Integration and sensory experience-dependent survival of newly-generated neurons in the accessory olfactory bulb of female mice

European Journal of Neuroscience

Volumn 29, Issue 4, 2009, Pages 679-692

  Oboti, L ^a   Savalli, G ^a,c   Giachino, C ^a,d   De Marchis, S ^a   Panzica, G C ^b   Fasolo, A ^a   Peretto, P ^a  

^a Department of Animal and Human Biology ^*  (Italy)

^b Department of Anatomy Pharmacology and Forensic Medicine   (Italy)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

Adult neurogenesis; Bedding exposure; Neuronal integration; Pheromones; Vomeronasal system

Indexed keywords

PHEROMONE; VOLATILE AGENT;

ACCESSORY NERVE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EXPERIENCE; FEMALE; GRAFT SURVIVAL; INTEGRATION; INTERNEURON; MALE; MOUSE; NEUROBLAST; NEUROCHEMISTRY; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; SENSORY NERVE CELL; SUBVENTRICULAR ZONE; SURVIVAL TIME;

ANIMALS; BROMODEOXYURIDINE; CELL SURVIVAL; CEREBRAL VENTRICLES; FEMALE; IMAGING, THREE-DIMENSIONAL; MALE; MICE; NEUROGENESIS; NEURONS; OLFACTORY BULB; ORGAN SIZE; PHEROMONES; PHYSICAL STIMULATION; PROSENCEPHALON; PROTO-ONCOGENE PROTEINS C-FOS; SEX CHARACTERISTICS; SMELL; TIME;

EID: 60349114134     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06614.x     Document Type: Article

References (89)

1. Alonso, M., Viollet, C., Gabellec, M.M., Meas-Yedid, V., Olivo-Marin, J.C. Lledo, P.M. (2006) Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci., 26, 10508 10513.
2. Alvarez-Buylla, A. Garcìa-Verdugo, J.M. (2002) Neurogenesis in adult subventricular zone. J. Neurosci., 22, 629 634.
3. Becker, J.B., Arnold, A.P., Berkley, K.J., Blaustein, J.D., Eckel, L.A., Hampson, E., Herman, J.P., Marts, S., Sadee, W., Steiner, M., Taylor, J. Young, E. (2005) Strategies and methods for research on sex differences in brain and behavior. Endocrinology, 146, 1650 1673.
4. Beltramino, C. Taleisnik, S. (1983) Release of LH in the female rat by olfactory stimuli. Effect of the removal of the vomeronasal organs or lesioning of the accessory olfactory bulbs. Neuroendocrinology, 36, 53 58.
5. Bonfanti, L., Peretto, P., Merighi, A. Fasolo, A. (1997) Newly generated cells from the rostral migratory stream in the accessory olfactory bulb of the adult rat. Neuroscience, 81, 489 502.
6. Bredt, D.S., Glatt, C.E., Hwang, P.M., Fothui, M., Dawson, T.M. Snyder, S.H. (1991) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron, 7, 615 624.
7. Brennan, P.A. Kendrick, K.M. (2006) Mammalian social odours: attraction and individual recognition. Philos. Trans. R. Soc. Lond. B Biol. Sci., 361, 2061 2078.
8. Brennan, P.A. Keverne, E.B. (2004) Something in the air? New insights into mammalian pheromones Curr. Biol., 14, R81 R89.
9. Brennan, P.A. Zufall, F. (2006) Pheromonal communication in vertebrates. Nature, 444, 308 315.
10. Broad, K.D. Keverne, E.B. (2008) More to pheromones than meets the nose. Nat. Neurosci., 11, 128 129.
11. Brown, J., Cooper-Kuhn, C.M., Kempermann, G., Van Praag, H., Winkler, J., Gage, F.H. Kuhn, H.G. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci., 17, 2042 2046.
12. Bruce, H.M. (1959) An exteroceptive block to pregnancy in the mouse. Nature, 184, 105.
13. Buonviso, N. Chaput, M. (2000) Olfactory experience decreases responsiveness of the olfactory bulb in the adult rat. Neuroscience, 95, 325 332.
14. Carletti, B., Grimaldi, P., Magrassi, L. Rossi, F. (2002) Specification of cerebellar progenitors after heterotopic-heterochronic transplantation to the embryonic CNS in vivo and in vitro. J. Neurosci., 15, 7132 7146.
15. Cajal, S.R.Y. (1901) Textura del lobulo olfativo accessorio. Rev. Trimest. Micrografica., 1, 141 150.
16. Chamero, P., Marton, T.F., Logan, D.W., Flanagan, K., Cruz, J.R., Saghatelian, A., Cravett, B.F. Stowers, L. (2007) Identification of protein pheromones that promote aggressive behaviour. Nature, 450, 899 902.
17. Champlin, A.K. (1971) Suppression of oestrus in grouped mice: the effects of various densities and the possible nature of the stimulus. J. Reprod. Fertil., 27, 233 241.
18. Collado, P., Guillamon, A., Valencia, A. Segovia, S. (1990) Sexual dimorphism in the bed nucleus of the accessory olfactory tract in the rat. Brain Res. Dev. Brain Res., 56, 263 268.
19. Conklin, B.R. Bourne, H.R. (1993) Structural elements of G alpha subunits that interact with G beta gamma, receptors, and effectors. Cell, 73, 631 641.
20. Coppola, D.M. O'Connel, R.J. (1988) Behavioural responses of peripubertal female mice towards puberty-accelerating and puberty-delaying chemical signals. Chem. Senses., 13, 407 424.
21. Corotto, F.S., Heneqar, J.N. Maruniak, J.A. (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience, 61, 739 744.
22. Cummings, D.M., Knab, B.R. Brunjes, P.C. (1997b) Effects of unilateral olfactory deprivation in the developing opossum, Monodelphis domestica. J. Neurobiol., 33, 429 438.
23. Czaja, K., Lakomy, M., Kaleczyc, J., Barb, C.R., Rampacek, G.B. Kraeling, R.R. (2002) Leptin receptors, NPY, and tyrosine hydroxylase in autonomic neurons supplying fat depots in a pig. Biochem. Biophys. Res. Commun., 293, 1138 1144.
24. Dawley, E.M. Crowder, J. (1995) Sexual and seasonal differences in the vomeronasal epithelium of the red-backed salamander (Plethodon cinereus). J. Comp. Neurol., 359, 382 390.
25. De Marchis, S., Fasolo, A., Shipley, M. Puche, A. (2001) Unique neuronal tracers show migration and differentiation of SVZ progenitors in organotypic slices. J. Neurobiol., 49, 326 338.
26. De Marchis, S., Bovetti, S., Carletti, B., Hsieh, Y.C., Garzotto, D., Peretto, P., Fasolo, A., Puche, A.C. Rossi, F. (2007) 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., 27, 657 664.
27. Dhaka, A., Earley, T.J., Watson, J. Patapoutian, A. (2008) Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J. Neurosci., 28, 566 575.
28. Doetsch, F. Hen, R. (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr. Opin. Neurobiol., 15, 121 128.
29. Drickamer, L.C. (1989) Odor preferences of wild stock female house mice (Mus domesticus) tested at three ages using urine and other cues from conspecific males and females. J. Chem. Ecol., 15, 1971 1987.
30. Dudley, C.A. Moss, R.L. (1999) Activation of an anatomically distinct subpopulation of accessory olfactory bulb neurons by chemosensory stimulation. Neuroscience, 91, 1549 1556.
31. Dulac, C. Torello, A.T. (2003) Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci., 4, 551 562.
32. Ernst, C. Christie, B.R. (2005) Nestin-expressing cells and their relationship to mitotically active cells in the subventricular zones of the adult rat. Eur. J. Neurosci., 22, 3059 3066.
33. Giachino, C., De Marchis, S., Giampietro, C., Parlato, R., Perroteau, I., Schütz, G., Fasolo, A. Peretto, P. (2005) cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J. Neurosci., 25, 10105 10118.
34. Goldman, J.M., Murr, A.S. Cooper, R.L. (2007) The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth. Defects. Res., 80, 84 87.
35. Gotti, S., Sica, M., Viglietti-Panzica, C. Panzica, G. (2005) Distribution of nitric oxide synthase immunoreactivity in the mouse brain. Microsc. Res. Tech., 68, 13 35.
36. Guillamon, A. Segovia, S. (1997) Sex differences in the vomeronasal system. Brain Res. Bull., 44, 377 382.
37. Huang, L. Bittman, E.L. (2002) Olfactory bulb cells generated in adult male golden hamsters are specifically activated by exposure to estrous females. Horm. Behav., 41, 343 350.
38. Kee, N., Teixeira, C.M., Wang, A.H. Frankland, P.W. (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci., 10, 355 362.
39. Kendrick, K.M., Guevara-Guzman, R., Zorrilla, J., Hinton, M.R., Broad, K.D., Mimmack, M. Ohkura, S. (1997) Formation of olfactory memories mediated by nitric oxide. Nature, 388, 670 674.
40. Keverne, E.B. (2004) Importance of olfactory and vomeronasal systems for male sexual function. Physiol. Behav., 83, 177 187.
41. Larsen, C.M., Kokay, I.C. Grattan, D.R. (2008) Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Horm. Behav., 53, 509 517.
42. Lau, Y.E. Cherry, J.A. (1999) Distribution of PDE4A and Ga0 immunoreactivity in the accessory olfactory system of the mouse. Neuroreport, 11, 27 33.
43. Leinders-Zufall, T., Lane, A.P., Puche, A.C., Ma, W., Novotny, M.V., Shipley, M.T. Zufall, F. (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature, 405, 792 796.
44. Lindholm, P., Voutilainen, M.H., Laurén, J., Peränen, J., Leppänen, V.M., Andressoo, J.O., Lindahl, M., Janhunen, S., Kalkkinen, N., Timmusk, T., Tuominen, R.K. Saarma, M. (2007) Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature, 448, 73 77.
45. Lois, C. Alvarez-Buylla, A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science, 264, 1145 1148.
46. Lonze, B.E. Ginty, D.D. (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron, 35, 605 623.
47. Luskin, M.B. (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 11, 173 189.
48. Luzzati, F., De Marchis, S., Fasolo, A. Peretto, P. (2006) Neurogenesis in the caudate nucleus of the adult rabbit. J. Neurosci., 26, 609 621.
49. Ma, W., Miao, Z. Novotny, M.V. (1998) Role of the adrenal gland and adrenal-mediated chemosignals in suppression of estrus in the house mouse: the lee-boot effect revisited. Biol. Reprod., 59, 1317 1320.
50. Magavi, S.S., Mitchell, B.D., Szentirmai, O., Carter, B.S. Macklis, J.D. (2005) Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J. Neurosci., 25, 10729 10739.
51. Mak, G.K., Enwere, E.K., Gregg, C., Pakarainen, T., Poutanen, M., Huhtaniemi, I. Weiss, S. (2007) Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behaviour. Nat. Neurosci., 10, 1003 1011.
52. Mansfield, J., Quan, W., Jia, C. Halpern, M. (1996) Sexual dimorphism in the vomeronasal system of the gray-short-tailed opossum, Monodelphis domestica. Chem. Senses., 21, 638.
53. Martinez-Marcos, A., Ubeda-Banon, I. Halpern, M. (2001) Cell migration to the anterior and posterior divisions of the granule cell layer of the accessory olfactory bulb of adult opossums. Brain Res. Dev. Brain Res., 127, 95 98.
54. Merkle, F.T., Mirzadeh, Z. Alvarez-Buylla, A. (2007) Mosaic organization of neural stem cells in the adult brain. Science, 317, 381 384.
55. Mogi, K., Sakurai, K., Ichimaru, T., Ohkura, S., Mori, Y. Okamura, H. (2007) Structure and chemical organization of the accessory olfactory bulb in the goat. Anat. Rec., 290, 301 310.
56. Moncho-Bogani, J., Lanuza, E., Hernández, A., Novejarque, A. Martínez-García, F. (2002) Attractive properties of sexual pheromones in mice: innate or learned? Physiol. Behav., 77, 167 176.
57. Moreno-López, B., Noval, J.A., González-Bonet, L.G. Estrada, C. (2000) Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res., 869, 244 250.
58. Mugnaini, E., Oertel, W.H. Wouterlood, F.F. (1984) Immunocytochemical localization of GABA neurons and dopamine neurons in the rat main and accessory olfactory bulbs. Neurosci. Lett., 47, 221 226.
59. Mullen, R.J., Buck, C.R. Smith, A.M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116, 201 211.
60. Muroi, Y., Ishii, T., Komori, S. Nishimura, M. (2006) A competitive effect of androgen signaling on male mouse attraction to volatile female mouse odors. Physiol. Behav., 87, 199 205.
61. Nakagawa, S., Kim, J.E., Lee, R., Chen, J., Fujioka, T., Malberg, J., Tsuji, S. Duman, R.S. (2002b) Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J. Neurosci., 22, 9868 9876.
62. Nakajima, T., Sakaue, M., Kato, M., Saito, S., Ogawa, K. Taniguchi, K. (1998) Immunohistochemical and enzyme-histochemical study on the accessory olfactory bulb in the dog. Anat. Rec., 252, 393 402.
63. Nelson, R.J. (1997) Effect of nitric oxide on neuroendocrine function and behaviour. Front. Neuroendocrinol., 18, 463 491.
64. Nishizawa, M., Goto, N. Kawai, S. (1987) An avian transforming retrovirus isolated from a nephroblastoma that carries the fos gene as the oncogene. J. Virol., 61, 3733 3740.
65. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. Nishimune, Y. (1997) Green mice as a source of ubiquitous green cells. FEBS Lett., 407, 313 319.
66. Okere, C.O., Kaba, H. Higuchi, T. (1995) Failure of intrabulbar and peripheral administration of N omega-nitro-L-arginine to prevent the formation of an olfactory memory in mice. Physiol. Behav., 58, 387 391.
67. Peretto, P., Giachino, C., Panzica, G.C. Fasolo, A. (2001) Sexually dimorphic neurogenesis is topographically matched with the anterior accessory olfactory bulb of the adult rat. Cell Tissue Res., 306, 385 389.
68. Petreanu, L. Alvarez-Buylla, A. (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci., 22, 6106 6113.
69. Pfannkuche, H., Reiche, D., Firzlaff, U., Sann, H. Schemann, M. (1998) Enkephalin-immunoreactive subpopulations in the myenteric plexus of the guinea-pig fundus project primarily to the muscle and not to the mucosa. Cell Tissue Res., 294, 45 55.
70. Ponti, G., Peretto, P. Bonfanti, L. (2008) Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS ONE, 3, e2366.
71. Porteros, A., Alonso, J.R., Arevaldo, R., Garcia-Ojeda, E., Crespo, C. Aijòn, J. (1994) Histochemical localization of NADPH-diaphorase in the rat accessory olfactory bulb. Chem. Senses., 19, 413 424.
72. Qin, Z.P., Ye, S.M., Du, J.Z. Shen, G.Y. (2005) Postnatal developmental expression of calbindin, calretinin and parvalbumin in mouse main olfactory bulb. Acta Biochim. Biophys. Sin., 37, 276 282.
73. Rochefort, C., Gheusi, G., Vincent, J.D. 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.
74. Salazar, I. Brennan, P.A. (2001) Retrograde labelling of mitral/tufted cells in the mouse accessory olfactory bulb following local injections of the lipophilic tracer DiI into the vomeronasal amygdale. Brain Res., 896, 198 203.
75. Schaefer, M.L., Yamazaki, K., Osada, K., Restrepo, D. Beauschamp, G.K. (2002) Olfactory fingerprints for major histocompatibility complex-determined body odors II: relationship among odor maps, genetics, odor composition and behaviour. J. Neurosci., 22, 9513 9521.
76. Schwaller, B., Buchwald, P., Blümcke, I., Celio, M.R. Hunziker, W. (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium, 14, 639 648.
77. Segovia, S. Guillamon, A. (1996) Searching for sex differences in the vomeronasal pathway. Horm. Behav., 30, 618 626.
78. Segovia, S., Orensanz, L.M., Valencia, A. Guillamon, A. (1984) Effects of sex steroids on the development of the accessory olfactory bulb in the rat: a volumetric study. Dev. Brain Res., 16, 312 314.
79. Segovia, S., Guillamon, A., Del Cerro, M.C.R., Ortega, E., Pérez-Laso, C., Rodriguez-Zafra, M. Beyer, C. (1999) The development of brain sex differences: a multisignaling process. Behav. Brain Res., 105, 69 80.
80. Segovia, S., Garcia-Falgueras, A., Carrello, B., Collado, P., Pinos, H., Perez-Laso, C., Vinader-Caerols, C. Guillamon, A. (2006) Sexual dimorphism in the vomeronasal system of the rabbit. Brain Res., 1102, 52 62.
81. Simmons, A.M. Chapman, J.A. (2002) Metamorphic Changes in GABA Immunoreactivity in the Brainstem of the Bullfrog, Rana catesbeiana. Brain Behav. Evol., 60, 189 206.
82. Trinh, K. Storm, D.R. (2003) Vomeronasal organ detects odorants in absence of signalling through the main olfactory epithelium. Nat. Neurosci., 6, 519 525.
83. Vandenbergh, J.G. (1976) Acceleration of sexual maturation in female rats by male stimulation. J. Reprod. Fertil., 46, 451 453.
84. Varea, E., Nácher, J., Blasco-Ibáñez, J.M., Gómez-Climent, M.A., Castillo-Gómez, E., Crespo, C. Martínez-Guijarro, F.J. (2005) PSA-NCAM expression in the rat medial prefrontal cortex. Neuroscience, 136, 435 443.
85. Vinader-Caerols, C., Collado, P., Segovia, S. Guillamon, A. (1998) Sex differences in the posteromedial cortical nucleus of the amygdala in the rat. Neuroreport, 9, 2653 2656.
86. Weissmann, D., Labatut, R., Gillon, J., Richard, F. Pujol, J. (1988) Measurement of brain tyrosine hydroxylase concentrations by quantitative autoradiography after transfer of soluble proteins to nitro-cellulose. C. R. Acad. Sci. III, 306, 457 460.
87. Whitten, W.K. (1956) Modification of the estrous cycle of the mouse by external stimuli associated with the male. J. Endocrinol., 13, 399 404.
88. Winner, B., Cooper-Kuhn, C.M., Aigner, R., Winkler, J. 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.
89. Xu, F., Schaefer, M., Kida, I., Schafer, J., Liu, N., Rothman, D.L., Hyder, F., Restrepo, D. Shepherd, G.M. (2005) Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J. Comp. Neurol., 489, 491 500.