Decreased neurogenesis after cholinergic forebrain lesion in the adult rat

Journal of Neuroscience Research

Volumn 77, Issue 2, 2004, Pages 155-165

  Cooper Kuhn, Christiana M ^a   Winkler, Jürgen ^a,b   Kuhn, H Georg ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell death; Dentate gyrus; Immunotoxin; Olfactory bulb; Progenitor cells

Indexed keywords

BROXURIDINE; CELL MARKER; IMMUNOTOXIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 1921GG; PROTEIN NEUN; SAPORIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN INJURY; CELL COUNT; CELL LOSS; CELL MATURATION; CELL SURVIVAL; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; FOREBRAIN; GRANULAR CELL; IMMUNOTOXICITY; LATERAL BRAIN VENTRICLE; LEARNING; MALE; MEMORY; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

ACETYLCHOLINE; ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; BASAL NUCLEUS OF MEYNERT; BRAIN INJURIES; CELL DIFFERENTIATION; CELL DIVISION; CHOLINERGIC FIBERS; COGNITION DISORDERS; DENTATE GYRUS; DOWN-REGULATION; IMMUNOTOXINS; MALE; N-GLYCOSYL HYDROLASES; NERVE REGENERATION; NEURAL PATHWAYS; NEURONAL PLASTICITY; OLFACTORY BULB; RATS; RATS, INBRED F344; STEM CELLS;

EID: 3042760266     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20116     Document Type: Article

References (101)

1. Abrous DN, Adriani W, Montaron MF, Aurousseau C, Rougon G, Le Moal M, Piazza PV. 2002. Nicotine self-administration impairs hippocampal plasticity. J Neurosci 22:3656-3662.
2. Altman J. 1969. 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 137:433-457.
3. Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, Ferri P, Sartini S, Del Grande P. 2000. Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett 286:21-24.
4. Banasr M, Hery M, Brezun JM, Daszuta A. 2001. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci 14:1417-1424.
5. Barker JL, Behar T, Li YX, Liu QY, Ma W, Maric D, Maric I, Schaffner AE, Serafini R, Smith SV, Somogyi R, Vautrin JY, Wen XL, Xian H. 1998. GABAergic cells and signals in CNS development. Perspect Dev Neurobiol 5:305-322.
6. Baxter MG, Bucci DJ, Sobel TJ, Williams MJ, Gorman LK, Gallagher M. 1996. Intact spatial learning following lesions of basal forebrain cholinergic neurons. Neuroreport 7:1417-1420.
7. Bedard A, Levesque M, Bernier PJ, Parent A. 2002. The rostral migratory stream in adult squirrel monkeys: contribution of new neurons to the olfactory tubercle and involvement of the antiapoptotic protein Bcl-2. Eur J Neurosci 16:1917-1924.
8. Benraiss A, Chmielnicki E, Lerner K, Roh D, Goldman SA. 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.
9. Berchtold NC, Kesslak JP, Cotman CW. 2002. Hippocampal brain-derived neurotrophic factor gene regulation by exercise and the medial septum. J Neurosci Res 68:511-521.
10. Berger-Sweeney J, Heckers S, Mesulam MM, Wiley RG, Lappi DA, Sharma M. 1994. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J Neurosci 14:4507-4519.
11. Bernabeu R, Sharp FR. 2000. NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab 20:1669-1680.
12. Betarbet R, Zigova T, Bakay RA, Luskin MB. 1996. Dopaminergic and GABAergic interneurons of the olfactory bulb are derived from the neonatal subventricular zone. Int J Dev Neurosci 14:921-930.
13. Biebl M, Cooper CM, Winkler J, Kuhn HG. 2000. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 291:17-20.
14. Brezun JM, Daszuta A. 1999. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 89:999-1002.
15. Brezun JM, Daszuta A. 2000a. Serotonergic reinnervation reverses lesion-induced decreases in PSA-NCAM labeling and proliferation of hippocampal cells in adult rats. Hippocampus 10:37-46.
16. Brezun JM, Daszuta A. 2000b. Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with foetal raphe neurons. Eur J Neurosci 12:391-396.
17. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
18. Calza L, Giardino L, Pozza M, Bettelli C, Micera A, Aloe L. 1998. Proliferation and phenotype regulation in the subventricular zone during experimental allergic encephalomyelitis: in vivo evidence of a role for nerve growth factor. Proc Natl Acad Sci USA 95:3209-3214.
19. Calza L, Giuliani A, Fernandez M, Pirondi S, D'Intino G, Aloe L, Giardino L. 2003. Neural stem cells and cholinergic neurons: regulation by immunolesion and treatment with mitogens, retinoic acid, and nerve growth factor. Proc Natl Acad Sci USA 100:7325-7330.
20. Cameron HA, Hazel TG, McKay RD. 1998. Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36:287-306.
21. Cameron HA, McKay RD. 1999. Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894-897.
22. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
23. Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J. 2002. Functional integration of adult-born neurons. Curr Biol 12:606-608.
24. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM. 2003. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507-518.
25. Carleton A, Rochefort C, Morante-Oria J, Desmaisons D, Vincent JD, Gheusi G, Lledo PM. 2002. Making scents of olfactory neurogenesis. J Physiol Paris 96:115-122.
26. Cooper-Kuhn CM, Vroemen M, Brown J, Ye H, Thompson MA, Winkler J, Kuhn HG. 2002. Impaired adult neurogenesis in mice lacking the transcription factor E2F1. Mol Cell Neurosci 21:312-323.
27. Coronas V, Durand M, Chabot JG, Jourdan F, Quirion R. 2000. Acetylcholine induces neuritic outgrowth in rat primary olfactory bulb cultures. Neuroscience 98:213-219.
28. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, et al. 1994. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
29. Cuello AC, Garofalo L, Maysinger D, Pioro EP, Da Silva AR. 1990. Injury and repair of central cholinergic neurons. Prog Brain Res 84:301-311.
30. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
31. Doty RL. 2001. Olfaction. Annu Rev Psychol 52:423-452.
32. Dunnett SB, Fibiger HC. 1993. Role of forebrain cholinergic systems in learning and memory: relevance to the cognitive deficits of aging and Alzheimer's dementia. Prog Brain Res 98:413-420.
33. Durand M, Coronas V, Jourdan F, Quirion R. 1998. Developmental and aging aspects of the cholinergic innervation of the olfactory bulb. Int J Dev Neurosci 16:777-785.
34. Elaagouby A, Ravel N, Gervais R. 1991. Cholinergic modulation of excitability in the rat olfactory bulb: effect of local application of cholinergic agents on evoked field potentials. Neuroscience 45:653-662.
35. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G. 2003. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 22:373-382.
36. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM. 2000. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci USA 97:1823-1828.
37. Gould E. 1999. Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 21:46S-51S.
38. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999a. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
39. Gould E, Tanapat P, Hastings NB, Shors TJ. 1999b. Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 3:186-192.
40. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ. 1988. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
41. Heckers S, Ohtake T, Wiley RG, Lappi DA, Geula C, Mesulam MM. 1994. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 14:1271-1289.
42. Kasa P, Rakonczay Z, Gulya K. 1997. The cholinergic system in Alzheimer's disease. Prog Neurobiol 52:511-535.
43. Kempermann G. 2002. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22:635-638.
44. Kempermann G, Gast D, Gage FH. 2002. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-143.
45. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
46. Kempermann G, Kuhn HG, Gage FH. 1998. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
47. Kornack DR, Rakic P. 2001. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA 98:4752-4757.
48. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
49. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. 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.
50. Leanza G, Muir J, Nilsson OG, Wiley RG, Dunnett SB, Bjorklund A. 1996a. Selective immunolesioning of the basal forebrain cholinergic system disrupts short-term memory in rats. Eur J Neurosci 8:1535-1544.
51. Leanza G, Nikkhah G, Nilsson OG, Wiley RG, Bjorklund A. 1996b. Extensive reinnervation of the hippocampus by embryonic basal forebrain cholinergic neurons grafted into the septum of neonatal rats with selective cholinergic lesions. J Comp Neurol 373:355-357.
52. Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR. 2001. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107:603-613.
53. Linnarsson S, Willson CA, Emfors P. 2000. Cell death in regenerating populations of neurons in BDNF mutant mice. Brain Res Mol Brain Res 75:61-69.
54. Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
55. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
56. Ma W, Maric D, Li BS, Hu Q, Andreadis JD, Grant GM, Liu QY, Shaffer KM, Chang YH, Zhang L, Pancrazio JJ, Pant HC, Stenger DA, Barker JL. 2000. Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur J Neurosci 12:1227-1240.
57. Mattsson A, Ogren SO, Olson L. 2002. Facilitation of dopamine-mediated locomotor activity in adult rats following cholinergic denervation. Exp Neurol 174:96-108.
58. McGaughy J, Kaiser T, Sarter M. 1996. Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci 110:247-265.
59. Mesulam MM, Mufson EJ, Wainer BH, Levey AI. 1983. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
60. Miranda-Contreras L, Benitez-Diaz PR, Mendoza-Briceno RV, Delgado-Saez MC, Palacios-Pru EL. 1999. Levels of amino acid neurotransmitters during mouse cerebellar neurogenesis and in histotypic cerebellar cultures. Dev Neurosci 21:147-158.
61. Miranda-Contreras L, Ramirez-Martens LM, Benitez-Diaz PR, Pena-Contreras ZC, Mendoza-Briceno RV, Palacios-Pru EL. 2000. Levels of amino acid neurotransmitters during mouse olfactory bulb neurogenesis and in histotypic olfactory bulb cultures. Int J Dev Neurosci 18:83-91.
62. Mount HT, Dreyfus CF, Black IB. 1994. Muscarinic stimulation promotes cultured Purkinje cell survival: a role for acetylcholine in cerebellar development? J Neurochem 63:2065-2073.
63. Muir JL. 1997. Acetylcholine, aging, and Alzheimer's disease. Pharmacol Biochem Behav 56:687-696.
64. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
65. Murphy C. 1999. Loss of olfactory function in dementing disease. Physiol Behav 66:177-182.
66. Nguyen L, Rigo JM, Rocher V, Belachew S, Malgrange B, Rogister B, Leprince P, Moonen G. 2001. Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 305:187-202.
67. Nordin S, Murphy C. 1998. Odor memory in normal aging and Alzheimer's disease. Ann N Y Acad Sci 855:686-693.
68. Palmer TD, Takahashi J, Gage FH. 1997. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8:389-404.
69. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
70. Pencea V, Bingaman KD, Freedman LJ, Luskin MB. 2001a. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1-16.
71. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB. 2001b. 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.
72. Petreanu L, Alvarez-Buylla A. 2002. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106-6113.
73. Pizzo DP, Thal LJ, Winkler J. 2002. Mnemonic deficits in animals depend upon the degree of cholinergic deficit and task complexity. Exp Neurol 177:292-305.
74. Pizzo DP, Waite JJ, Thal LJ, Winkler J. 1999. Intraparenchymal infusions of 192 IgG-saporin: development of a method for selective and discrete lesioning of cholinergic basal forebrain nuclei. J Neurosci Methods 91: 9-19.
75. Ravel N, Elaagouby A, Gervais R. 1994. Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats. Behav Neurosci 108:317-324.
76. Ravel N, Vigouroux M, Elaagouby A, Gervais R. 1992. Scopolamine impairs delayed matching in an olfactory task in rats. Psychopharmacology (Berl) 109:439-443.
77. Rawlins JN, Olton DS. 1982. The septo-hippocampal system and cognitive mapping. Behav Brain Res 5:331-358.
78. Rochefort C, Gheusi G, Vincent JD, Lledo PM. 2002. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679-2689.
79. Rossner S, Schliebs R, Hartig W, Bigl V. 1995a. 192IGG-saporin-induced selective lesion of cholinergic basal forebrain system: neurochemical effects on cholinergic neurotransmission in rat cerebral cortex and hippocampus. Brain Res Bull 38:371-381.
80. Rossner S, Schliebs R, Perez-Polo JR, Wiley RG, Bigl V. 1995b. Differential changes in cholinergic markers from selected brain regions after specific immunolesion of the rat cholinergic basal forebrain system. J Neurosci Res 40:31-43.
81. Schiffman SS. 1997. Taste and smell losses in normal aging and disease. JAMA 278:1357-1362.
82. Seki T, Arai Y. 1995. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6:2479-2482.
83. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
84. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S. 2003. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117-120.
85. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
86. Squire LR, Davis HP. 1981. The pharmacology of memory: a neurobiological perspective. Annu Rev Pharmacol Toxicol 21:323-356.
87. Torres EM, Perry TA, Blockland A, Wilkinson LS, Wiley RG, Lappi DA, Dunnet SB. 1994. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63:95-122.
88. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
89. Waite JJ, Wardlow ML, Chen AC, Lappi DA, Wiley RG, Thal LJ. 1994. Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin. Neurosci Lett 169:154-158.
90. Walsh TJ, Kelly RM, Dougherty KD, Stackman RW, Wiley RG, Kutscher CL. 1995. Behavioral and neurobiological alterations induced by the immunotoxin 192-IgG-saporin: cholinergic and non-cholinergic effects following i.c.v. injection. Brain Res 702:233-245.
91. Wenk GL, Stoehr JD, Quintana G, Mobley S, Wiley RG. 1994. Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J Neurosci 14: 5986-5995.
92. Wiley RG, Lappi DA. 1994. Suicide Transport and Immunolesion. Austin, TX.
93. Wiley RG, Oeltmann TN, Lappi DA. 1991. Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res 562:149-153.
94. Williams RW, Rakic P. 1988. Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J Comp Neurol 278:344-352.
95. Winkler J, Suhr ST, Gage FH, Thal LJ, Fisher LJ. 1995. Essential role of neocortical acetylcholine in spatial memory. Nature 375:484-487.
96. Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG. 2002. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16:1681-1689.
97. Wrenn CC, Wiley RG. 1998. The behavioral functions of the cholinergic basal forebrain: lessons from 192 IgG-saporin. Int J Dev Neurosci 16: 595-602.
98. Yan GM, Lin SZ, Irwin RP, Paul SM. 1995. Activation of muscarinic cholinergic receptors blocks apoptosis of cultured cerebellar granule neurons. Mol Pharmacol 47:248-257.
99. Zaborszky L, Carlsen J, Brashear HR, Heimer L. 1986. Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J Comp Neurol 243:488-509.
100. Zheng JQ, Felder M, Connor JA, Poo MM. 1994. Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
101. Zigova T, Pencea V, Wiegand SJ, Luskin MB. 1998. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11:234-245.