From progenitors to integrated neurons: Role of neurotransmitters in adult olfactory neurogenesis

Journal of Chemical Neuroanatomy

Volumn 42, Issue 4, 2011, Pages 304-316

  Bovetti, Serena ^a   Gribaudo, Simona ^a   Puche, Adam C ^b   De Marchis, Silvia ^a   Fasolo, Aldo ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Adult neurogenesis; Interneuron; Neurotransmitters

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; DOPAMINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NITRIC OXIDE; NORADRENALIN; SEROTONIN;

AUTONOMIC INNERVATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; DENTATE GYRUS; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; LATERAL BRAIN VENTRICLE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; OLFACTORY BULB; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SENSORIMOTOR INTEGRATION; STEM CELL;

ADULT; ANIMALS; CELL AGING; CELL DIFFERENTIATION; HUMANS; NEUROGENESIS; NEURONS; NEUROTRANSMITTER AGENTS; OLFACTORY BULB; STEM CELLS;

EID: 80555123072     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2011.05.006     Document Type: Review

References (150)

1. Akiba Y., Sasaki H., Huerta P.T., Estevez A.G., Baker H., Cave J.W. gamma-Aminobutyric acid-mediated regulation of the activity-dependent olfactory bulb dopaminergic phenotype. J. Neurosci. Res. 2009, 87:2211-2221.
2. Alonso M., Viollet C., Gabellec M.M., Meas-Yedid V., Olivo-Marin J.C., Lledo P.M. Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci. 2006, 26:10508-10513.
3. Araki K.Y., Sims J.R., Bhide P.G. Dopamine receptor mRNA and protein expression in the mouse corpus striatum and cerebral cortex during pre- and postnatal development. Brain Res. 2007, 1156:31-45.
4. Azmitia E.C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol. 1978, 179:641-667.
5. Baker S.A., Baker K.A., Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur. J. Neurosci. 2004, 20:575-579.
6. Banasr M., Hery M., Printemps R., Daszuta A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 2004, 29:450-460.
7. Bauer S., Moyse E., Jourdan F., Colpaert F., Martel J.C., Marien M. Effects of the alpha 2-adrenoreceptor antagonist dexefaroxan on neurogenesis in the olfactory bulb of the adult rat in vivo: selective protection against neuronal death. Neuroscience 2003, 117:281-291.
8. Behar T.N., Schaffner A.E., Colton C.A., Somogyi R., Olah Z., Lehel C., Barker J.L. GABA-induced chemokinesis and NGF-induced chemotaxis of embryonic spinal cord neurons. J. Neurosci. 1994, 14:29-38.
9. Behar T.N., Scott C.A., Greene C.L., Wen X., Smith S.V., Maric D., Liu Q.Y., Colton C.A., Barker J.L. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J. Neurosci. 1999, 19:4449-4461.
10. Belluzzi O., Benedusi M., Ackman J., LoTurco J.J. Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 2003, 23:10411-10418.
11. Bolteus A.J., Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 2004, 24:7623-7631.
12. Bonnert T.P., McKernan R.M., Farrar S., le B.B., Heavens R.P., Smith D.W., Hewson L., Rigby M.R., Sirinathsinghji D.J., Brown N., Wafford K.A., Whiting P.J. theta, a novel gamma-aminobutyric acid type A receptor subunit. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:9891-9896.
13. Borta A., Hoglinger G.U. Dopamine and adult neurogenesis. J. Neurochem. 2007, 100:587-595.
14. Bovetti S., Bovolin P., Perroteau I., Puche A.C. Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodelling. Eur. J. Neurosci. 2007, 25:2021-2033.
15. Bovetti S., Hsieh Y.C., Bovolin P., Perroteau I., Kazunori T., Puche A.C. Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb. J. Neurosci. 2007, 27:5976-5980.
16. Bovetti S., Peretto P., Fasolo A., De Marchis S. Spatio-temporal specification of olfactory bulb interneurons. J. Mol. Histol. 2007, 38:563-569.
17. Bovetti S., Veyrac A., Peretto P., Fasolo A., De Marchis S. Olfactory enrichment influences adult neurogenesis modulating GAD67 and plasticity-related molecules expression in newborn cells of the olfactory bulb. PLoS ONE 2009, 4:e6359.
18. Brazel C.Y., Nunez J.L., Yang Z., Levison S.W. Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience 2005, 131:55-65.
19. Brennan P., Kaba H., Keverne E.B. Olfactory recognition: a simple memory system. Science 1990, 250:1223-1226.
20. Brezun J.M., Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 1999, 89:999-1002.
21. Castillo P.E., Carleton A., Vincent J.D., Lledo P.M. Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. J. Neurosci. 1999, 19:9180-9191.
22. Changeux J.P., Bertrand D., Corringer P.J., Dehaene S., Edelstein S., Lena C., Le N.N., Marubio L., Picciotto M., Zoli M. Brain nicotinic receptors: structure and regulation, role in learning and reinforcement. Brain Res. Brain Res. Rev. 1998, 26:198-216.
23. Chen J., Zacharek A., Zhang C., Jiang H., Li Y., Roberts C., Lu M., Kapke A., Chopp M. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J. Neurosci. 2005, 25:2366-2375.
24. Cheng A., Wang S., Cai J., Rao M.S., Mattson M.P. Nitric oxide acts in a positive feedback loop with BDNF to regulate neural progenitor cell proliferation and differentiation in the mammalian brain. Dev. Biol. 2003, 258:319-333.
25. Clarke P.B. Nicotine dependence - mechanisms and therapeutic strategies. Biochem. Soc. Symp. 1993, 59:83-95.
26. Cooper-Kuhn C.M., Winkler J., Kuhn H.G. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J. Neurosci. Res. 2004, 77:155-165.
27. Coronas V., Bantubungi K., Fombonne J., Krantic S., Schiffmann S.N., Roger M. Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post-natal subventricular zone. J. Neurochem. 2004, 91:1292-1301.
28. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., van der K.D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 1996, 16:2649-2658.
29. Cui X., Chen J., Zacharek A., Roberts C., Yang Y., Chopp M. Nitric oxide donor up-regulation of SDF1/CXCR4 and Ang1/Tie2 promotes neuroblast cell migration after stroke. J. Neurosci. Res. 2009, 87:86-95.
30. D'Hulst C., Atack J.R., Kooy R.F. The complexity of the GABAA receptor shapes unique pharmacological profiles. Drug Discov. Today 2009, 14:866-875.
31. De Marchis S., Fasolo A., Shipley M., Puche A. Unique neuronal tracers show migration and differentiation of SVZ progenitors in organotypic slices. J. Neurobiol. 2001, 49:326-338.
32. De Marchis S., Bovetti S., Carletti B., Hsieh Y.C., Garzotto D., Peretto P., Fasolo A., Puche A.C., Rossi F. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J. Neurosci. 2007, 27:657-664.
33. De Marchis S., Temoney S., Erdelyi F., Bovetti S., Bovolin P., Szabo G., Puche A.C. GABAergic phenotypic differentiation of a subpopulation of subventricular derived migrating progenitors. Eur. J. Neurosci. 2004, 20:1307-1317.
34. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci. 2010, 11:339-350.
35. Di Giorgi Gerevini V., Caruso A., Cappuccio I., Ricci V.L., Romeo S., Della R.C., Gradini R., Melchiorri D., Nicoletti F. The mGlu5 metabotropic glutamate receptor is expressed in zones of active neurogenesis of the embryonic and postnatal brain. Brain Res. Dev. Brain Res. 2004, 150:17-22.
36. Diaz D., Valero J., Airado C., Baltanas F.C., Weruaga E., Alonso J.R. Sexual dimorphic stages affect both proliferation and serotonergic innervation in the adult rostral migratory stream. Exp. Neurol. 2009, 216:357-364.
37. Diaz J., Ridray S., Mignon V., Griffon N., Schwartz J.C., Sokoloff P. Selective expression of dopamine D3 receptor mRNA in proliferative zones during embryonic development of the rat brain. J. Neurosci. 1997, 17:4282-4292.
38. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:11619-11624.
39. Duan W., Peng Q., Masuda N., Ford E., Tryggestad E., Ladenheim B., Zhao M., Cadet J.L., Wong J., Ross C.A. Sertraline slows disease progression and increases neurogenesis in N171-82Q mouse model of Huntington's disease. Neurobiol. Dis. 2008, 30:312-322.
40. Duman R.S. Depression: a case of neuronal life and death?. Biol. Psychiatry 2004, 56:140-145.
41. Ennis M., Hamilton K.A., Hayar A. Neurochemistry of the main olfactory system. Handbook of neurochemistry and molecular neurobiology 2007, Springer, New York, pp. 137-204.
42. Freundlieb N., Francois C., Tande D., Oertel W.H., Hirsch E.C., Hoglinger G.U. Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J. Neurosci. 2006, 26:2321-2325.
43. Gascon E., Dayer A.G., Sauvain M.O., Potter G., Jenny B., De R.M., Zgraggen E., Demaurex N., Muller D., Kiss J.Z. GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J. Neurosci. 2006, 26:12956-12966.
44. Gascon E., Vutskits L., Zhang H., Barral-Moran M.J., Kiss P.J., Mas C., Kiss J.Z. Sequential activation of p75 and TrkB is involved in dendritic development of subventricular zone-derived neuronal progenitors in vitro. Eur. J. Neurosci. 2005, 21:69-80.
45. Ge S., Pradhan D.A., Ming G.L., Song H. GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci. 2007, 30:1-8.
46. Gerzanich V., Anand R., Lindstrom J. Homomers of alpha 8 and alpha 7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties. Mol. Pharmacol. 1994, 45:212-220.
47. Giachino C., De M.S., Giampietro C., Parlato R., Perroteau I., Schutz G., Fasolo A., Peretto P. cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J. Neurosci. 2005, 25:10105-10118.
48. Gribaudo S., Bovetti S., Garzotto D., Fasolo A., De Marchis S. Expression and localization of the calmodulin-binding protein neurogranin in the adult mouse olfactory bulb. J. Comp. Neurol. 2009, 517:683-694.
49. Gutierrez-Mecinas M., Crespo C., Blasco-Ibanez J.M., Nacher J., Varea E., Martinez-Guijarro F.J. Migrating neuroblasts of the rostral migratory stream are putative targets for the action of nitric oxide. Eur. J. Neurosci. 2007, 26:392-402.
50. Harley C.W., rby-King A., McCann J., McLean J.H. Beta1-adrenoceptor or alpha1-adrenoceptor activation initiates early odor preference learning in rat pups: support for the mitral cell/cAMP model of odor preference learning. Learn. Mem. 2006, 13:8-13.
51. Hevers W., Luddens H. The diversity of GABAA receptors, Pharmacological and electrophysiological properties of GABAA channel subtypes. Mol. Neurobiol. 1998, 18:35-86.
52. Hitoshi S., Maruta N., Higashi M., Kumar A., Kato N., Ikenaka K. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J. Neurosci. Res. 2007, 85:3574-3585.
53. Hoglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004, 7:726-735.
54. Inta D., Alfonso J., von E.J., Kreuzberg M.M., Meyer A.H., van Hooft J.A., Monyer H. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:20994-20999.
55. Jagasia R., Steib K., Englberger E., Herold S., Faus-Kessler T., Saxe M., Gage F.H., Song H., Lie D.C. GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J. Neurosci. 2009, 29:7966-7977.
56. Kaneko N., Okano H., Sawamoto K. Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 2006, 11:1145-1159.
57. Kasa P., Hlavati I., Dobo E., Wolff A., Joo F., Wolff J.R. Synaptic and non-synaptic cholinergic innervation of the various types of neurons in the main olfactory bulb of adult rat: immunocytochemistry of choline acetyltransferase. Neuroscience 1995, 67:667-677.
58. Keilhoff G., Becker A., Grecksch G., Bernstein H.G., Wolf G. Cell proliferation is influenced by bulbectomy and normalized by imipramine treatment in a region-specific manner. Neuropsychopharmacology 2006, 31:1165-1176.
59. Kempermann G. Regulation of adult hippocampal neurogenesis-implications for novel theories of major depression. Bipolar. Disord. 2002, 4:17-33.
60. Kempermann G., Krebs J., Fabel K. The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr. Opin. Psychiatry 2008, 21:290-295.
61. Kim Y., Wang W.Z., Comte I., Pastrana E., Tran P.B., Brown J., Miller R.J., Doetsch F., Molnar Z., Szele F.G. Dopamine stimulation of postnatal murine subventricular zone neurogenesis via the D3 receptor. J. Neurochem. 2010, 114:750-760.
62. Kippin T.E., Kapur S., van der K.D. Dopamine specifically inhibits forebrain neural stem cell proliferation, suggesting a novel effect of antipsychotic drugs. J. Neurosci. 2005, 25:5815-5823.
63. Kiyokage E., Pan Y.Z., Shao Z., Kobayashi K., Szabo G., Yanagawa Y., Obata K., Okano H., Toida K., Puche A.C., Shipley M.T. Molecular identity of periglomerular and short axon cells. J. Neurosci. 2010, 30:1185-1196.
64. Kohwi M., Petryniak M.A., Long J.E., Ekker M., Obata K., Yanagawa Y., Rubenstein J.L., Alvarez-Buylla A. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J. Neurosci. 2007, 27:6878-6891.
65. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 1997, 17:5820-5829.
66. Lazarini F., Lledo P.M. Is adult neurogenesis essential for olfaction?. Trends Neurosci. 2010.
67. Le Jeune H., Aubert I., Jourdan F., Quirion R. Developmental profiles of various cholinergic markers in the rat main olfactory bulb using quantitative autoradiography. J. Comp. Neurol. 1996, 373:433-450.
68. Lin C.W., Sim S., Ainsworth A., Okada M., Kelsch W., Lois C. Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 2010, 65:32-39.
69. Liu X., Wang Q., Haydar T.F., Bordey A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 2005, 8:1179-1187.
70. Lledo P.M., Alonso M., Grubb M.S. Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 2006, 7:179-193.
71. Lledo P.M., Merkle F.T., Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 2008, 31:392-400.
72. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
73. Lois C., Garcia-Verdugo J.M., Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271:978-981.
74. Lonze B.E., Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 2002, 35:605-623.
75. LoTurco J.J., Owens D.F., Heath M.J., Davis M.B., Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995, 15:1287-1298.
76. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
77. Luskin M.B., Boone M.S. Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem. Senses 1994, 19:695-714.
78. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000, 20:9104-9110.
79. Mandairon N., Peace S., Karnow A., Kim J., Ennis M., Linster C. Noradrenergic modulation in the olfactory bulb influences spontaneous and reward-motivated discrimination, but not the formation of habituation memory. Eur. J. Neurosci. 2008, 27:1210-1219.
80. Mandairon N., Sacquet J., Jourdan F., Didier A. Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience 2006, 141:443-451.
81. Matarredona E.R., Murillo-Carretero M., Moreno-Lopez B., Estrada C. Nitric oxide synthesis inhibition increases proliferation of neural precursors isolated from the postnatal mouse subventricular zone. Brain Res. 2004, 995:274-284.
82. Matsutani S., Yamamoto N. Centrifugal innervation of the mammalian olfactory bulb. Anat. Sci. Int. 2008, 83:218-227.
83. McLean J.H., rby-King A., Sullivan R.M., King S.R. Serotonergic influence on olfactory learning in the neonate rat. Behav. Neural Biol. 1993, 60:152-162.
84. McLean J.H., Shipley M.T. Serotonergic afferents to the rat olfactory bulb: I. Origins and laminar specificity of serotonergic inputs in the adult rat. J. Neurosci. 1987, 7:3016-3028.
85. McLean J.H., Shipley M.T., Nickell W.T., ston-Jones G., Reyher C.K. Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J. Comp. Neurol. 1989, 285:339-349.
86. Mechawar N., Saghatelyan A., Grailhe R., Scoriels L., Gheusi G., Gabellec M.M., Lledo P.M., Changeux J.P. Nicotinic receptors regulate the survival of newborn neurons in the adult olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9822-9826.
87. Mejia-Gervacio S., Murray K., Lledo P.M. NKCC1 controls GABAergic signaling and neuroblast migration in the postnatal forebrain. Neural Dev. 2011, 6:4.
88. Merkle F.T., Mirzadeh Z., Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science 2007, 317:381-384.
89. Merlo S., Canonico P.L., Sortino M.A. Distinct effects of pramipexole on the proliferation of adult mouse sub-ventricular zone-derived cells and the appearance of a neuronal phenotype. Neuropharmacology 2011, 60:892-900.
90. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 2005, 28:223-250.
91. Misgeld U., Deisz R.A., Dodt H.U., Lux H.D. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 1986, 232:1413-1415.
92. Moreno-Lopez B., Noval J.A., Gonzalez-Bonet L.G., Estrada C. Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res. 2000, 869:244-250.
93. Moreno-Lopez B., Romero-Grimaldi C., Noval J.A., Murillo-Carretero M., Matarredona E.R., Estrada C. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci. 2004, 24:85-95.
94. Moriizumi T., Tsukatani T., Sakashita H., Miwa T. Olfactory disturbance induced by deafferentation of serotonergic fibers in the olfactory bulb. Neuroscience 1994, 61:733-738.
95. Mueller A.L., Taube J.S., Schwartzkroin P.A. Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J. Neurosci. 1984, 4:860-867.
96. Murillo-Carretero M., Torroglosa A., Castro C., Villalobo A., Estrada C. S-Nitrosylation of the epidermal growth factor receptor: a regulatory mechanism of receptor tyrosine kinase activity. Free Radic. Biol. Med. 2009, 46:471-479.
97. Nguyen L., Malgrange B., Breuskin I., Bettendorff L., Moonen G., Belachew S., Rigo J.M. Autocrine/paracrine activation of the GABAA receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive PSA-NCAM+ precursor cells from postnatal striatum. J. Neurosci. 2003, 23:3278-3294.
98. Nicholas A.P., Pieribone V.A., Hokfelt T. Cellular localization of messenger RNA for beta-1 and beta-2 adrenergic receptors in rat brain: an in situ hybridization study. Neuroscience 1993, 56:1023-1039.
99. Nickell W.T., Shipley M.T. Frequency potentiation of a central cholinergic circuit. J. Neural Transm. Suppl. 1987, 24:153-160.
100. O'Keeffe G.C., Tyers P., Aarsland D., Dalley J.W., Barker R.A., Caldwell M.A. Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8754-8759.
101. Oboti L., Savalli G., Giachino C., De Marchis S., Panzica G.C., Fasolo A., Peretto P. Integration and sensory experience-dependent survival of newly-generated neurons in the accessory olfactory bulb of female mice. Eur. J. Neurosci. 2009, 29:679-692.
102. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat. Rev. Neurosci. 2002, 3:715-727.
103. Packer M.A., Stasiv Y., Benraiss A., Chmielnicki E., Grinberg A., Westphal H., Goldman S.A., Enikolopov G. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:9566-9571.
104. Parrish-Aungst S., Shipley M.T., Erdelyi F., Szabo G., Puche A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 2007, 501:825-836.
105. Pathania M., Yan L.D., Bordey A. A symphony of signals conducts early and late stages of adult neurogenesis. Neuropharmacology 2010, 58:865-876.
106. Pauwels P.J. Diverse signalling by 5-hydroxytryptamine 5-HT receptors. Biochem. Pharmacol. 2000, 60:1743-1750.
107. Peretto P., Giachino C., Aimar P., Fasolo A., Bonfanti L. Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J. Comp. Neurol. 2005, 487:407-427.
108. Peretto P., Giachino C., Panzica G.C., Fasolo A. Sexually dimorphic neurogenesis is topographically matched with the anterior accessory olfactory bulb of the adult rat. Cell Tissue Res. 2001, 306:385-389.
109. Peretto P., Merighi A., Fasolo A., Bonfanti L. Glial tubes in the rostral migratory stream of the adult rat. Brain Res. Bull. 1997, 42:9-21.
110. Peretto P., Merighi A., Fasolo A., Bonfanti L. The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain. Brain Res. Bull. 1999, 49:221-243.
111. Petreanu L., Alvarez-Buylla A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 2002, 22:6106-6113.
112. Petzold G.C., Hagiwara A., Murthy V.N. Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat. Neurosci. 2009, 12:784-791.
113. Platel J.C., Dave K.A., Bordey A. Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J. Physiol. 2008, 586:3739-3743.
114. Platel J.C., Dave K.A., Gordon V., Lacar B., Rubio M.E., Bordey A. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 2010, 65:859-872.
115. Platel J.C., Heintz T., Young S., Gordon V., Bordey A. Tonic activation of GLUK5 kainate receptors decreases neuroblast migration in whole-mounts of the subventricular zone. J. Physiol. 2008, 586:3783-3793.
116. Platel J.C., Lacar B., Bordey A. GABA and glutamate signaling: homeostatic control of adult forebrain neurogenesis. J. Mol. Histol. 2007, 38:303-311.
117. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 2002, 22:2679-2689.
118. Romero-Grimaldi C., Gheusi G., Lledo P.M., Estrada C. Chronic inhibition of nitric oxide synthesis enhances both subventricular zone neurogenesis and olfactory learning in adult mice. Eur. J. Neurosci. 2006, 24:2461-2470.
119. Romero-Grimaldi C., Moreno-Lopez B., Estrada C. Age-dependent effect of nitric oxide on subventricular zone and olfactory bulb neural precursor proliferation. J. Comp. Neurol. 2008, 506:339-346.
120. Rosser A.E., Keverne E.B. The importance of central noradrenergic neurones in the formation of an olfactory memory in the prevention of pregnancy block. Neuroscience 1985, 15:1141-1147.
121. Saghatelyan A., de C.A., Schachner M., Lledo P.M. Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat. Neurosci. 2004, 7:347-356.
122. Saghatelyan A., Roux P., Migliore M., Rochefort C., Desmaisons D., Charneau P., Shepherd G.M., Lledo P.M. Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 2005, 46:103-116.
123. Shibui Y., He X.J., Uchida K., Nakayama H. MPTP-induced neuroblast apoptosis in the subventricular zone is not regulated by dopamine or other monoamine transporters. Neurotoxicology 2009, 30:1036-1044.
124. Shipley M.T., Halloran F.J., de la T.J. Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat. Brain Res. 1985, 329:294-299.
125. Sinkkonen S.T., Hanna M.C., Kirkness E.F., Korpi E.R. GABAA receptor epsilon and theta subunits display unusual structural variation between species and are enriched in the rat locus ceruleus. J. Neurosci. 2000, 20:3588-3595.
126. Snapyan M., Lemasson M., Brill M.S., Blais M., Massouh M., Ninkovic J., Gravel C., Berthod F., Gotz M., Barker P.A., Parent A., Saghatelyan A. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J. Neurosci. 2009, 29:4172-4188.
127. Stewart R.R., Hoge G.J., Zigova T., Luskin M.B. Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABAA receptors. J. Neurobiol. 2002, 50:305-322.
128. Sullivan R.M., Zyzak D.R., Skierkowski P., Wilson D.A. The role of olfactory bulb norepinephrine in early olfactory learning. Brain Res. Dev. Brain Res. 1992, 70:279-282.
129. Sun Y., Jin K., Childs J.T., Xie L., Mao X.O., Greenberg D.A. Neuronal nitric oxide synthase and ischemia-induced neurogenesis. J. Cereb. Blood Flow Metab. 2005, 25:485-492.
130. Taupin P. Adult neurogenesis in mammals. Curr. Opin. Mol. Ther. 2006, 8:345-351.
131. Thakker-Varia S., Krol J.J., Nettleton J., Bilimoria P.M., Bangasser D.A., Shors T.J., Black I.B., Alder J. The neuropeptide VGF produces antidepressant-like behavioral effects and enhances proliferation in the hippocampus. J. Neurosci. 2007, 27:12156-12167.
132. Van Kampen J.M., Hagg T., Robertson H.A. Induction of neurogenesis in the adult rat subventricular zone and neostriatum following dopamine D3 receptor stimulation. Eur. J. Neurosci. 2004, 19:2377-2387.
133. Vandenbosch R., Borgs L., Beukelaers P., Belachew S., Moonen G., Nguyen L., Malgrange B. Adult neurogenesis and the diseased brain. Curr. Med. Chem. 2009, 16:652-666.
134. Veyrac A., Didier A., Colpaert F., Jourdan F., Marien M. Activation of noradrenergic transmission by alpha2-adrenoceptor antagonists counteracts deafferentation-induced neuronal death and cell proliferation in the adult mouse olfactory bulb. Exp. Neurol. 2005, 194:444-456.
135. Veyrac A., Sacquet J., Nguyen V., Marien M., Jourdan F., Didier A. Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 2009, 34:786-795.
136. Wang D.D., Krueger D.D., Bordey A. Biophysical properties and ionic signature of neuronal progenitors of the postnatal subventricular zone in situ. J. Neurophysiol. 2003, 90:2291-2302.
137. Wang D.D., Krueger D.D., Bordey A. GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J. Physiol. 2003, 550:785-800.
138. Whiting P.J., Bonnert T.P., McKernan R.M., Farrar S., le B.B., Heavens R.P., Smith D.W., Hewson L., Rigby M.R., Sirinathsinghji D.J., Thompson S.A., Wafford K.A. Molecular and functional diversity of the expanding GABA-A receptor gene family. Ann. N. Y. Acad. Sci. 1999, 868:645-653.
139. Whitman M.C., Greer C.A. Adult-generated neurons exhibit diverse developmental fates. Dev. Neurobiol. 2007, 67:1079-1093.
140. Whitman M.C., Greer C.A. Adult neurogenesis and the olfactory system. Prog. Neurobiol. 2009, 89:162-175.
141. Winner B., Desplats P., Hagl C., Klucken J., Aigner R., Ploetz S., Laemke J., Karl A., Aigner L., Masliah E., Buerger E., Winkler J. Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Exp. Neurol. 2009, 219:543-552.
142. Winner B., Geyer M., Couillard-Despres S., Aigner R., Bogdahn U., Aigner L., Kuhn G., Winkler J. Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Exp. Neurol. 2006, 197:113-121.
143. Wright D.E., Seroogy K.B., Lundgren K.H., Davis B.M., Jennes L. Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain. J. Comp. Neurol. 1995, 351:357-373.
144. Yamada J., Okabe A., Toyoda H., Kilb W., Luhmann H.J., Fukuda A. Cl-uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 2004, 557:829-841.
145. Yamaguchi M., Mori K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9697-9702.
146. Yang P., Arnold S.A., Habas A., Hetman M., Hagg T. Ciliary neurotrophic factor mediates dopamine D2 receptor-induced CNS neurogenesis in adult mice. J. Neurosci. 2008, 28:2231-2241.
147. Young S.Z., Platel J.C., Nielsen J.V., Jensen N.A., Bordey A. GABAA increases calcium in subventricular zone astrocyte-like cells through L- and T-type voltage-gated calcium channels. Front. Cell. Neurosci. 2010, 4:8.
148. Zhang Z.W., Vijayaraghavan S., Berg D.K. Neuronal acetylcholine receptors that bind alpha-bungarotoxin with high affinity function as ligand-gated ion channels. Neuron 1994, 12:167-177.
149. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
150. Zhao N., Zhong C., Wang Y., Zhao Y., Gong N., Zhou G., Xu T., Hong Z. Impaired hippocampal neurogenesis is involved in cognitive dysfunction induced by thiamine deficiency at early pre-pathological lesion stage. Neurobiol. Dis. 2008, 29:176-185.