Reorganization of neuronal circuits of the central olfactory system during postprandial sleep

Frontiers in Neural Circuits

Volumn , Issue JUL, 2013, Pages

  Yamaguchi, Masahiro ^a,b   Manabe, Hiroyuki ^a,b   Murata, Koshi ^a,b   Mori, Kensaku ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Adult neurogenesis; Behavioral state; Cell elimination; Olfactory bulb; Olfactory cortex; Sensory experience; Sharp waves; Slow wave sleep

Indexed keywords

CASPASE 3; ODORANT RECEPTOR; PROLACTIN; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DEATH; CELL SURVIVAL; EMBRYO DEVELOPMENT; INFORMATION PROCESSING; INTERNEURON; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY MEMORY; OLFACTORY SENSORY NEURON; OLFACTORY SYSTEM; ORBITAL CORTEX; POSTPRANDIAL STATE; PYRAMIDAL NERVE CELL; REM SLEEP; REVIEW; SENSORY DEPRIVATION; SENSORY NERVE CELL; SENSORY STIMULATION; SLOW WAVE SLEEP; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84882678176     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00132     Document Type: Review

References (111)

1. Allison, A. C., and Warwick, R. T. (1949). Quantitative observations on the olfactory system of the rabbit. Brain 72, 186-197. doi: 10.1093/brain/72.2.186
2. Alonso, M., Viollet, C., Gabellec, M. M., Meas-Yedid, V., Olivo-Marin, J. C., and Lledo, P. M. (2006). Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci. 26, 10508-10513. doi: 10.1523/JNEUROSCI.2633-06.2006
3. Alvarez-Buylla, A., Garcia-Verdugo, J., and Tramontin, A. D. (2001). A unified hypothesis on the lineage of neuroal stem cells. Nat. Rev. Neurosci. 2, 287-293. doi: 10.1038/35067582
4. Arenkiel, B. R., Hasegawa, H., Yi, J. J., Larsen, R. S., Wallace, M. L., Philpot, B. D., et al. (2011). Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS ONE 6:e29423. doi: 10.1371/journal.pone.0029423
5. Bayer, S. A. (1983). 3H-thymidineradiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50, 329-340.
6. Biebl, M., Cooper, C. M., Winkler, J., and Kuhn, H. G. (2000). Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett. 291, 17-20. doi: 10.1016/S0304-3940(00)01368-9
7. Boyd, A. M., Sturgill, J. F., Poo, C., and Isaacson, J. S. (2012). Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161-1174. doi: 10.1016/j.neuron.2012.10.020
8. Brennan, P., Kaba, H., and Keverne, E. B. (1990). Olfactory recognition: a simple memory system. Science 250, 1223-1226. doi: 10.1126/science.2147078
9. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187. doi: 10.1016/0092-8674(91)90418-X
10. Bushey, D., Tononi, G., and Cirelli, C. (2011). Sleep and synaptic homeostasis: structural evidence in drosophila. Science 332, 1676-1581. doi: 10.1126/science.1202839
11. Buss, R. R., Sun, W., and Oppenheim, R. W. (2006). Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 29, 1-35. doi: 10.1146/annurev.neuro.29.051605.112800
12. Buzsaki, G. (1989). Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31, 551-570. doi: 10.1016/03064522(89)90423-5
13. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A., and Lledo, P. M. (2003). Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507-518.
14. Chess, A., Simon, I., Cedar, H., and Axel, R. (1994). Allelic inactivation regulates olfactory gene expression. Cell 78, 823-834. doi: 10.1016/S0092-8674(94)90562-2
15. Cooper-Kuhn, C. M., Winkler, J., and Kuhn, H. G. (2004). Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J. Neurosci. Res. 77, 155-165. doi: 10.1002/jnr.20116
16. Corotto, F., Henegar, J., and Maruniak, J. (1994). Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61, 739-744. doi: 10.1016/0306-4522(94)90397-2
17. Crick, F. C., and Koch, C. (2005). What is the function of the claustrum? Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 1271-1279. doi: 10.1098/rstb.2005.1661
18. Csicsvari, J., Hirase, H., Mamiya, A., and Buzsaki, G. (2000). Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585-594. doi: 10.1016/S0896-6273(00)00135-5
19. Dallman, M. F., Strack, A. M., Akana, S. F., Bradbury, M. J., Hanson, E. S., Scribner, K. A., et al. (1993). Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front. Neuroendocrin. 14, 303-347. doi: 10.1006/frne.1993.1010
20. Deshpande, A., Bergami, M., Ghanem, A., Conzelmann, K. K., Lepier, A., Götz, M., et al. (2013). Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 110, E1152-E1161. doi: 10.1073/pnas.1218991110
21. Devore, S., Manella, L. C., and Linster, C. (2012). Blocking muscarinic receptors in the olfactory bulb impairs performance on an olfactory short-term memory task. Front. Behav. Neurosci. 6:59. doi: 10.3389/fnbeh.2012.00059
22. Diekelmann, S., and Born, J. (2010). The memory function of sleep. Nat. Rev. Neurosci. 11, 114-126.
23. Doty, R. L. (1986). Odor-guided behavior in mammals. Experientia 42, 257-271. doi: 10.1007/BF01942506
24. Eyre, M. D., Antal, M., and Nusser, Z. (2008). Distinct deep shortaxon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J. Neurosci. 28, 8217-8229. doi: 10.1523/JNEUROSCI.2490-08.2008
25. Foster, D. J., and Wilson, M. A. (2006). Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680-683. doi: 10.1038/nature04587
26. Frey, U., and Morris, R. G. M. (1997). Synaptic tagging and long-term potentiation. Nature 385, 533-536. doi: 10.1038/385533a0
27. Gao, Q., and Horvath, T. L. (2007). Neurobiology of feeding and energy expenditure. Annu. Rev. Neurosci. 30, 367-398. doi: 10.1146/annurev.neuro.30.051606.094324
28. Gao, Y., and Strowbridge, W. (2009). Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb. Nat. Neurosci. 12, 731-733. doi: 10.1038/nn.2319
29. Ghosh, S., Larson, S. D., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K., et al. (2011). Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220. doi: 10.1038/nature09945
30. Gogos, J. A., Osborne, J., Nemes, A., Mendelsohn, M., and Axel, R. (2000). Genetic ablation and restoration of the olfactory topographic map. Cell 103, 609-620. doi: 10.1016/S0092-8674(00)00164-1
31. Haberly, L. B. (2001). Paralleldistributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26, 551-576. doi: 10.1093/chemse/26.5.551
32. Hasselmo, M. E. (1999). Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3, 351-359. doi: 10.1016/S1364-6613(99)01365-0
33. Hasselmo, M. E., and Bower, J. M. (1992). Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J. Neurophysiol. 67, 1222-1229.
34. Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888. doi: 10.1038/nrn1787
35. Hinds, J. W. (1968). Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J. Comp. Neurol. 134, 287-304. doi: 10.1002/cne.901340304
36. Igarashi, K. M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., et al. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970-7985. doi: 10.1523/JNEUROSCI.0154-12.2012
37. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., et al. (2008). Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11, 1153-1161. doi: 10.1038/nn.2185
38. Kaba, H., and Nakanishi, S. (1995). Synaptic mechanisms of olfactory recognition memory. Rev. Neurosci. 6, 125-141. doi: 10.1515/REVNEURO.1995.6.2.125
39. Kaneko, N., Okano, H., and Sawamoto, K. (2006). Role of cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 11, 1145-1159. doi: 10.1111/j.1365-2443.2006. 01010.x
40. Kanter, E. D., and Haberly, L. B. (1990). NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro. Brain Res. 525, 175-179. doi: 10.1016/0006-8993(90)91337-G
41. Kaplan, M. S., McNelly, N. A., and Hinds, J. W. (1985). Population dynamics of adult-formed granule neurons of the rat olfactory bulb. J. Comp. Neurol. 239, 117-125. doi: 10.1002/cne.902390110
42. Kasa, P., Hlavati, I., Dobo, E., Wolff, A., Joo, F., and Wolff, J. R. (1995). Synaptic and nonsynaptic cholinergic innervation of the various types of neurons in the main olfactory bulb of adult rat: immunocytochemistry of choline acethyltransferase. Neuroscience 67, 667-677. doi: 10.1016/0306-4522(95) 00031-D
43. Kashiwadani, H., Sasaki, Y. F., Uchida, N., and Mori, K. (1999). Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J. Neurophysiol. 82, 1786-1792.
44. Katagiri, H., Pallotto, M., Nissant, A., Murray, K., Sassoè-Pognetto, M., and Lledo, P. M. (2011). Dynamic development of the first synapse impinging on adult-born neurons in the olfactory bulb circuit. Neural Syst. Circuits 1:6. doi: 10.1186/2042-1001-1-6
45. Kelsch, W., Lin, C. W., and Lois, C. (2008). Sequential development of synapses in dendritic domains during adult neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 16803-16808. doi: 10.1073/pnas.0807970105
46. Kelsch, W., Sim, S., and Lois, C. (2010). Watching synaptogenesis in the adult brain. Annu. Rev. Neurosci. 33, 131-149. doi: 10.1146/annurev-neuro-060909-153252
47. Keverne, E. B. (2004). Importance of olfactory and vomeronasal systems for male sexual function. Physiol. Behav. 83, 177-187.
48. Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., et al. (2007). Innate versus learned odour processing in the mouse olfactory bulb. Nature 450, 503-508. doi: 10.1038/nature 06281
49. Lagace, D. C., Whitman, M. C., Nooman, M. A., Ables, J. L., DeCarolis, N. A., Arguella, A. A., et al. (2007). Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 27, 12623-12629. doi: 10.1523/JNEUROSCI.3812-07.2007
50. Landers, M. S., and Sullivan, R. M. (2012). The development and neurobiology of infant attachment and fear. Dev. Neurosci. 34, 101-114. doi: 10.1159/000336732
51. Lau, W. M., Qiu, G., Helmeste, D. M., Lee, T. M., Tang, S. W., So, K. F., et al. (2007). Corticosteroid decreases subventricular zone cell proliferation, which could be reversed by paroxetine. Restor. Neurol. Neurosci. 25, 17-23.
52. Lazarini, F., Gabellec, M. M., Torquet, N., and Lledo, P. M. (2012). Early activation of microglia triggers long-lasting impairment of adult neurogenesis in the olfactory bulb. J. Neurosci. 32, 3652-3664. doi: 10.1523/JNEUROSCI.6394-11.2012
53. Lee, A. K., and Wilson, M. A. (2002). Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183-1194. doi: 10.1016/S0896-6273(02)01096-6
54. Le Jeune, H., Aubert, I., Jourdan, F., and Quirion, R. (1995). Comparative laminar distribution of various autoradiographic cholinergic markers in adult rat main olfactory bulb. J. Chem. Neuroanat. 9, 99-112. doi: 10.1016/0891-0618(95)00070-N
55. Lledo, P. M., Alonso, M., and Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179-193. doi: 10.1038/nrn1867
56. Luskin, M. B., and Price, J. L. (1983). The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J. Comp. Neurol. 216, 264-291. doi: 10.1002/cne.902160305
57. Mak, G. K., Enwere, E. K., Gregg, C., Pakarainen, T., Poutanen, M., Huhtaniemi, I., et al. (2007). Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat. Neurosci. 10, 1003-1011. doi: 10.1038/nn1928
58. Mak, G. K., and Weiss, S. (2010). Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat. Neurosci. 13, 753-758. doi: 10.1038/nn.2550
59. Malnic, B., Hirono, J., Sato, T., and Buck, L. B. (1999). Combinatorial receptor codes for odors. Cell 96, 713-723. doi: 10.1016/S0092-8674(00)80581-4
60. Manabe, H., Kusumoto-Yoshida, I., Ota, M., and Mori, K. (2011). Olfactory cortex generates synchronized top-down inputs to the olfactory bulb during slow-wave sleep. J. Neurosci. 31, 8123-8133. doi: 10.1523/JNEUROSCI.6578-10.2011
61. Mandairon, N., Jourdan, F., and Didier, A. (2003). Deprivation of sensory inputs to the olfactory bulb upregulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 119, 507-516. doi: 10.1016/S0306-4522(03) 00172-6
62. Mandairon, N., Sacquet, J., Jourdan, F., and Didier, A. (2006). Longterm fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience 141, 443-451. doi: 10.1016/j.neuroscience.2006.03.066
63. Maret, S., Faraguna, U., Nelson, A. B., Cirelli, C., and Tononi, G. (2011). Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat. Neurosci. 14, 1418-1420. doi: 10.1038/nn.2934
64. Markopoulos, F., Rokni, D., Gire, D. H., and Murthy, V. N. (2012). Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76, 1175-1188. doi: 10.1016/j.neuron.2012.10.028
65. McCune, S. K., Voigt, M. M., and Hill, J. M. (1993). Expression of multiple alpha adrenergic receptor subtype messenger RNAs in the adult rat brain. Neuroscience 57, 143-151. doi: 10.1016/0306-4522(93) 90116-W
66. McLean, J. H., Shipley, M. T., Nickell, W. T., Aston-Jones, G., and Reyher, C. K. H. (1989). Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J. Comp. Neurol. 285, 339-349. doi: 10.1002/cne.902850305
67. Moreno, M. M., Bath, K., Kuczewski, N., Sacquet, J., Didier, A., and Mandairon, N. (2012). Action of the noradrenergic system on adult-born cells is required for olfactory learning in mice. J. Neurosci. 32, 3748-3758. doi: 10.1523/JNEUROSCI.6335-11.2012
68. Moreno, M. M., Linster, C., Escanilla, O., Sacquet, J., Didier, A., and Mandairon, N. (2009). Olfactory perceptual learning requires adult neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 106, 17980-17985. doi: 10.1073/pnas.0907063106
69. Mori, K. (1987). Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog. Neurobiol. 29, 275-320. doi: 10.1016/0301-0082(87)90024-4
70. Mori, K., and Sakano, H. (2011). How is the olfactory map formed and interpreted in the mammalian brain? Annu. Rev. Neurosci. 34, 467-499. doi: 10.1146/annurevneuro-112210-112917
71. Mori, K., Takahashi, Y. K., Igarashi, K. M., and Yamaguchi, M. (2006). Maps of odorant molecular features in the mammalian olfactory bulb. Physiol. Rev. 86, 409-433. doi: 10.1152/physrev. 00021.2005
72. Morrow, B. A., Redmond, A. J., Roth, R. H., and Elsworth, J. D. (2000). The predator odor, TMT, displays a unique, stress-like pattern of dopaminergic and endocrinological activation in the rat. Brain Res. 864, 146-151. doi: 10.1016/S0006-8993(00)02174-0
73. Mouret, A., Gheusi, G., Gabellec, M. M., de Chaumont, F., Olivo-Martin, J. C., and Lledo, P. M. (2008). Learning and survival of newly generated neurons: when time matters. J. Neurosci. 28, 11511-11516. doi: 10.1523/JNEUROSCI.2954-08.2008
74. Mouret, A., Lepousez, G., Gras, J., Gabellec, M. M., and Lledo, P. M. (2009). Turnover of newborn olfactory bulb neurons optimizes olfaction. J. Neurosci. 29, 12302-12314. doi: 10.1523/JNEUROSCI.3383-09.2009
75. Murakami, M., Kashiwadani, H., Kirino, Y., and Mori, K. (2005). State-dependent sensory gating in olfactory cortex. Neuron 46, 285-296. doi: 10.1016/j.neuron.2005.02.025
76. Murata, K., Imai, M., Nakanishi, S., Watanabe, D., Pastan, I., Kobayashi, K., et al. (2011). Compensation of depleted neuronal subsets by new neurons in a local area of the adult olfactory bulb. J. Neurosci. 31, 10540-10557. doi: 10.1523/JNEUROSCI.1285-11.2011
77. Nagayama, S., Enerva, A., Fletcher, M. L., Masurkar, A. V., Igarashi, K. M., Mori, K., et al. (2010). Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front. Neural Circuits 4:120. doi: 10.3389/fncir.2010.00120
78. Nai, Q., Dong, H. W., Linster, C., and Ennis, M. (2010). Activation of alpha1 and alpha2 noradrenergic receptors exert opposing effects on excitability of main olfactory bulb granule cells. Neuroscience 169, 882-892. doi: 10.1016/j.neuroscience.2010.05.010
79. Neville, K. R., and Haberly, L. B. (2004). "Olfactory cortex," in The Synaptic Organization of the Brain, 5th Edn., ed G. Shepherd (New York, NY: Oxford UP), 415-454. doi: 10.1093/acprof:oso/9780195159561.003.0010
80. Ninkovic, J., Mori, T., and Gotz, M. (2007). Distinct modes of neuron addition in adult mouse neurogenesis. J. Neurosci. 27, 10906-10911. doi: 10.1523/JNEUROSCI.2572-07.2007
81. Nissant, A., Bardy, C., Katagiri, H., Murray, K., and Lledo, P. M. (2009). Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat. Neurosci. 12, 728-730. doi: 10.1038/nn.2298
82. Parrish-Aungst, S., Shipley, M. T., Erdelyi, F., Szabo, G., and Puche, A. C. (2007). Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 501, 825-836. doi: 10.1002/cne.21205
83. Petreanu, L., and Alvarez-Buylla, A. (2002). Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22, 6106-6113.
84. Poo, C., and Isaacson, J. S. (2007). An early critical period for long-term plasticity and structural modification of sensory synapses in olfactory cortex. J. Neurosci. 27, 7553-7558. doi: 10.1523/JNEUROSCI.1786-07.2007
85. Poo, C., and Isaacson, J. S. (2011). A major role for intracortical circuits in the strength and tuning of odor-evoked excitation in olfactory cortex. Neuron 72, 41-48. doi: 10.1016/j.neuron.2011.08.015
86. Redondo, R. L., and Morris, R. G. (2011). Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 12, 17-30. doi: 10.1038/nrn2963
87. Rochefort, C., Gheusi, G., Vincent, J., and Lledo, P. M. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689.
88. Saar, D., Grossman, Y., and Barkai, E. (2002). Learning-induced enhancement of postsynaptic potentials in pyramidal neurons. J. Neurophysiol. 87, 2358-2363.
89. Saghatelyan, A., Roux, P., Migliore, M., Rochefort, C., Desmaisons, D., Charneau, P., et al. (2005). Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46, 103-116. doi: 10.1016/j.neuron.2005.02.016
90. Sanchez-Andrade, G., and Kendrick, K. M. (2009). The main olfactory system and social learning in mammals. Behav. Brain Res. 200, 323-335. doi: 10.1016/j.bbr.2008.12.021
91. Schneider, S. P., and Macrides, F. (1978). Laminar distributions of interneurons in the main olfactory bulb of the adult hamster. Brain Res. Bull. 3, 73-82. doi: 10.1016/0361-9230(78)90063-1
92. Shepherd, G. M., Chen, W., and Greer, C. (2004). "Olfactory bulb," in The Synaptic Organization of the Brain, 5th Edn., Ed G. Shepherd (New York, NY: Oxford University Press) 165-216.doi: 10.1093/acprof:oso/9780195159561.003.0005
93. Shingo, T., Gregg, C., Enwere, E., Fujikawa, H., Hassam, R., Geary, C., et al. (2003). Pregnancystimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299, 117-120. doi: 10.1126/science.1076647
94. Shipley, M. T., and Ennis, M. (1996). Functional organization of olfactory system. J. Neurobiol. 30, 123-176.
95. Sosulski, D. L., Bloom, M. L., Cutforth, T., Axel, R., and Datta, S. R. (2011). Distinct representations of olfactory information in different cortical centres. Nature 472, 213-216. doi: 10.1038/nature09868
96. Sullivan, R. M., Wilson, D. A. and Leon, M. (1989). Norepinephrine and learning-induced plasticity in infant rat olfactory system. J. Neurosci. 9, 3998-4006.
97. Sultan, S., Mandairon, N., Kermen, F., Garcia, S., Sacquet, J., and Didier, A. (2010). Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J. 24, 2355-2363. doi: 10.1096/fj.09-151456
98. Tononi, G., and Cirelli, C. (2006). Sleep function and synaptic homeostasis. Sleep Med. Rev. 10, 49-62. doi: 10.1016/j.smrv.2005.05.002
99. Tsuno, Y., Kashiwadani, H., and Mori, K. (2008). Behavioral state regulation of dendrodendritic synaptic inhibition in the olfactory bulb. J. Neurosci. 28, 9227-9238. doi: 10.1523/JNEUROSCI.1576-08.2008
100. Veyrac, A., Sacquet, J., Nguyen, V., Marien, M., Jourdan, F., and Didier, A. (2009). Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 34, 786-795. doi: 10.1038/npp.2008.191
101. Vyazovskiy, V. V., Cirelli, C., Pfister-Genskow, M., Faraguna, U., and Tononi, G. (2008). Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci. 11, 200-208. doi: 10.1038/nn2035
102. Wellman, P. J. (2000). Norepinephrine and the control of food intake. Nutrition 16, 837-842. doi: 10.1016/S0899-9007(00)00415-9
103. Whitman, M. C., and Greer, C. A. (2007). Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J. Neurosci. 27, 9951-9961. doi: 10.1523/JNEUROSCI. 1633-07.2007
104. Wilson, D. A. (2010). Single-unit activity in piriform cortex during slow-wave state is shaped by recent odor experience. J. Neurosci. 30, 1760-1765. doi: 10.1523/JNEUROSCI.5636-09.2010
105. Wilson, D. A., and Sullivan, R. M. (2011). Cortical processing of odor objects. Neuron 72, 506-519. doi: 10.1016/j.neuron. 2011.10.027
106. Wilson, M. A., and McNaughton, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679. doi: 10.1126/science.8036517
107. Winner, B., Cooper-Kuhn, C. M., Aigner, R., Winkler, J., and Kuhn, H. G. (2002). Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci. 16, 1681-1689. doi: 10.1046/j.1460-9568.2002.02238.x
108. Yamaguchi, M., and 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. doi: 10.1073/pnas.0406082102
109. Yokoi, M., Mori, K., and Nakanishi, S. (1995). Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 92, 3371-3375. doi: 10.1073/pnas.92.8.3371
110. Yokoyama, T. K., Mochimaru, D., Murata, K., Manabe, H., Kobayakawa, K., Kobayakawa, R., et al. (2011). Elimination of adult-born neurons in the olfactory bulb is promoted during the postprandial period. Neuron 71, 883-897. doi: 10.1016/j.neuron.2011.05.046
111. Young, K. M., Fogarty, M., Kessaris, N., and Richardson, W. D. (2007). Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci. 27, 8286-8296. doi: 10.1523/JNEUROSCI.0476-07.2007