Adult-born neurons in the olfactory bulb: Integration and functional consequences

Current Topics in Behavioral Neurosciences

Volumn 15, Issue , 2012, Pages 49-72

  Gheusi, Gilles ^a,b   Lepousez, Gabriel ^a   Lledo, Pierre Marie ^a  

^a CNRS   (France)

^b UNIVERSITÉ PARIS 13   (France)

Author keywords

Adult neurogenesis; Behavior; Brain plasticity; Learning; Memory; Neural stem cells; Olfaction

Indexed keywords

PROTEIN BAX; PROTEIN BCL 2; RHODOPSIN;

ARTICLE; CELL MATURATION; CELL PROLIFERATION; HUMAN; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY EPITHELIUM; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; SENSORIMOTOR INTEGRATION; SENSORY STIMULATION; SHORT TERM MEMORY; SUBVENTRICULAR ZONE; TASK PERFORMANCE; TIME LAPSE IMAGING; ADULT STEM CELL; ANIMAL; CYTOLOGY; NERVE CELL; PHYSIOLOGY; REVIEW;

ADULT STEM CELLS; ANIMALS; HUMANS; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; OLFACTORY BULB;

EID: 84891688221     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2012_228     Document Type: Article

References (128)

1. Alonso M, Viollet C, Gabellec MM, Meas-Yedid V, Olivo-Marin JC, Lledo PM (2006) Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci 26: 10508-10513
2. Alonso M, Lepousez G, Wagner S, Bardy C, Gabellec MM, Torquet N, Lledo PM (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15: 897-904
3. Altman J (1962) Are neurons formed in the brains of adult mammals? Science 135: 1127-1128
4. Altman J, Das GD (1965) Autoradiographic and histological studies of postnatal hippocampus neurogenesis in rats. J Comp Neurol 124: 319-333
5. Amrein I, Isler K, Lipp HP (2011) Comparing adult hippocampal neurogenesis in mammalian species and orders: Influence of chronological age and life history stage. Eur J Neurosci 34: 978-987
6. Baker JM, Boonstra R, Wotjtowicz JM (2011) From pattern to purpose: How comparative studies contribute to understanding the function of adult neurogenesis. Eur J Neurosci 34: 963-977
7. Balu R, Pressler RT, Strowbridge BW (2007) Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci 27: 5621-5632
8. Bardy C, Alonso M, Bouthour W, Lledo PM (2010) How, when and where new inhibitory neurons release neurotransmitters in the adult olfactory bulb. J Neurosci 30: 17023-17034
9. Bath KG, Mandairon N, Jing D, Rajagopal R, Kapoor R, Chen ZY, Khan T, Proenca CC, Kraemer R, Cleland TA, Hempstead BL, Chao MV, Lee FS (2008) Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J Neurosci 28: 2383-2393
10. Bauer S, Moyse E, Jourdan F, Colpaert F, Martel JC, Marien M (2003) 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 117: 281-291
11. Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151: 159-168
12. Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MSY, Steier P, Kutschera W, Johnson L, Landén M, Druid H, Spalding KL, Frisén J (2012) The age of olfactory bulb neurons in humans. Neuron 74: 634-639
13. Bernier PJ, Vinet J, Cossette M, Parent A (2000) Characterization of the subventricular zone of the adult human brain: Evidence for the involvement of Bcl-2. Neurosci Res 37: 67-78
14. 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
15. Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals-a theme with many variations. Eur J Neurosci 34: 930-950
16. Bovetti S, Gribaudo S, Puche AC, De Marchis S, Fasolo A (2011) From progenitors to integrated neurons: Role of neurotransmitters in adult neurogenesis. J Chem Neuroanat 42: 304-316
17. Bovetti S, Hsieh YC, Bovolin P, Perroteau I, Kazunori T, Puche AC (2007) Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb. J Neurosci 27: 5976-5980
18. Bovetti S, Veyrac A, Peretto P, Fasolo A, De Marchis S (2009) Olfactory enrichment influences adult neurogenesis modulating GAD67 and plasticity-related molecules expression in newborn cells of the olfactory bulb. PLoS One 4: E6359
19. Brennan PA, Schellinck HM, de la Riva C, Kendrick KM, Keverne EB (1998) Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure in mice. Neuroscience 87: 583-590
20. Breton-Provencher V, Lemasson M, Peralta MR III, Seghatelyan A (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29: 15245-15257
21. Bruce HM (1959) An exteroceptive block to pregnancy in the mouse. Nature 184: 105
22. Brus M, Meurisse M, Franceschini I, Keller M, Lévy F (2010) Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm Behav 58: 737-746
23. Brus M, Meurisse M, Gheusi G, Keller M, Lledo PM, Lévy F (2012) Dynamics of olfactory and hippocampal neurogenesis in adult sheep. J Comp Neurol (in press). doi: 10. 1002/cne. 23169
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. Coderre JA, Morris GM, Micca PL, Hopewell JW, Verhagen I, Kleiboer BJ, van der Kogel AJ (2006) Late effects of radiation on the central nervous system: Role of vascular endothelial damage and glial stem cell survival. Radiat Res 166: 495-503
26. Corotto FS, Henegar JR, Maruniak JA (1994) Odor deprivation leads to reduced neurogenesis and reduced survival in the olfactory bulb of the adult mouse. Neuroscience 61: 739-744
27. Doetsch F, Caillé I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716
28. Enewere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis and deficits in fine olfactory discrimination. J Neurosci 24: 8354-8365
29. Eyre MD, Antal M, Nusser Z (2008) Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J Neurosci 28: 8217-8229
30. Fereistein CE, Lazarini F, Wagner S, Gabellec MM, de Chaumont F, Olivo-Marin JC, Boussin FD, Lledo PM, Gheusi G (2010) Disruption of adult neurogenesis in the olfactory bulb affects social interaction but not maternal behavior. Front Behav Neurosci 4: 176
31. Firestein S (2001) How the olfactory system makes sense of scents. Nature 413: 211-218
32. Freundlieb N, François C, Tandé D, Oertel WH, Hirsch EC, Höglinger GU (2006) Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci 22: 2321-2325
33. Friedman D, Strowbridge BW (2003) Both electrical and chemical synapses mediate fast network oscillations in the olfactory bulb. J Neurophysiol 89: 2601-2610
34. Futura M, Bridges RS (2005) Gestation-induced cell proliferation in the rat brain. Dev Brain Res 156: 61-66
35. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7: 1233-1241
36. Geffen MN, Broome BM, Laurent G, Mesiter M (2009) Neural encoding of rapidly fluctuating odors. Neuron 61: 570-586
37. 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 U S A 97: 1823-1828
38. Gheusi G, Ortega-Perez I, Murray K, Lledo PM (2009) A niche for adult neurogenesis in social behavior. Behav Brain Res 200: 315-322
39. Gilbert CD, Sigman M, Crist RE (2001) The neural basis of perceptual learning. Neuron 31: 681-697
40. Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1: 67-73
41. Gross CG (2009) Three before their time: neuroscientists whose ideas were ignored by their contemporaries. Exp Brain Res 192: 321-324
42. Huang L, Bittman EL (2002) Olfactory bub cells generated in adut male golden hamsters are specifically activated by exposure to estrous females. Horm Behav 41: 34-350
43. Imayoshi I, Sajkamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11: 1153-1161
44. Katagiri H, Pallotto M, Nissant A, Murray K, Sassoe-Pognetto M, Lledo PM (2011) Dynamic development of the first synapse umpinging on adult-born olfactory neurons. Neural Syst Circuits 1: 6. doi: 10. 1186/2042-1001-1-6
45. Kelsch W, Lin CW, Lois C (2008) Sequential development of synapses in dendritic domains during adult neurogenesis. Proc Natl Acad Sci U S A 105: 16803-16808
46. Kelsch W, Lin CW, Mosley CP, Lois C (2009) A critical period for activity-dependent synaptic development during olfactory bulb adult neurogenesis. J Neurosci 29: 11852-11858
47. Kelsch W, Sim S, Lois C (2012) Increasing heterogeneity in the organization of synaptic inputs of mature olfactory bulb neurons generated in newborn rats. J Comp Neurol 6: 1327-1338
48. Kermen F, Sultan S, Sacquet J, Mandairon N, Didier A (2010) Consolidation of an olfactory memory trace in the olfactory bulb is required for learning-induced survival of adult-born neurons and long-term memory. PLoS ONE 5: E1218
49. Kim WR, Kim Y, Eun B, Park OH, Kim H, Kim K, Park CH, Vinsant S, Oppenheim RW, Sun W (2007) Impaired migration in the rostral migratory stream but spared olfactory function after the elimination of programmed cell death in Bax knock-out mice. J Neurosci 27: 14392-14403
50. Kornack DR, Rakic P (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294: 2127-2130
51. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32: 149-184
52. Larsen CM, Grattan DR (2012) Prolactin, neurogenesis and maternal behaviors. Brain Behav Immun 26: 201-209
53. Larsen CM, Kokay IC, Grattan DR (2008) Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Horm Behav 53: 509-517
54. Larsen CM, Grattan DR, Gerald L (2010) Exposure to female pheromones during pregnancy causes postpartum anxiety in mice. Vitam Horm 83: 137-149
55. Lazarini F, Mouthon MA, Gheusi G, de Chaumont F, Olivo-Marin JC, Lamarque S, Abrous DN, Boussin FD, Lledo PM (2009) Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One 4: E7017
56. Lemaire V, Tronel S, Montaron MF, Fabre A, Dugats E, Abrous DN (2012) Long-lasting plasticity of hippocampal adult-born neurons. J Neurosci 32: 3101-3108
57. Lemasson M, Saghatelyan M, Olivo-Marin JC, Lledo PM (2005) Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J Neurosci 25: 6816-6825
58. Leuner B, Glasper ER, Gould E (2010) Parenting plasticity. Trends Neurosci 33: 465-473
59. Lévy F, Gervais R, Kindermann U, Orgeur P, Piketty V (1990) Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav Neurosci 104: 464-469
60. Lévy F, Gheusi G, Keller M (2011) Plasticity of the parental brain: A case of neurogenesis. J Neuroendocrinol 23: 984-993
61. Lin CW, Sim S, Ainsworth A, Okada M, Kelsch W, Lois C (2010) Genetically increased cellinstrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 65: 32-39
62. Liu Z, Martin LJ (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
63. Livneh Y, Mizrahi A (2011) Experience-dependent plasticity of mature adult-born neurons. Nat Neurosci 15: 26-28
64. Livneh Y, Feinstein N, Klein M, Mizrahi A (2009) Sensory input enhances synaptogenesis of adult-born neurons. J Neurosci 29: 86-97
65. Lledo PM, Alonso M, Grubb M (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Neurosci Rev 7: 179-193
66. Lloyd-Thomas A, Keverne EB (1982) Role of the brain and accessory olfactory system in the block to pregnancy in mice. Neuroscience 7: 907-913
67. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148
68. Mak GK, Weiss S (2010) Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci 13: 753-758
69. Mak G, Enewere EK, Gregg C, Pakarainen T, Poutanen M, Huhtaniemi I, Weiss S (2007) Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci 10: 1003-1011
70. Mandairon N, Sacquet J, Garcia S, Ravel N, Jourdan F, Didier A (2006) Neurogenic correlates of an olfactory discrimination task in the adult olfactory bulb. Eur J Neurosci 24: 3578-3588
71. Maresh A, Rodriguez Gil D, Whitman MC, Greer CA (2008) Principles of glomeruar organization in the human olfactory bulb-implications for odor processing. PLoS One 3: E2640
72. McGinn MJ, Sun D, Colello RJ (2008) Utilizing X-irradiation to selectively eliminate neural stem/progenitor cells from neurogenic regions of the mammalian brain. J Neurosci Methods 170: 9-15
73. Mignone JL, Kukekov V, Chaing AS, Steindler D, Enikolopov G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469: 311-324
74. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250
75. Miwa N, Storm DR (2005) Odorant-induced activation of extracellular signal-regulated kinase/mitogen-activated protein kinase in the olfactory bulb promotes survival of newly formed granule cells. J Neurosci 25: 5404-5413
76. Mizrahi A (2007) Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10: 444-452
77. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8: 955-962
78. Moreno MM, Linster C, Escanilla O, Sacquet J, Didier A, Mandairon N (2009) Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci USA 106: 17980-17985
79. Moreno MM, Bath K, Kuczewski N, Sacquet J, Didier A, Mandairon N (2012) Action of noradrenergic system on adult-born cells is required for olfactory learning in mice. J Neurosci 32: 3748-3758
80. Mouret A, Gheusi G, Gabellec MM, de Chaumont F, Olivo-Marin JC, Lledo PM (2008) Learning and survival of newly generated neurons: when time matters. J Neurosci 28: 11511-11516
81. Mouret A, Lepousez G, Gras J, Gabellec MM, Lledo PM (2009) Turnover of newborn olfactory bulb neurons optimizes olfaction. J Neurosci 29: 12302-12314
82. Nicholas AP, Pieribone VA, Hokfelt T (1993) Cellular localization of messenger RNA for beta-1 and beta-2 adrenergic receptors in rat brain: An in situ hybridization study. Neuroscience 56: 1023-1039
83. Nissant A, Bardy C, Katagiri H, Murray K, Lledo PM (2009) Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12: 728-730
84. Nunez-Parra A, Pugh V, Araneda RC (2011) Regulation of adult neurogenesis by behaviorand age in the accessory olfactory bulb. Mol Cell Neurosci 47: 274-285
85. Oboti L, Savalli G, Giachino C, De Marchis S, Panzica GC, Fasolo A, Peretto P (2009) Integration and sensory experience-dependent survival of newly-generated neurons in the accessory olfactory bulb of female mice. Eur J Neurosci 29: 679-692
86. Oboti L, Schellino R, Giachino C, Chamero P, Pyrski M, Leinders-Zufall T, Zufall F, Fasolo A, Peretto P (2011) Newborn interneurons in the accessory olfactory bulb promote mate recognition in female mice. Front Neurosci 5: 113
87. Panagiotakos G, Alshamy G, Chan B, Abrams R, Greenberg E, Saxena A, Bradbury M, Edgar M, Gutin P, Tabar V (2007) Long-term impact of radiation on the stem cell and oligodendrocyte precursors in the brain. PLoS One 2: E588
88. Panzanelli P, Bardy C, Nissant A, Pallotto M, Sassoe-Pognetto M, Lledo PM, Fritschy JM (2009) Early synapse formation in developing interneurons of the adult olfactory bulb. J Neurosci 29: 15039-15052
89. Peele P, Salazar I, Mimmack M, Keverne EB, Brennan PA (2003) Low molecular weight constituents of male mouse urine mediate the pregnancy block effect and convey information about the identity of the mating male. Eur J Neurosci 18: 622-628
90. Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: Role of olfaction. J Neurosci 22: 6106-6113
91. Ponti G, Aimar P, Bonfanti L (2006) Cellular composition and cytorchitecture of the rabbit subventricular zone (SVZ) and its extensions in the forebrain. J Comp Neurol 498: 491-507
92. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2006) Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J Comp Neurol 494: 415-434
93. Rall W, Shepherd GM (1968) Theoretical reconstruction of field potentials and dendrodentritic synaptic interactions in olfactory bulb. J Neurophysiol 31: 884-915
94. 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
95. Rodriguez-Perez LM, Perez-Martin M, Jimenez AJ, Fernandez-Llebrez P (2003) Immunocytochemical characterization of the wall of the bovine ventricle. Cell Tissue Res 314: 325-335
96. Rosser AE, Keverne EB (1985) The importance of central noradrenergic neurons in the formation of an olfactory memory in the prevention of pregnancy block. Neuroscience 15: 1141-1147
97. Sagathelyan A, Roux P, Migliore, Rochefort C, Demesaisons D, Charneau P, Shepherd GM, Lledo PM (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46: 103-116
98. Saghatelyan A (2009) Role of blood vessels in the neuronal migration. Semin Cell Dev Biol 20: 744-750
99. Sahay A, Wilson DA, Hen R (2011) Pattern separation: A common function for new neurons in hippocampus and olfactory bulb. Neuron 70: 582-588
100. Sakamoto M, Imayoshi I, Ohtsuka T, Yamaguchi M, Mori K, Kageyama R (2011) Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc Natl Acad Sci USA 108: 8479-8484
101. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740-744
102. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch D, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478: 382-386
103. Schoppa NE (2006) Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49: 271-283
104. Shepherd GM, Chen WR, Greer CA (2004) Olfactory bulb. In: Shepherd GM (ed) The synaptic organization of the brain, 5th edn. Oxford University Press, New York
105. Shingo T, Gregg C, Enwere, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003) Pregancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299: 117-120
106. Shipley MT, Halloran FJ, de la Torre J (1985) Surprinsingly rich projection from locus coeruleus to the olfactory bulb in the rat. Brain Res 329: 294-299
107. Sierra A, Encinas JM, Maletic-Savatic M (2011) Adult human neurogenesis: from microscopy to magnetic resonance imaging. Front Neurosci 5: 47
108. Singer BH, Jutkiewicz EM, Fuller CL, Lichtenwalner RJ, Zhang H, Velander AJ, Li X, Gnegy ME, Burant CF, Parent JM (2009) Conditional ablation and recovery of forebrain neurogenesis in the mouse. J Comp Neurol 514: 567-582
109. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12: 37-53
110. Smith MT, Pencea V, Wang Z, Luskin MB, Insel TR (2001) Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 39: 11-21
111. Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, Parent A, Saghatelyan A (2009) Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci 29: 4172-4188
112. Sullivan RM, Stackenwalt G, Nasr F, Lemon C, Wilson DA (2000) Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behav Neurosci 114: 957-962
113. Sultan S, Mandairon N, Kermen Fn Garcia S, Sacquet J, Didier A (2010) Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J 24: 2355-2363
114. Sultan S, Lefort JM, Sacquet J, Mandairon N, Didier A (2011a) Acquisition of an olfactory associative task triggers a regionalized down-regulation of adult born neuron cell death. Front Neurosci 5: 52
115. Sultan S, Rey N, Sacquet J, Mandairon N, Didier A (2011b) Newborn neurons in the olfactory bulb selected for long-term survival through olfactory learning are prematurely suppressed when the olfactory memory is erased. J Neurosci 31: 14893-14898
116. Temple S, Alvarez-Buylla A (1999) Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9: 135-141
117. Tepavcevic V, Lazarini F, Alfaro-cervello C, Kerninon C, Yoshikawa K, Garcia-Verdugo JM, Lleod PM, Nait-Oumesmar B, Baron-Van Evercooren A (2011) Inflammation-induced subventricular zone dysfunction leads to olfactory deficits in a targeted mouse model of multiple sclerosis. J Clin Invest 121: 4722-474
118. Valley MT, Mullen TR, Schultz LC, Sagdullaev BT, Firestein S (2009) Ablation of mouse adult neurogenesis alters olfactory bulb structure and olfactory fear conditioning. Front Neurosci 3: 51
119. Veyrac A, Sacquet J, Nguyen V, Marien M, Jourdan F, Didier A (2009) Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 34: 786-795
120. Wang X, Qiu R, Tsark W, Lu Q (2007) Rapid promoter analysis in developing mouse brain and genetic labeling of young neurons by doublecortin-DsRed-express. J Neurosci Res 85: 3576-3573
121. Wei L, Meaney M, Duman RS, Kaffman A (2011) Affiliative behavior requires juvenile, but not adult neurogenesis. J Neurosci 31: 14335-14345
122. Whitman MC, Greer C (2007) Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J Neurosci 27: 9951-9961
123. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebarin. Development 128: 3759-3771
124. Wilson DA, Stevenson RJ (2003) Olfactory perceptual learning: The critical role of memory in odor discrimination. Neurosci Biobehav Rev 4: 307-328
125. 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
126. Yamaguchi M, Mori K (2005) 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 102: 9697-9702
127. Yokoyama TK, Mochimaru D, Murata K, Manabe H, Kobayakawa K, Kobayakawa R, Sakano H, Mori K, Yamaguchi M (2011) Elimination of adult-born neurons in the olfactory bulb is promoted during the postprandial period. Neuron 71: 883-897
128. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132: 645-660