One nose, one brain: Contribution of the main and accessory olfactory system to chemosensation

Frontiers in Neuroanatomy

Volumn , Issue OCTOBER 2012, 2012, Pages

  Mucignat Caretta, Carla ^a   Redaelli, Marco ^a   Caretta, Antonio ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

Nose; Olfaction; Pheromones; Vomeronasal organ

Indexed keywords

CHEMICAL AGENT; GENERAL ODORANT; PHEROMONE; UNCLASSIFIED DRUG;

ACCESSORY OLFACTORY BULB; ACCESSORY OLFACTORY SYSTEM; BRAIN CORTEX; CHEMOSENSITIZATION; HUMAN; MAIN OLFACTORY BULB; MAIN OLFACTORY SYSTEM; MOLECULAR INTERACTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NOSE; ODOR; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY PROCESSING; OLFACTORY SYSTEM; REVIEW; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SMELLING; SOCIAL INTERACTION; SOCIAL ODOR; VOMERONASAL ORGAN;

EID: 84868158598     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2012.00046     Document Type: Review

References (106)

1. Adrian, E. D. (1942). Olfactory reactions in the brain of the hedgehog. J. Physiol., Lond. 100, 459-473.
2. Adrian, E. D. (1955) Synchronised activity in the vomero-nasal nerves with a note on the function of the organ of Jacobsen. Pfluegers Arch. 260, 188-192.
3. Barber, P.C., and Raisman, G. (1974). An autoradiographic investigation of the projection of the vomeronasal organ to the accessory olfactory bulb in the mouse. Brain Res. 81, 21-30.
4. Belluscio, L., Koentges, G., Axel, R., and Dulac, C. (1999). A map of pheromone receptor activation in the mammalian brain. Cell 97, 209-220.
5. Baum, M.J. (2009). Sexual differentiation of pheromone processing: links to male-typical mating behavior and partner preference. Horm. Behav. 55, 579-588.
6. Baum, M.J. (2012). Contribution of pheromones processed by the main olfactory system to mate recognition in female mammals. Front Neuroanat. 6, 20.
7. Bigiani, A., Mucignat-Caretta, C., Montani, G., and Tirindelli, R. (2005). Pheromone reception in mammals. Rev. Physiol. Biochem. Pharmacol. 154, 1-35.
8. Boschat, C., Pelofi, C., Randin, O., Roppolo, D., Luescher, C., Broillet, M.C., and Rodriguez, I. (2002). Pheromone detection mediated by a V1r vomeronasal receptor. Nature Neurosci. 5, 1261-1262.
9. Breer, H., Fleischer, J., and Strotmann, J. (2006). The sense of smell: multiple olfactory subsystems. Cell. Mol. Life Sci. 63,1465-1475.
10. Broman, I. (1920). Das Organon vomero-nasale Jacobsoni-ein Wassergeruchsorgan! Anat. Hefte 174, 137-191.
11. Brechbühl, J., Klaey, M., and Broillet, M.C. (2008). Grueneberg ganglion cells mediate alarm pheromone detection in mice. Science. 321, 1092-1095.
12. Brouette-Lahlou, I., Godinot, F., and Vernet-Maury, E. (1999). The mother rat's vomeronasal organ is involved in detection of dodecyl propionate, the pup's preputial gland pheromone. Physiol. Behav. 66, 427-436.
13. Charra, R., Datiche, F., Casthano, A., Gigot, V., Schaal, B., and Coureaud, G. (2012). Brain processing of the mammary pheromone in newborn rabbits. Behav. Brain Res. 226, 179-188.
14. Choi, G.B., Stettler, D.D., Kallman, B.R., Bhaskar, S.T., Fleischmann, A., and Axel, R. (2011). Driving opposing behaviors with ensembles of piriform neurons. Cell 146, 1004-1015.
15. Coppola, D.M., and O'Connell, R.J. (1989). Stimulus access to olfactory and vomeronasal receptors in utero. Neurosci. Lett. 106, 241-248.
16. Corona, R., Larriva-Sahd, J., and Paredes, R.G. (2011). Paced-mating increases the number of adult new born cells in the internal cellular (granular) layer of the accessory olfactory bulb. PLoS One 6, e19380.
17. De la Rosa-Prieto, C., Ubeda-Banon, I., Mohedano-Moriano, A., Pro-Sistiaga, P., Saiz-Sanchez, D., Insausti, R., and Martinez-Marcos, A. (2009). Subicular and CA1 hippocampal projections to the accessory olfactory bulb. Hippocampus 19, 124-129.
18. Del Punta, K., Leinders-Zufall, T., Rodriguez, I., Jukam, D., Wysocki, C.J., Ogawa, S., Zufall, F., and Mombaerts, P. (2002). Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419, 70-74.
19. Dudley, C.A., and Moss, R.L. (1999). Activation of an anatomically distinct subpopulation of accessory olfactory bulb neurons by chemosensory stimulation. Neuroscience 91, 1549-1556.
20. Eisthen, H.L. (1992). Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates. Micr. Res. Tech. 23, 1-21.
21. Fan, S., Luo, M. (2009). The organization of feedback projections in a pathway important for processing pheromonal signals. Neuroscience 161, 489-500.
22. Fleischer, J., Breer, H., and Strotmann, J. (2009). Mammalian olfactory receptors. Front. Cell. Neurosci. 3, 9.
23. Ghosh, S., Larson, S.D., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K., and Baldwin, K.K. (2011). Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220.
24. Greer, C.A., Stewart, W.B., Teicher, M.H., and Shepherd, G.M. (1982). Functional development of the olfactory bulb and a unique glomerular complex in the neonatal rat. J. Neurosci. 2, 1744-1759.
25. Guillamon, A., and Segovia, S. (1997). Sex differences in the vomeronasal system. Brain Res. Bull. 44, 377-382.
26. Guo, J., Zhou, A., and Moss, R.L. (1997). Urine and urine-derive compounds induce c-fos mRNA expression in accessory olfactory bulb. Neuroreport 8, 1679-1683.
27. He, J., Ma, L., Kim, S.S., Nakai, J., and Yu, C.R. (2008). Encoding gender and individual information in the mouse vomeronasal organ. Science 320, 535-538.
28. Holy, T.E., Dulac, C., and Meister, M. (2000). Responses of vomeronasal neurons to naural stimuli. Science 289, 1569-1572.
29. Hovis, K.R., Ramnath, R., Dahlen, J.E., Romanova, A.L., Larocca, G., Bier, M.E., and Urban, N.N. (2012). Activity regulates functional connectivity from the vomeronasal organ to the accessory olfactory bulb. J. Neurosci. 32, 7907-7916.
30. Illig, K.R. (2007). Developmental changes in odor-evoked activity in rat piriform cortex. Neuroscience 145, 370-376.
31. Inagaki, H., Taniguchi, M., Muramoto, K., Kaba, H., Takeuchi, Y., and Mori, Y. (2010). The effect of vapor of propylene glycol on rats. Chem. Senses 35, 221-228.
32. Inamura, K., Matsumoto, Y., Kashiwayanagi, M., and Kurihara, K. (1999). Laminar distribution of pheromone-receptive neurons in rat vomeronasal epithelium. J. Physiol. 517, 731-739.
33. Jia, C., Chen, W.R., and Shepherd, G.M. (1999). Synaptic Organization and Neurotransmitters in the Rat Accessory Olfactory Bulb. J. Neurophysiol. 81, 345-355.
34. Jakupovic, J., Kang, N., and Baum, M.J. (2008). Effect of bilateral accessory olfactory bulb lesions on volatile urinary odor discrimination and investigation as well as mating behavior in male mice. Physiol. Behav. 93, 467-473.
35. Kang, N., Baum, M.J., and Cherry, J.A. (2009) A direct main olfactory bulb projection to the 'vomeronasal' amygdala in female mice selectively responds to volatile pheromones from males. Eur. J. Neurosci. 29, 624-634.
36. Kawagishi, K., Yokouchi, K., Fukushima, N., Sakamoto, M., Sumitomo, N., Morizumi, T. (2009). Determination of functionally essential neuronal population of the olfactory epithelium for nipple search and subsequent suckling behavior in newborn rats. Brain Res. 1276, 50-57.
37. Keller, M., Baum, M.J., Brock, O., Brennan, P.A., and Bakker, J. (2009). The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav. Brain Res. 200, 268-276.
38. Keller, M., and Lévy, F. (2012). The main but not the accessory olfactory system is involved in the processing of socially relevant chemosignals in ungulates. Front. Neuroanat. 6, 39.
39. Keverne, E.B. (2004). Importance of olfactory and vomeronasal systems for male sexual function. Physiol. Behav. 83, 177-187.
40. Kiyokawa, Y., Kikusui, T., Takeuchi, Y., and Mori, Y. (2007). Removal of the vomeronasal organ blocks the stress-induced hyperthermia response to alarm pheromone in male rats. Chem. Senses 32, 57-64.
41. Kimoto, H., Haga, S., Sato, K., and Touhara, K. (2005). Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437, 898-901.
42. Krieger, J., Schmitt, A., Löbel, D., Gudermann, T., Schultz, G., Breer, H., and Boekhoff, I. (1999). Selective activation of G protein subtypes in the vomeronasal organ upon stimulation with urine-derived compounds. J. Biol. Chem. 274, 4655-4662.
43. Lanuza, E., Novejarque, A., Martínez-Ricós, J., Martínez-Hernández, J., Agustín-Pavón, C., and Martínez-García, F. (2008). Sexual pheromones and the evolution of the reward system of the brain: the chemosensory function of the amygdala. Brain Res. Bull. 75, 460-466.
44. Larriva-Sahd, J. (2008). The accessory olfactory bulb in the adult rat: a cytological study of its cell types, neuropil, neuronal modules, and interactions with the main olfactory system. J. Comp. Neurol. 510, 309-350.
45. Lei, H., Mooney R., and Katz LC. (2006). Synaptic Integration of Olfactory Information in Mouse Anterior Olfactory Nucleus. J. Neurosci. 26, 12023-12032.
46. Leinders-Zufall, T., Lane, A.P., Puche, A.C., Ma, W., Novotny, M.V., Shipley, M.T., and Zufall, F. (2000). Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405, 792-796.
47. Leinders-Zufall, T., Brennan, P., Wildmayer, P., Chandramani, P.S., Maul-Pavicic, A., Jaeger, M., Li, X.H., Breer, H., Zufall, F., and Boehm, T. (2004). MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306, 1033-1037.
48. Lévai, O., Feistel, T., Breer, H., and Strotmann, J. (2006). Cells in the vomeronasal organ express odorant receptors but project to the accessory olfactory bulb. J. Comp. Neurol. 498, 476-490.
49. Lévy, F., and Keller, M. (2009). Olfactory mediation of maternal behavior in selected mammalian species. Behav. Brain Res. 200, 336-345.
50. Liberles, S.D., Horowitz, L.F., Kuang, D., Contos, J.J., Wilson, K.L., Siltberg-Liberles, J., Liberles, D.A., and Buck, L.B. (2009). Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ. Proc. Natl. Acad. Sci. U. S. A. 106, 9842-9847.
51. Licht, G., and Meredith, M. (1987). Convergence of main and accessory olfactory pathways onto single neurons in the hamster amygdala. Exp. Brain Res. 69, 7-18.
52. Luo, M., and Katz, L.C. (2004). Encoding pheromonal signals in the mammalian vomeronasal system. Curr. Opinion Neurobiol. 14, 428-434.
53. Ma, M. (2007). Encoding olfactory signals via multiple chemosensory systems. Crit. Rev. Biochem. Mol. Biol. 42, 463-480.
54. Martel, K.L., and Baum, M.J. (2007). Sexually dimorphic activation of the accessory, but not the main, olfactory bulb in mice by urinary volatiles. Eur. J. Neurosci. 26, 463-475.
55. Martel, K.L., and Baum, M.J. (2009). A centrifugal pathway to the mouse accessory olfactory bulb from the medial amygdala conveys gender-specific volatile pheromonal signals. Eur. J. Neurosci. 29, 368-376.
56. Martínez-García, F., Novejarque, A, and Lanuza, E. (2008). Two interconnected functional systems in the amygdala of amniote vertebrates. Brain Res. Bull. 75, 206-213.
57. Martínez-García, F., Martínez-Ricós, J., Agustín-Pavón, C., Martínez-Hernández, J., Novejarque, A., and Lanuza, E. (2009). Refining the dual olfactory hypothesis: pheromone reward and odour experience. Behav. Brain Res. 200, 277-286.
58. Martinez-Marcos, A. (2009). On the organization of olfactory and vomeronasal cortices. Prog. Neurobiol. 87, 21-30.
59. Martínez-Ricós, J., Agustín-Pavón, C., Lanuza, E., and Martínez-García, F. (2008). Role of the vomeronasal system in intersexual attraction in female mice. Neuroscience 153, 383-395.
60. Masini, C.V., Garcia, R.J., Sasse, S.K., Nyhuis, T.J., Day, H.E., and Campeau, S. (2010). Accessory and main olfactory systems influences on predator odor-induced behavioral and endocrine stress responses in rats. Behav. Brain Res. 207, 70-77.
61. McLean, J.H., Darby-King, A., and Paterno, G.D. (1995). Localization of 5-HT2A receptor mRNA by in situ hybridization in the olfactory bulb of the postnatal rat. J. Comp. Neurol. 353, 371-378.
62. Mendoza, A.S., and Szabo, K. (1988). Developmental studies on the rat vomeronasal organ: vascular pattern and neuroepithelial differentiation. II. Electron microscopy. Dev. Brain Res. 39, 259-268.
63. Meredith, M. (1991) Sensory processing in the main and accessory olfactory systems: comparisons and contrasts. J. Steroid Biochem. Mol. Biol. 39, 601-614.
64. Meredith, M. (1998). Vomeronasal function. Chem. Senses 23, 463-466.
65. Meredith, M., and O'Connell, R.J. (1979). Efferent control of stimulus access to the hamster vomeronasal organ. J. Physiol. 286, 301-316.
66. Miller, S.S., and Spear, N.E. (2008). Olfactory learning in the rat neonate soon after birth. Dev. Psychobiol. 50, 554-565.
67. Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N.R., Taniguchi, H., Tasic, B., Huang, Z.J., He, Z., Callaway, E.M., Horowitz, M.A., and Luo L. (2011). Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191-196.
68. Moffatt, C.A. (2003). Steroid hormone modulation of olfactory processing in the context of socio-sexual behaviors in rodents and humans. Brain Res. Brain Res. Rev. 43, 192-206.
69. Mohedano-Moriano, A., Pro-Sistiaga, P., Ubeda-Bañon, I., de la Rosa-Prieto, C., Saiz-Sanchez, D., and Martinez-Marcos, A. (2008). V1R and V2R segregated vomeronasal pathways to the hypothalamus. Neuroreport 19, 1623-1626.
70. Mohedano-Moriano, A., de la Rosa-Prieto, C., Saiz-Sanchez, D., Ubeda-Bañon, I., Pro-Sistiaga, P., de Moya-Pinilla, M., and Martinez-Marcos, A. (2012). Centrifugal telencephalic afferent connections to the main and accessory olfactory bulbs. Front. Neuroanat. 6, 19.
71. Moriceau, S., Wilson, D.A., Levine, S., and Sullivan, R.M. (2006). Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J. Neurosci. 26, 6737-6748.
72. Mucignat-Caretta, C. (2010). The rodent accessory olfactory system. J. Comp. Physiol. A 196, 767-777.
73. Mucignat-Caretta, C., Caretta, A., and Cavaggioni, A. (1995). Acceleration of puberty onset in female mice by male urinary proteins. J. Physiol. (London) 486, 517-522.
74. Mucignat-Caretta, C., Caretta, A., and Baldini E. (1998). Protein-bound male urinary pheromones: differential responses according to age and gender. Chem. Senses 23, 67-70.
75. Mucignat-Caretta, C., Colivicchi, M.A., Fattori, M., Ballini, C., Bianchi, L., Gabai, G., Cavaggioni, A., Della Corte, L. (2006). Species-specific chemosignals evoke delayed excitation of the vomeronasal amygdala in freely-moving female rats. J. Neurochem. 99, 881-891.
76. Nodari, F., Hsu, F.F., Fu, X., Holekamp, T.F., Kao, L.F., Turk, J., and Holy, T.E. (2008). Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J. Neurosci. 28, 6407-6418.
77. O'Connell, R.J., and Meredith, M. (1984). Effects of volatile and nonvolatile chemical signals on male sex behaviors mediated by the main and accessory olfactory systems. Behav. Neurosci. 98, 1083-1093.
78. Powell, T.P.S., Cowan, W.M., and Raisman, G. (1965). The central olfactory connexions. J. Anat. 99, 791-813.
79. Pro-Sistiaga, P., Mohedano-Moriano, A., Ubeda-Bañon, I., Del Mar Arroyo-Jimenez, M., Marcos, P., Artacho-Pérula, E., Crespo, C., Insausti, R., and Martinez-Marcos, A. (2007). Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J. Comp. Neurol. 504, 346-362.
80. Raisman, G. (1972). An experimental study of the projection of the amygdala to the accessory olfactory bulb and its relationship to the concept of a dual olfactory system. Exp. Brain Res. 14, 395-408.
81. Restrepo, D., Arellano, J., Oliva, A.M., Schaefer, M.L., and Lin, W. (2004). Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice. Horm. Behav. 46, 247-256.
82. Rivière, S., Challet, L., Fluegge, D., Spehr, M., and Rodriguez, I. (2009). Formyl peptide receptorlike proteins are a novel family of vomeronasal chemosensors. Nature 459, 574-577.
83. Salazar, I., and Quinteiro, P.S. (2009). The risk of extrapolation in neuroanatomy: the case of the Mammalian vomeronasal system. Front. Neuroanat. 23, 22.
84. Samuelsen, C.L., and Meredith, M. (2009). The vomeronasal organ is required for the male mouse medial amygdala response to chemical-communication signals, as assessed by immediate early gene expression. Neuroscience 164, 1468-1476.
85. Sanchez-Andrade, G., and Kendrick, K.M. (2009). The main olfactory system and social learning in mammals. Behav. Brain Res. 200, 323-335.
86. Scalia, F., and Winans, S. (1975). The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161, 31-56.
87. Serra, J., Ferreira, G., Mirabito, L., Lévy, F., and Nowak, R. (2009). Post-oral and perioral stimulations during nursing enhance appetitive olfactory memory in neonatal rabbits. Chem. Senses 34, 405-413.
88. Singer, A.G., Macrides, F., Clancy, A.N., and Agosta, W.C. (1986). Purification and analysis of a proteinaceous aphrodisiac pheromone from hamster vaginal discharge. J. Biol. Chem. 261, 13323-13326.
89. 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.
90. Spehr, M., Spehr, J., Ukhanov, K., Kelliher, K.R., Leinders-Zufall, T., and Zufall, F. (2006). Parallel processing of social signals by the mammalian main and accessoryolfactory systems. Cell. Mol. Life Sci. 63, 1476-1484.
91. Sugai, T., Miyazawa, T., Yoshimura, H., and Onoda, N. (2005). Developmental changes in oscillatory and slow responses of the rat accessory olfactory bulb. Neuroscience 134, 605-616.
92. Swaney, W.T., and Keverne, E.B. (2009). The evolution of pheromonal communication. Behav. Brain Res. 200, 239-247.
93. Teicher, M.H., Stewart, W.B., Kauer, J.S., and Shepherd, G.M. (1980). Suckling pheromone stimulation of a modified glomerular region in the developing rat olfactory bulb revealed by the 2-deoxyglucose method. Brain Res. 194, 530-535.
94. Taha, M., McMillon, R., Napier, A., and Wekesa, K.S. (2009). Extracts from salivary glands stimulate aggression and inositol-1, 4, 5-triphosphate (IP3) production in the vomeronasal organ of mice. Physiol. Behav. 98, 147-155.
95. Thompson, R.N., Robertson, B.K., Napier, A., and Wekesa, K.S. (2004). Sex-specific responses to urinary chemicals by the mouse vomeronasal organ. Chem. Senses 29, 749-754.
96. Tirindelli, R., Dibattista, M., Pifferi, S., Menini, A. (2009). From pheromones to behavior. Physiol. Rev. 80, 921-956.
97. Trotier, D., and Doving, K.B. (1998). 'Anatomical description of a new organ in the nose of the domesticated animals' by Ludvig Jacobson (1813). Chem. Senses 23, 743-754.
98. Tucker, D. (1963). Olfactory vomeronasal and trigeminal receptor responses to odorants, in Olfaction and taste, ed. Zotterman, Y. (New York, USA, Macmillan), 45-69.
99. Vandenbergh, J.G., Whitsett, J.M., and Lombardi, J.R. (1975). Partial isolation of a pheromone accelerating puberty in female mice. J. Reprod. Fertil. 43, 515-523.
100. Von Campenhausen, H., and Mori, K. (2000). Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur. J. Neurosci. 12, 33-46.
101. Wacker, D.W., Engelmann, M., Tobin, V.A., Meddle, S.L., and Ludwig, M. (2011). Vasopressin and social odor processing in the olfactory bulb and anterior olfactory nucleus. Ann. N. Y. Acad. Sci. 1220, 106-116.
102. Wagner, S., Gresser, A.L., Torello, A.T., and Dulac, C. (2006). A multireceptor genetic approach uncovers an ordered integration of VNO sensory inputs in the accessory olfactory bulb. Neuron 50, 697-709.
103. Winans, S.S., and Scalia, F. (1970). Amygdaloid nucleus: new afferent input from the vomeronasal organ. Science 170, 330-332.
104. Wysocki, C.J., Wellington, J.L., and Beauchamp, G.K. (1980). Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 207, 781-783.
105. Xu, F., Schaefer, M., Kida, I., Schafer, J., Liu, N., Rothman, D.L., Hyder, F., Restrepo, D., and Shepherd, G.M. (2005). Simultaneous Activation of Mouse Main and Accessory Olfactory Bulbs by Odors or Pheromones. J. Comp. Neurol. 489, 491-500.
106. Zibman, S., Shpak, G., and Wagner, S. (2011). Distinct intrinsic membrane properties determine differential information processing between main and accessory olfactory bulb mitral cells. Neuroscience 189, 51-67.