Enriched Odor Exposure Increases the Number of Newborn Neurons in the Adult Olfactory Bulb and Improves Odor Memory

Journal of Neuroscience

Volumn 22, Issue 7, 2002, Pages 2679-2689

  Rochefort, Christelle ^a   Gheusi, Gilles ^a,b   Vincent, Jean Didier ^a   Lledo, Pierre Marie ^a  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ PARIS 13   (France)

Author keywords

Behavior; Cell survival; Hippocampus; Interneurons; Neurogenesis; Olfaction; Progenitor cells

Indexed keywords

BROXURIDINE; 3 XYLENE; 3-XYLENE; ALDEHYDE; ESSENTIAL OIL; OCTANOL; XYLENE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; HIPPOCAMPUS; INJECTION; LEARNING; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY NERVE; PRIORITY JOURNAL; STEM CELL; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CELL DIVISION; CYTOLOGY; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; INHALATIONAL DRUG ADMINISTRATION; NERVE CELL; PHYSIOLOGY; STIMULATION;

ADMINISTRATION, INHALATION; ALDEHYDES; ANIMALS; BEHAVIOR, ANIMAL; BROMODEOXYURIDINE; CELL COUNT; CELL DIVISION; CELL SURVIVAL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MICE; MICE, INBRED C57BL; NEURONS; OCTANOLS; ODORS; OILS, VOLATILE; OLFACTORY BULB; SMELL; STEM CELLS; STIMULATION, CHEMICAL; XYLENES;

EID: 0036550759     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-07-02679.2002     Document Type: Article

References (51)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal neurogenesis in rats. J Comp Neurol 124:319-335.
2. Barnea A, Nottebohm F (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217-11221.
3. Bennett EL, Rosenzweig MR, Diamond MC, Morimoto H, Hebert M (1974) Effects of successive environments on brain measures. Physiol Behav 12:621-631.
4. Berardi N, Pizzorusso T, Maffei L (2000) Critical periods during sensory development. Curr Opin Neurobiol 10:138-145.
5. 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.
6. Bluthé RM, Gheusi G, Dantzer R (1993). Gonadal steroids influence the involvement of arginine vasopressin in social recognition in mice. Psychoneuroendocrinology 18:323-351.
7. Bonfanti L, Theodosis DT (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62:291-305.
8. Brunjes PC, Armstrong AM (1996) Apoptosis in the rostral migratory stream of the developing rat. Brain Res Dev 92:219-222.
9. Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H (2000) Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20:1446-1457.
10. Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3:1091-1097.
11. Corotto FS, Henegar JR, Maruniak JA (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61:739-744.
12. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16:2649-2658.
13. Cummings DM, Henning HE, Brunjes PC (1997) Olfactory bulb recovery after early sensory deprivation. J Neurosci 17:7433-7440.
14. Doetsch F, Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 93:14895-14900.
15. Dusek JA, Eichenbaum H (1997) The hippocampus and memory for orderly stimulus relations. Proc Natl Acad Sci USA 94:7109-7114.
16. Fagiolini M, Hensch TK (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404:183-186.
17. Fiske BK, Brunjes PC (2001) Cell death in the developing and sensory-deprived rat olfactory bulb. J Comp Neurol 431:311-319.
18. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438.
19. Gould E, Beylin A, Tanapat P, Reeves AJ, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
20. Green EJ, Greenough WT (1986) Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro. J Neurophysiol 55:739-750.
21. Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1:67-73.
22. Hu H (1999) Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron 23:703-711.
23. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755.
24. Jankovski A, Garcia C, Soriano E, Sotelo C (1998) Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci 10:3853-3868.
25. Kempermann G, Kuhn GH, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
26. Kennedy TE, Tessier-Lavigne M (1995) Guidance and induction of branch formation in developing axons by target-derived diffusible factors. Curr Opin Neurobiol 5:83-90.
27. Kirschenbaum B, Goldman SA (1995) Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc Natl Acad Sci USA 92:210-214.
28. Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A (1999) Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci 19:2171-2180.
29. 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.
30. Levison SW, Rothstein RP, Brazel CY, Young GM, Albrecht PJ (2000) Selective apoptosis within the rat subependymal zone: a plausible mechanism for determining which lineages develop from neural cells. Dev Neurosci 22:106-115.
31. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
32. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978-981.
33. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
34. Lynch G, Granger R (1991) Serial steps in memory processings: possible clues from studies of plasticity in the olfactory-hippocampal circuit. In: Olfaction, a model system for computational neuroscience (Davis JL, Eichenbaum H, eds), pp 141-165. Cambridge, MA: MIT.
35. Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711-715.
36. Morshead CM, van der Kooy D (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12:249-256.
37. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
38. Murray RC, Calof AL (1999) Neuronal regeneration: lessons from the olfactory system. Semin Cell Dev Biol 10:421-431.
39. Najbauer J, Leon M (1995) Olfactory experience modulated apoptosis in the developing olfactory bulb. Brain Res 674:245-251.
40. Peretto P, Merighi A, Fasolo A, Bonfanti L (1999) The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain. Brain Res Bull 49:221-243.
41. Rabin MD (1988) Experience facilitates olfactory quality discrimination. Percept Psychophys 44:532-540.
42. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ (2000) Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3:238-244.
43. Rosselli-Austin L, Williams J (1990) Enriched neonatal odor exposure leads to increased numbers of olfactory bulb mitral and granule cells. Dev Brain Res 51:135-137.
44. Rousselot P, Lois C, Alvarez-Buylla A (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol 351:51-61.
45. Svendsen CN, Sofroniew MV (1996) Do central nervous system neurons require target-derived neurotrophic support for survival throughout adult life and aging? Perspect Dev Neurobiol 3:133-142.
46. Temple S, Alvarez-Buylla A (1999) Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9:135-141.
47. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
48. Woo CC, Leon M (1995) Early olfactory enrichment and deprivation both decrease beta-adrenergic receptor density in the main olfactory bulb of the rat. J Comp Neurol 360:634-642.
49. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity, Nature 397:613-616.
50. Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY, Rao Y (1999) Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400:331-336.
51. 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.