Centrifugal telencephalic afferent connections to the main and accessory olfactory bulbs

Frontiers in Neuroanatomy

Volumn , Issue MAY, 2012, Pages

  Mohedano Moriano, Alicia ^a   de la Rosa Prieto, Carlos ^b   Saiz Sanchez, Daniel ^b   Ubeda Bañon, Isabel ^b   Pro Sistiaga, Palma ^c   de Moya Pinilla, Miguel ^b   Martinez Marcos, Alino ^b  

^a Universidad de Castilla La Mancha   (Spain)

^b UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^c GIP CYCERON   (France)

Author keywords

Chemical senses; Olfactory system; Tract tracing; Vomeronasal system

Indexed keywords

NEURONAL TRACT TRACER;

ACCESSORY OLFACTORY BULB; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL LABELING; CORTICAL AMYGDALA; FEMALE; MAIN OLFACTORY BULB; MALE; MEDIAL AMYGDALA; MOUSE; NEUROANATOMY; NEUROMODULATION; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; PYRIFORM CORTEX; RAT; SENSORY NERVE; TELENCEPHALON; VOMERONASAL ORGAN;

EID: 84863112066     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2012.00019     Document Type: Article

References (83)

1. Barber, P. C. (1982). Adjacent laminar terminations of two centrifugal afferent pathways to the accessory olfactory bulb in the mouse. Brain Res. 245,215-221.
2. Barber, P. C., and Field, P. M. (1975). Autoradiographic demonstration of afferent connections of the accessory olfactory bulb in the mouse. Brain Res. 85, 201-203.
3. Belluscio, L., Koentges, G., Axel, R., and Dulac, C. (1999). A map of pheromone receptor activation in the mammalian brain. Cell 97, 209-220.
4. Berghard, A., and Buck, L. B. (1996). Sensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J. Neurosci. 16, 909-918.
5. Brennan, P., Kaba, H., and Keverne, E. B. (1990). Olfactory recognition: a simple memory system. Science 250, 1223-1226.
6. Broadwell, R. D., and Jacobowitz, D. M. (1976). Olfactory relationships of the telencephalon and diencephalon in the rabbit. III. The ipsilateral centrifugal fibers to the olfactory bulbar and retrobulbar formations. J. Comp. Neurol. 170, 321-345.
7. Carmichael, S. T., Clugnet, M. C., and Price, J. L. (1994). Central olfactory connections in the macaque monkey. J. Comp. Neurol. 346, 403-434.
8. Cenquizca, L. A., and Swanson, L. W. (2007). Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res. Rev. 56, 1-26.
9. Davis, B. J., Macrides, F., Youngs, W. M., Schneider, S. P., and Rosene, D. L. (1978). Efferents and centrifugal afferents of the main and accessory olfactorybulbs inthe hamster. Brain Res. Bull. 3, 59-72.
10. 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.
11. de Olmos, J., Hardy, H., and Heimer, L. (1978). The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J. Comp. Neurol. 181, 213-244.
12. Devor, M. (1976). Fiber trajectories of olfactory bulb efferents in the hamster. J. Comp. Neurol. 166, 31-47.
13. Dulac, C., and Axel, R. (1995). A novel family of genes encoding putative pheromone receptors in mammals. Cell 83, 195-206.
14. Fan, S., and Luo, M. (2009). The organization of feedback projections in a pathway important for processing pheromonal signals. Neuroscience 161, 489-500.
15. Fletcher, M. L., and Chen, W. R. (2010). Neural correlates of olfactory learning: critical role of centrifugal neuromodulation. Learn. Mem. 17, 561-570.
16. Franklin, K.B.J., and Paxinos, G. (2008). The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
17. Gutierrez-Castellanos, N., Martinez-Marcos, A., Martinez-Garcia, F., and Lanuza, E. (2010). Chemosensory function of the amygdala. Vitam. Horm. 83, 165-196.
18. Halpern, M. (1987). The organization and function of the vomeronasal system. Annu. Rev. Neurosci. 10, 325-362.
19. Halpern, M., Jia, C., and Shapiro, L.S. (1998a). Segregated pathways in the vomeronasal system. Microsc. Res. Tech. 41, 519-529.
20. Halpern, M., and Martinez-Marcos, A. (2003). Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70, 245-318.
21. Halpern, M., Shapiro, L.S., and Jia, C. (1998b). Heterogeneityin the accessory olfactory system. Chem. Senses 23, 477-481.
22. Herrada, G., and Dulac, C. (1997). A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90, 763-773.
23. Jansen, H. T., Iwamoto, G. A., and Jackson, G. L. (1998). Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res.Bull. 45, 27-39.
24. Jia, C., and Halpern, M. (1996). Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res. 719, 117-128.
25. 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.
26. Kang, N., Baum, M.J., and Cherry, J. A. (2011a). Different profiles of main and accessory olfactory bulb mitral/tufted cell projections revealed in mice using an antero-grade tracer and a whole-mount, flattened cortex preparation. Chem.Senses 36, 251-260.
27. Kang, N., McCarthy, E. A., Cherry, J. A., and Baum, M. J. (2011b). A sex comparison of the anatomy and function of the main olfactory bulb-medial amygdala projection in mice. Neuroscience 172, 196-204.
28. 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.
29. Keverne, E. B., and Brennan, P. A. (1996). Olfactoryrecognition memory. J. Physiol. Paris 90, 399-401.
30. Kiselycznyk, C. L., Zhang, S., and Linster, C. (2006). Role of centrifugal projections to the olfactory bulb in olfactoryprocessing. Learn. Mem. 13, 575-579.
31. Kosel, K. C., Van Hoesen, G. W., and West, J. R. (1981). Olfactory bulb projections to the parahippocampal area of the rat. J. Comp. Neurol. 198, 467-482.
32. Kunze, W. A., Shafton, A. D., Kem, R. E., and McKenzie, J. S. (1992). Intracellular responses of olfactory bulb granule cells to stimulating the horizontal diagonal band nucleus. Neuroscience 48, 363-369.
33. 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.
34. Leinders-Zufall, T., Brennan, P., Widmayer, P., Chandramani, P., Maul-Pavicic, A., Jager, 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.
35. 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.
36. 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.
37. Lin, W., Arellano, J., Slotnick, B., and Restrepo, D. (2004). Odors detected by mice deficient in cyclic nucleotide-gated channel subunit A2 stimulate the main olfactory system. J. Neurosci. 24, 3703-3710.
38. 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.
39. Macrides, F., Davis, B. J., Youngs, W. M., Nadi, N. S., and Margolis, F. L. (1981). Cholinergic and cat-echolaminergic afferents to the olfactory bulb in the hamster: a neuroanatomical, biochemical, and histochemical investigation. J. Comp. Neurol. 203, 495-514.
40. 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.
41. Martinez-Marcos, A. (2009). On the organization of olfactory and vomeronasal cortices. Prog. Neurobiol. 87, 21-30.
42. Martinez-Marcos, A., and Halpern, M. (1999a). Differential centrifugal afferents to the anterior and posterior accessory olfactory bulb. Neuroreport 10, 2011-2015.
43. Martinez-Marcos, A., and Halpern, M. (1999b). Differential projections from the anterior and posterior divisions of the accessory olfactory bulb to the medial amygdala in the opossum, Monodelphis domes-tica. Eur. J. Neurosci. 11, 3789-3799.
44. Martinez-Marcos, A., and Halpern, M. (2006). Efferent connections of the main olfactory bulb in the opossum (Monodelphis domestica): a characterization of the olfactory entorhi-nal cortex in a marsupial. Neurosci. Lett. 395, 51-56.
45. Matsunami, H., and Buck, L. B. (1997). A multigene family encoding a diversearrayofputativepheromone receptors in mammals. Cell 90, 775-784.
46. Matsutani, S., and Yamamoto, N. (2008). Centrifugal innervation of the mammalian olfactory bulb. Anat. Sci. Int. 83, 218-227.
47. Meyer, R. P. (1981). Central connections of the olfactory bulb in the American opossum (Didelphys virginiana): a light microscopic degeneration study. Anat. Rec. 201, 141-156.
48. Mohedano-Moriano, A., Martinez-Marcos, A., Munoz, M., Arroyo-Jimenez, M. M., Marcos, P., Artacho-Perula, E., Blaizot, X., and Insausti, R. (2005). Reciprocal connections between olfactory structures and the cortex of the rostral superior temporal sulcus in the Macaca fascicularis monkey. Eur. J. Neurosci. 22, 2503-2518.
49. Mohedano-Moriano, A., Pro-Sistiaga, P., Ubeda-Banon, I., Crespo, C., Insausti, R., and Martinez-Marcos, A. (2007). Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur. J. Neurosci. 25, 2065-2080.
50. Mohedano-Moriano, A., Pro-Sistiaga, P., Ubeda-Banon, 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.
51. Mouret, A., Murray, K., and Lledo, P. M. (2009). Centrifugal drive onto local inhibitory interneurons of the olfactory bulb. Ann. N.Y. Acad. Sci. 1170, 239-254.
52. Mucignat-Caretta, C. (2010). The rodent accessory olfactory system. J. Comp. Physiol. ANeuroethol. Sens. Neural Behav. Physiol. 196, 767-777.
53. Oboti, L., Schellino, R., Giachino, C., Chamero, P., Pyrski, M., Leinders-Zufall, T., Zufall, F., Fasolo, A., and Peretto, P. (2011). Newborn interneurons in the accessory olfactory bulb promote mate recognition in female mice. Front. Neurosci. 5:113. doi: 10.3389/fnins.2011.00113
54. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. Amsterdam: Academic Press.
55. Peele, P., Salazar, I., Mimmack, M., Keverne, E. B., and Brennan, P. A. (2003). Low molecular weight constituents of male mouse urine mediate the pregnancy block effect and convey information about the identity of the mating male. Eur. J. Neurosci. 18, 622-628.
56. Price, J. L., and Powell, T. P. (1970). An experimental study of the origin and the course of the centrifugal fibres to the olfactory bulb in the rat. J. Anat. 107, 215-237.
57. Pro-Sistiaga, P., Mohedano-Moriano, A., Ubeda-Banon, I., de la Rosa-Prieto, C., Saiz-Sanchez, D., and Martinez-Marcos, A. (2008). Projections of olfactory bulbs to the olfactory and vomeronasal cortices. Neuroreport 19, 1541-1544.
58. Pro-Sistiaga, P., Mohedano-Moriano, A., Ubeda-Banon, I., del Mar Arroyo-Jimenez, M., Marcos, P., Artacho-Perula, 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.
59. 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.
60. 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.
61. Rodriguez, I., Feinstein, P., and Mombaerts, P. (1999). Variable pat-ternsofaxonalprojectionsofsensory neurons in the mouse vomeronasal system. Cell 97, 199-208.
62. Ryba, N. J., and Tirindelli, R. (1997). A new multigene family of putative pheromone receptors. Neuron 19, 371-379.
63. Salazar, I., and Brennan, P. A. (2001). Retrograde labelling ofmitral/tufted cells in the mouse accessory olfactory bulb following local injections of the lipophilic tracer DiI into the vomeronasal amygdala. Brain Res. 896, 198-203.
64. Scalia, F., and Winans, S. S. (1975). The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161, 31-55.
65. Scott, J. W., McBride, R. L., and Schneider, S. P. (1980). The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J. Comp. Neurol. 194, 519-534.
66. Shammah-Lagnado, S. J., and Negrao, N. (1981). Efferent connections of the olfactory bulb in the opossum (Didelphis marsupialis aurita): a Fink-Heimer study. J. Comp. Neurol. 201, 51-63.
67. Shipley, M.T., and Adamek, G.D. (1984). The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res. Bull. 12, 669-688.
68. Skeen, L. C., and Hall, W. C. (1977). Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis). J. Comp. Neurol. 172, 1-35.
69. Spehr, M., Kelliher, K. R., Li, X. H., Boehm, T., Leinders-Zufall, T., and Zufall, F. (2006a). Essential role of the main olfactory system in social recognition of major histo-compatibility complex peptide lig-ands. J. Neurosci. 26, 1961-1970.
70. Spehr, M., Spehr, J., Ukhanov, K., Kelliher, K. R., Leinders-Zufall, T., and Zufall, F. (2006b). Parallel processing of social signals by the mammalian main and accessory olfactory systems. Cell. Mol. Life Sci. 63, 1476-1484.
71. Taniguchi, K., and Saito, S. (2011). Phylogenic outline of the olfactory system in vertebrates. J. Vet. Med. Sci. 73, 139-147.
72. Trinh, K., and Storm, D. R. (2004). Detection of odorants through the main olfactory epithelium and vomeronasal organ of mice. Nutr. Rev. 62, S189-S192.discussion S224-S241.
73. Turner, B.H., Gupta, K.C., and Mishkin, M. (1978). The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta. J. Comp. Neurol. 177, 381-396.
74. Ubeda-Banon, I., Novejarque, A., Mohedano-Moriano, A., Pro-Sistiaga, P., de la Rosa-Prieto, C., Insausti, R., Martinez-Garcia, F., Lanuza, E., and Martinez-Marcos, A. (2007). Projections from the posterolateral olfactory amygdala to the ventral striatum: neural basis for reinforcing properties of chemical stimuli. BMC Neurosci. 8, 103.
75. Ubeda-Banon, I., Novejarque, A., Mohedano-Moriano, A., Pro-Sistiaga, P., Insausti, R., Martinez-Garcia, F., Lanuza, E., and Martinez-Marcos, A. (2008). Vomeronasal inputs to the rodent ventral stria-tum. Brain Res. Bull. 75, 467-473.
76. Ubeda-Banon, I., Pro-Sistiaga, P., Mohedano-Moriano, A., Saiz-Sanchez, D., delaRosa-Prieto, C., Gutierrez-Castellanos, N., Lanuza, E., Martinez-Garcia, F., and Martinez-Marcos, A. (2011). Cladistic analysis of olfactory and vomeronasal systems. Front. Neuroanat. 5:3. doi: 10.3389/fnana.2011.00003
77. 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.
78. Wang, Z., Balet Sindreu, C., Li, V., Nudelman, A., Chan, G. C., and Storm, D. R. (2006). Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J. Neurosci. 26, 7375-7379.
79. 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.
80. Winans, S. S., and Scalia, F. (1970). Amygdaloid nucleus: new afferent input from the vomeronasal organ. Science 170, 330-332.
81. 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.
82. Zaborszky, L., Carlsen, J., Brashear, H. R., and Heimer, L. (1986). Cholinergic and GABAergic affer-ents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J. Comp. Neurol. 243, 488-509.
83. Zheng, L. M., Ravel, N., and Jourdan, F. (1987). Topographyofcentrifugal acetylcholinesterase-positive fibres in the olfactory bulb of the rat: evidence for original projections in atypical glomeruli. Neuroscience 23, 1083-1093.