., Cudkowicz, M.E., Caplan, K., Marek, K., Seidman, L.J., Makris, N., Jenkins, B.G. and Goldstein, J.M. (2003). Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology, 60, 1615-1620 https://doi.org/10.1212/01.WNL.0000065888.88988.6E
  85. Sadgrove, M.P., Chad, J.E. and Gray, W.P. (2005). Kainic acid induces rapid cell death followed by transiently reduced cell proliferation in the immature granule cell layer of rat organotypic hippocampal slice cultures. Brain Res., 1035, 111-119 https://doi.org/10.1016/j.brainres.2004.11.059
  86. Saxe, M.D., Malleret, G., Vronskaya, S., Mendez, I., Garcia, A.D., Sofroniew, M.V., Kandel, E.R. and Hen, R. (2007). Paradoxical influence of hippocampal neurogenesis on working memory. Proc. Natl. Acad. Sci. USA, 104, 4642- 4646 https://doi.org/10.1073/pnas.0611718104
  87. Scharfman, H.E., Goodman, J.H. and Sollas, A.L. (2000). Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J. Neurosci., 20, 6144-6158 https://doi.org/10.1523/JNEUROSCI.20-16-06144.2000
  88. Scharfman, H.E. and Hen, R. (2007). Neuroscience. Is more neurogenesis always better? Science, 315, 336-338 https://doi.org/10.1126/science.1138711
  89. Scott, B.W., Wang, S., Burnham, W.M., De Boni, U. and Wojtowicz, J.M. (1998). Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci. Lett., 248, 73-76 https://doi.org/10.1016/S0304-3940(98)00355-3
  90. Shan, X., Chi, L., Bishop, M., Luo, C., Lien, L., Zhang, Z. and Liu, R. (2006) Enhanced de novo neurogenesis and dopaminergic neurogenesis in the substantia nigra of MPTP-induced Parkinson's disease-like mice. Stem Cells, 24, 1280-1287 https://doi.org/10.1634/stemcells.2005-0487
  91. Smith, P.D., McLean, K.J., Murphy, M.A., Turnley, A.M. and Cook, M.J. (2006). Functional dentate gyrus neurogenesis in a rapid kindling seizure model. Eur. J. Neurosci., 24, 3195-3203 https://doi.org/10.1111/j.1460-9568.2006.05205.x
  92. Spanagel, R. and Weiss, F. (1999). The dopamine hypothesis of reward: past and current status. Trends Neurosci., 22, 521-527 https://doi.org/10.1016/S0166-2236(99)01447-2
  93. Steiner, B., Winter, C., Hosman, K., Siebert, E., Kempermann, G., Petrus, D.S. and Kupsch, A. (2006). Enriched environment induces cellular plasticity in the adult substantia nigra and improves motor behavior function in the 6-OHDA rat model of Parkinson's disease. Exp. Neurol., 199, 291-300 https://doi.org/10.1016/j.expneurol.2005.11.004
  94. Takagi, Y., Nozaki, K., Takahashi, J., Yodoi, J., Ishikawa, M. and Hashimoto, N. (1999). Proliferation of neuronal precursor cells in the dentate gyrus is accelerated after transient forebrain ischemia in mice. Brain Res., 831, 283- 287 https://doi.org/10.1016/S0006-8993(99)01411-0
  95. Takasawa, K., Kitagawa, K., Yagita, Y., Sasaki, T., Tanaka, S., Matsushita, K., Ohstuki, T., Miyata, T., Okano, H., Hori, M. and Matsumoto, M. (2002). Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab., 22, 299- 307 https://doi.org/10.1097/00004647-200203000-00007
  96. Tanaka, R., Yamashiro, K., Mochizuki, H., Cho, N., Onodera, M., Mizuno, Y. and Urabe, T. (2004). Neurogenesis after transient global ischemia in the adult hippocampus visualized by improved retroviral vector. Stroke, 35, 1454-1459 https://doi.org/10.1161/01.STR.0000126480.40967.b3
  97. Tashiro, A., Makino, H. and Gage, F.H. (2007). Experiencespecific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J. Neurosci., 27, 3252-3259 https://doi.org/10.1523/JNEUROSCI.4941-06.2007
  98. Tattersfield, A.S., Croon, R.J., Liu, Y.W., Kells, A.P., Faull, R.L. and Connor, B. (2004). Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neuroscience, 127, 319-332 https://doi.org/10.1016/j.neuroscience.2004.04.061
  99. Teuchert-Noodt, G., Dawirs, R.R. and Hildebrandt, K. (2000). Adult treatment with methamphetamine transiently decreases dentate granule cell proliferation in the gerbil hippocampus. J. Neural. Transm., 107, 133-143 https://doi.org/10.1007/s007020050012
  100. Tureyen, K., Vemuganti, R., Sailor, K.A., Bowen, K.K. and Dempsey, R.J. (2004). Transient focal cerebral ischemiainduced neurogenesis in the dentate gyrus of the adult mouse. J. Neurosurg., 101, 799-805 https://doi.org/10.3171/jns.2004.101.5.0799
  101. van Praag, H., Schinder, A.F., Christie, B.R., Toni, N., Palmer, T.D. and Gage, F.H. (2002). Functional neurogenesis in the adult hippocampus. Nature, 415, 1030-1034 https://doi.org/10.1038/4151030a
  102. Walker, D.W., Barnes, D.E., Zornetzer, S.F., Hunter, B.E. and Kubanis, P. (1980). Neuronal loss in hippocampus induced by prolonged ethanol consumption in rats. Science, 209, 711-713 https://doi.org/10.1126/science.7394532
  103. Walling, H.W., Baldassare, J.J. and Westfall, T.C. (1998). Molecular aspects of Huntington's disease. J. Neurosci. Res., 54, 301-308 https://doi.org/10.1002/(SICI)1097-4547(19981101)54:3<301::AID-JNR1>3.0.CO;2-W
  104. Yamaguchi, M., Suzuki, T., Seki, T., Namba, T., Liu, J., Arai, H., Hori, T. and Shiga, T. (2005). Decreased cell proliferation in the dentate gyrus of rats after repeated administration of cocaine. Synapse, 58, 63-71 https://doi.org/10.1002/syn.20182
  105. Yoshimi, K., Ren, Y.R., Seki, T., Yamada, M., Ooizumi, H., Onodera, M., Saito, Y., Murayama, S., Okano, H., Mizuno, Y. and Mochizuki, H. (2005). Possibility for neurogenesis in substantia nigra of parkinsonian brain. Ann. Neurol., 58, 31-40 https://doi.org/10.1002/ana.20506
  106. Zhang, C., McNeil, E., Dressler, L. and Siman, R. (2007). Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp. Neurol., 204, 77-87 https://doi.org/10.1016/j.expneurol.2006.09.018
  107. Zhang, R.L., Zhang, Z.G., Zhang, L. and Chopp, M. (2001). Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience, 105, 33-41 https://doi.org/10.1016/S0306-4522(01)00117-8
  108. Zhao, M., Momma, S., Delfani, K., Carlen, M., Cassidy, R.M., Johansson, C.B., Brismar, H., Shupliakov, O., Frisen, J. and Janson, A.M. (2003). Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. USA, 100, 7925-7930 https://doi.org/10.1073/pnas.1131955100
  109. Ziabreva, I., Perry, E., Perry, R., Minger, S.L., Ekonomou, A., Przyborski, S. and Ballard, C. (2006). Altered neurogenesis in Alzheimer's disease. J. Psychosom. Res., 61, 311- 316 https://doi.org/10.1016/j.jpsychores.2006.07.017