 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, July 15, 2002, 22(14):6106-6113
Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction
Leopoldo Petreanu1 and Arturo Alvarez-Buylla2 1 The Rockefeller University, New York, New York 10021, and 2 Neurosurgery Research, University of California, San Francisco, San Francisco, California 94134
Young neurons born in the subventricular zone (SVZ) of adult mice migrate to the olfactory bulb (OB) where they differentiate into granule cells (GCs) and periglomerular interneurons. Using retroviral labeling of precursors in the SVZ, we describe five stages and the timing for the maturation of newly formed GCs: (1) tangentially migrating neuroblasts (days 2-7); (2) radially migrating young neurons (days 5-7); (3) GCs with a simple unbranched dendrite that does not extend beyond the mitral cell layer (days 9-13); (4) GCs with a nonspiny branched dendrite in the external plexiform layer (days 11-22); and (5) mature GCs (days 15-30). Using [3H]thymidine, we show that the maximum number of labeled GCs is observed around day 15 after injection. Interestingly, between days 15 and 45 after birth, soon after the cells developed spines, the number of [3H]thymidine-labeled GCs declined by 50%. Using anosmic mice, we found that sensory input was critical for the survival of GCs from day 15 to 45 after labeling. However, the number and morphology of 15-d-old cells in the granule cell layer was similar in anosmic and wild-type mice. We infer that the lack of activity did not have an effect on the generation, migration, and early differentiation of granule cells. Soon after young GCs matured, and presumably became synaptically connected, their survival depended on the level of activity that they received. This selection mechanism might allow the construction of specific OB circuits based on olfactory experience and suggests possible functions of OB cell replacement.
Key words: olfactory bulb; granule cells; neurogenesis; new neurons; cell death; olfaction
Copyright © 2002 Society for Neuroscience 0270-6474/02/22146106-08$05.00/0
This article has been cited by other articles:
A. Mouret, G. Lepousez, J. Gras, M.-M. Gabellec, and P.-M. Lledo
Turnover of Newborn Olfactory Bulb Neurons Optimizes Olfaction
J. Neurosci., September 30, 2009; 29(39): 12302 - 12314.
[Abstract] [Full Text] [PDF]
W. Kelsch, C.-W. Lin, C. P. Mosley, and C. Lois
A Critical Period for Activity-Dependent Synaptic Development during Olfactory Bulb Adult Neurogenesis
J. Neurosci., September 23, 2009; 29(38): 11852 - 11858.
[Abstract] [Full Text] [PDF]
I. M. Wittko, A. Schanzer, A. Kuzmichev, F. T. Schneider, M. Shibuya, S. Raab, and K. H. Plate
VEGFR-1 Regulates Adult Olfactory Bulb Neurogenesis and Migration of Neural Progenitors in the Rostral Migratory Stream In Vivo
J. Neurosci., July 8, 2009; 29(27): 8704 - 8714.
[Abstract] [Full Text] [PDF]
N. Mandairon and C. Linster
Odor Perception and Olfactory Bulb Plasticity in Adult Mammals
J Neurophysiol, May 1, 2009; 101(5): 2204 - 2209.
[Abstract] [Full Text] [PDF]
F. Liu, Y. You, X. Li, T. Ma, Y. Nie, B. Wei, T. Li, H. Lin, and Z. Yang
Brain Injury Does Not Alter the Intrinsic Differentiation Potential of Adult Neuroblasts
J. Neurosci., April 22, 2009; 29(16): 5075 - 5087.
[Abstract] [Full Text] [PDF]
D. P. Darcy and J. S. Isaacson
L-Type Calcium Channels Govern Calcium Signaling in Migrating Newborn Neurons in the Postnatal Olfactory Bulb
J. Neurosci., February 25, 2009; 29(8): 2510 - 2518.
[Abstract] [Full Text] [PDF]
C. Gregorian, J. Nakashima, J. Le Belle, J. Ohab, R. Kim, A. Liu, K. B. Smith, M. Groszer, A. D. Garcia, M. V. Sofroniew, et al.
Pten Deletion in Adult Neural Stem/Progenitor Cells Enhances Constitutive Neurogenesis
J. Neurosci., February 11, 2009; 29(6): 1874 - 1886.
[Abstract] [Full Text] [PDF]
Y. Livneh, N. Feinstein, M. Klein, and A. Mizrahi
Sensory Input Enhances Synaptogenesis of Adult-Born Neurons
J. Neurosci., January 7, 2009; 29(1): 86 - 97.
[Abstract] [Full Text] [PDF]
M. C. Havrda, B. T. Harris, A. Mantani, N. M. Ward, B. R. Paolella, V. C. Cuzon, H. H. Yeh, and M. A. Israel
Id2 Is Required for Specification of Dopaminergic Neurons during Adult Olfactory Neurogenesis
J. Neurosci., December 24, 2008; 28(52): 14074 - 14087.
[Abstract] [Full Text] [PDF]
M. O. Karl, S. Hayes, B. R. Nelson, K. Tan, B. Buckingham, and T. A. Reh
Stimulation of neural regeneration in the mouse retina
PNAS, December 9, 2008; 105(49): 19508 - 19513.
[Abstract] [Full Text] [PDF]
A. Alvarez-Buylla, M. Kohwi, T.M. Nguyen, and F.T. Merkle
The Heterogeneity of Adult Neural Stem Cells and the Emerging Complexity of Their Niche
Cold Spring Harb Symp Quant Biol, November 6, 2008; (2008) sqb.2008.73.019v1.
[Abstract] [PDF]
A. Mouret, G. Gheusi, M.-M. Gabellec, F. de Chaumont, J.-C. Olivo-Marin, and P.-M. Lledo
Learning and Survival of Newly Generated Neurons: When Time Matters
J. Neurosci., November 5, 2008; 28(45): 11511 - 11516.
[Abstract] [Full Text] [PDF]
W. Kelsch, C.-W. Lin, and C. Lois
Sequential development of synapses in dendritic domains during adult neurogenesis
PNAS, October 28, 2008; 105(43): 16803 - 16808.
[Abstract] [Full Text] [PDF]
M. Alonso, I. Ortega-Perez, M. S. Grubb, J.-P. Bourgeois, P. Charneau, and P.-M. Lledo
Turning Astrocytes from the Rostral Migratory Stream into Neurons: A Role for the Olfactory Sensory Organ
J. Neurosci., October 22, 2008; 28(43): 11089 - 11102.
[Abstract] [Full Text] [PDF]
J. J. Ohab and S. T. Carmichael
Poststroke Neurogenesis: Emerging Principles of Migration and Localization of Immature Neurons
Neuroscientist, August 1, 2008; 14(4): 369 - 380.
[Abstract] [PDF]
M. Kukley, M. Kiladze, R. Tognatta, M. Hans, D. Swandulla, J. Schramm, and D. Dietrich
Glial cells are born with synapses
FASEB J, August 1, 2008; 22(8): 2957 - 2969.
[Abstract] [Full Text] [PDF]
H. Okano and K. Sawamoto
Neural stem cells: involvement in adult neurogenesis and CNS repair
Phil Trans R Soc B, June 27, 2008; 363(1500): 2111 - 2122.
[Abstract] [Full Text] [PDF]
L. Belluscio and D. M. Cummings
Charting Plasticity in the Regenerating Maps of the Mammalian Olfactory Bulb
Neuroscientist, June 1, 2008; 14(3): 251 - 263.
[Abstract] [PDF]
R. Batista-Brito, J. Close, R. Machold, and G. Fishell
The Distinct Temporal Origins of Olfactory Bulb Interneuron Subtypes
J. Neurosci., April 9, 2008; 28(15): 3966 - 3975.
[Abstract] [Full Text] [PDF]
K. A. Hamilton, S. Parrish-Aungst, F. L. Margolis, F. Erdelyi, G. Szabo, and A. C. Puche
Sensory Deafferentation Transsynaptically Alters Neuronal GluR1 Expression in the External Plexiform Layer of the Adult Mouse Main Olfactory Bulb
Chem Senses, February 1, 2008; 33(2): 201 - 210.
[Abstract] [Full Text] [PDF]
W. R. Kim, Y. Kim, B. Eun, O.-h. Park, H. Kim, K. Kim, C.-H. Park, S. Vinsant, R. W. Oppenheim, and W. Sun
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., December 26, 2007; 27(52): 14392 - 14403.
[Abstract] [Full Text] [PDF]
H.T. Ghashghaei, J. M. Weimer, R. S. Schmid, Y. Yokota, K. D. McCarthy, B. Popko, and E.S. Anton
Reinduction of ErbB2 in astrocytes promotes radial glial progenitor identity in adult cerebral cortex
Genes & Dev., December 15, 2007; 21(24): 3258 - 3271.
[Abstract] [Full Text] [PDF]
J. Ninkovic, T. Mori, and M. Gotz
Distinct Modes of Neuron Addition in Adult Mouse Neurogenesis
J. Neurosci., October 3, 2007; 27(40): 10906 - 10911.
[Abstract] [Full Text] [PDF]
M. C. Whitman and C. A. Greer
Synaptic Integration of Adult-Generated Olfactory Bulb Granule Cells: Basal Axodendritic Centrifugal Input Precedes Apical Dendrodendritic Local Circuits
J. Neurosci., September 12, 2007; 27(37): 9951 - 9961.
[Abstract] [Full Text] [PDF]
M. Kohwi, M. A. Petryniak, J. E. Long, M. Ekker, K. Obata, Y. Yanagawa, J. L. R. Rubenstein, and A. Alvarez-Buylla
A Subpopulation of Olfactory Bulb GABAergic Interneurons Is Derived from Emx1- and Dlx5/6-Expressing Progenitors
J. Neurosci., June 27, 2007; 27(26): 6878 - 6891.
[Abstract] [Full Text] [PDF]
I. Fishbein and M. Segal
Miniature Synaptic Currents Become Neurotoxic to Chronically Silenced Neurons
Cereb Cortex, June 1, 2007; 17(6): 1292 - 1306.
[Abstract] [Full Text] [PDF]
R. Balu, R. T. Pressler, and B. W. Strowbridge
Multiple Modes of Synaptic Excitation of Olfactory Bulb Granule Cells
J. Neurosci., May 23, 2007; 27(21): 5621 - 5632.
[Abstract] [Full Text] [PDF]
N. Andrade, V. Komnenovic, S. M. Blake, Y. Jossin, B. Howell, A. Goffinet, W. J. Schneider, and J. Nimpf
ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of Reelin
PNAS, May 15, 2007; 104(20): 8508 - 8513.
[Abstract] [Full Text] [PDF]
G. Gheusi and P.-M. Lledo
Control of Early Events in Olfactory Processing by Adult Neurogenesis
Chem Senses, May 1, 2007; 32(4): 397 - 409.
[Abstract] [Full Text] [PDF]
S. De Marchis, S. Bovetti, B. Carletti, Y.-C. Hsieh, D. Garzotto, P. Peretto, A. Fasolo, A. C. Puche, and F. Rossi
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., January 17, 2007; 27(3): 657 - 664.
[Abstract] [Full Text] [PDF]
M. Alonso, C. Viollet, M.-M. Gabellec, V. Meas-Yedid, J.-C. Olivo-Marin, and P.-M. Lledo
Olfactory Discrimination Learning Increases the Survival of Adult-Born Neurons in the Olfactory Bulb
J. Neurosci., October 11, 2006; 26(41): 10508 - 10513.
[Abstract] [Full Text] [PDF]
N. Kaneko, H. Okano, and K. Sawamoto
Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb.
Genes Cells, October 1, 2006; 11(10): 1145 - 1159.
[Abstract] [Full Text] [PDF]
U Shivraj Sohur, J. G Emsley, B. D Mitchell, and J. D Macklis
Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells
Phil Trans R Soc B, September 29, 2006; 361(1473): 1477 - 1497.
[Abstract] [Full Text] [PDF]
A. Mizrahi, J. Lu, R. Irving, G. Feng, and L. C. Katz
In vivo imaging of juxtaglomerular neuron turnover in the mouse olfactory bulb
PNAS, February 7, 2006; 103(6): 1912 - 1917.
[Abstract] [Full Text] [PDF]
F. Luzzati, S. De Marchis, A. Fasolo, and P. Peretto
Neurogenesis in the Caudate Nucleus of the Adult Rabbit
J. Neurosci., January 11, 2006; 26(2): 609 - 621.
[Abstract] [Full Text] [PDF]
S. S. P. Magavi, B. D. Mitchell, O. Szentirmai, B. S. Carter, and J. D. Macklis
Adult-Born and Preexisting Olfactory Granule Neurons Undergo Distinct Experience-Dependent Modifications of their Olfactory Responses In Vivo
J. Neurosci., November 16, 2005; 25(46): 10729 - 10739.
[Abstract] [Full Text] [PDF]
C. Giachino, S. De Marchis, C. Giampietro, R. Parlato, I. Perroteau, G. Schutz, A. Fasolo, and P. Peretto
cAMP Response Element-Binding Protein Regulates Differentiation and Survival of Newborn Neurons in the Olfactory Bulb
J. Neurosci., November 2, 2005; 25(44): 10105 - 10118.
[Abstract] [Full Text] [PDF]
M. Kohwi, N. Osumi, J. L. R. Rubenstein, and A. Alvarez-Buylla
Pax6 Is Required for Making Specific Subpopulations of Granule and Periglomerular Neurons in the Olfactory Bulb
J. Neurosci., July 27, 2005; 25(30): 6997 - 7003.
[Abstract] [Full Text] [PDF]
M. Lemasson, A. Saghatelyan, J.-C. Olivo-Marin, and P.-M. Lledo
Neonatal and Adult Neurogenesis Provide Two Distinct Populations of Newborn Neurons to the Mouse Olfactory Bulb
J. Neurosci., July 20, 2005; 25(29): 6816 - 6825.
[Abstract] [Full Text] [PDF]
M. Yamaguchi and K. Mori
Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb
PNAS, July 5, 2005; 102(27): 9697 - 9702.
[Abstract] [Full Text] [PDF]
T.-W. Wang, H. Zhang, and J. M. Parent
Retinoic acid regulates postnatal neurogenesis in the murine subventricular zone-olfactory bulb pathway
Development, June 15, 2005; 132(12): 2721 - 2732.
[Abstract] [Full Text] [PDF]
N. Miwa and D. R. Storm
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., June 1, 2005; 25(22): 5404 - 5412.
[Abstract] [Full Text] [PDF]
A. J. Lombardino, X.-C. Li, M. Hertel, and F. Nottebohm
Replaceable neurons and neurodegenerative disease share depressed UCHL1 levels
PNAS, May 31, 2005; 102(22): 8036 - 8041.
[Abstract] [Full Text] [PDF]
V. Egger, K. Svoboda, and Z. F. Mainen
Dendrodendritic Synaptic Signals in Olfactory Bulb Granule Cells: Local Spine Boost and Global Low-Threshold Spike
J. Neurosci., April 6, 2005; 25(14): 3521 - 3530.
[Abstract] [Full Text] [PDF]
D. N. Abrous, M. Koehl, and M. Le Moal
Adult Neurogenesis: From Precursors to Network and Physiology
Physiol Rev, April 1, 2005; 85(2): 523 - 569.
[Abstract] [Full Text] [PDF]
P.-M. Lledo, G. Gheusi, and J.-D. Vincent
Information Processing in the Mammalian Olfactory System
Physiol Rev, January 1, 2005; 85(1): 281 - 317.
[Abstract] [Full Text] [PDF]
H. G. Kuhn, C. Cooper-Kuhn, P. Eriksson, and M. Nilsson
Signals Regulating Neurogenesis in the Adult Olfactory Bulb
Chem Senses, January 1, 2005; 30(suppl_1): i109 - i110.
[Full Text] [PDF]
M. Yamaguchi
Analysis of neurogenesis using transgenic mice expressing GFP with nestin gene regulatory regions
Chem Senses, January 1, 2005; 30(suppl_1): i117 - i118.
[Full Text] [PDF]
A. Pignatelli, M. Benedusi, J. Ackman, J. J. LoTurco, and O. Belluzzi
Functional Properties of Adult-born Juxtaglomerular Cells in the Mammalian Olfactory Bulb
Chem Senses, January 1, 2005; 30(suppl_1): i119 - i120.
[Full Text] [PDF]
W. Sun, A. Winseck, S. Vinsant, O.-h. Park, H. Kim, and R. W. Oppenheim
Programmed Cell Death of Adult-Generated Hippocampal Neurons Is Mediated by the Proapoptotic Gene Bax
J. Neurosci., December 8, 2004; 24(49): 11205 - 11213.
[Abstract] [Full Text] [PDF]
J. Chen, S. S. P. Magavi, and J. D. Macklis
Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice
PNAS, November 16, 2004; 101(46): 16357 - 16362.
[Abstract] [Full Text] [PDF]
A. Consiglio, A. Gritti, D. Dolcetta, A. Follenzi, C. Bordignon, F. H. Gage, A. L. Vescovi, and L. Naldini
From the Cover: Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors
PNAS, October 12, 2004; 101(41): 14835 - 14840.
[Abstract] [Full Text] [PDF]
A. Nicot, T. Otto, P. Brabet, and E. M. DiCicco-Bloom
Altered Social Behavior in Pituitary Adenylate Cyclase-Activating Polypeptide Type I Receptor-Deficient Mice
J. Neurosci., October 6, 2004; 24(40): 8786 - 8795.
[Abstract] [Full Text] [PDF]
A. F. Schinder and F. H. Gage
A Hypothesis About the Role of Adult Neurogenesis in Hippocampal Function
Physiology, October 1, 2004; 19(5): 253 - 261.
[Abstract] [Full Text] [PDF]
E. Enwere, T. Shingo, C. Gregg, H. Fujikawa, S. Ohta, and S. Weiss
Aging Results in Reduced Epidermal Growth Factor Receptor Signaling, Diminished Olfactory Neurogenesis, and Deficits in Fine Olfactory Discrimination
J. Neurosci., September 22, 2004; 24(38): 8354 - 8365.
[Abstract] [Full Text] [PDF]
P.-M. Lledo, A. Saghatelyan, and M. Lemasson
Inhibitory Interneurons in the Olfactory Bulb: From Development to Function
Neuroscientist, August 1, 2004; 10(4): 292 - 303.
[Abstract] [PDF]
N. Mechawar, A. Saghatelyan, R. Grailhe, L. Scoriels, G. Gheusi, M.-M. Gabellec, P.-M. Lledo, and J.-P. Changeux
Nicotinic receptors regulate the survival of newborn neurons in the adult olfactory bulb
PNAS, June 29, 2004; 101(26): 9822 - 9826.
[Abstract] [Full Text] [PDF]
B. Alvarez-Borda, B. Haripal, and F. Nottebohm
Timing of brain-derived neurotrophic factor exposure affects life expectancy of new neurons
PNAS, March 16, 2004; 101(11): 3957 - 3961.
[Abstract] [Full Text] [PDF]
K. T. Nguyen-Ba-Charvet, N. Picard-Riera, M. Tessier-Lavigne, A. Baron-Van Evercooren, C. Sotelo, and A. Chedotal
Multiple Roles for Slits in the Control of Cell Migration in the Rostral Migratory Stream
J. Neurosci., February 11, 2004; 24(6): 1497 - 1506.
[Abstract] [Full Text] [PDF]
O. Belluzzi, M. Benedusi, J. Ackman, and J. J. LoTurco
Electrophysiological Differentiation of New Neurons in the Olfactory Bulb
J. Neurosci., November 12, 2003; 23(32): 10411 - 10418.
[Abstract] [Full Text] [PDF]
D. Ehninger and G. Kempermann
Regional Effects of Wheel Running and Environmental Enrichment on Cell Genesis and Microglia Proliferation in the Adult Murine Neocortex
Cereb Cortex, August 1, 2003; 13(8): 845 - 851.
[Abstract] [Full Text] [PDF]
R. C. Murray, D. Navi, J. Fesenko, A. D. Lander, and A. L. Calof
Widespread Defects in the Primary Olfactory Pathway Caused by Loss of Mash1 Function
J. Neurosci., March 1, 2003; 23(5): 1769 - 1780.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|