Phylogenic outline of the olfactory system in vertebrates

Journal of Veterinary Medical Science

Volumn 73, Issue 2, 2011, Pages 139-147

  Taniguchi, Kazumi ^a   Saito, Shouichiro ^b   Taniguchi, Kazuyuki ^c  

^a KITASATO UNIVERSITY   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c IWATE UNIVERSITY   (Japan)

Author keywords

Monophyletic; Olfactory system; Paraphyletic; Phylogeny; Vomeronasal system

Indexed keywords

ANIMAL; GENETICS; HISTOLOGY; OLFACTORY SYSTEM; PHYLOGENY; REVIEW; VERTEBRATE;

ANIMALS; OLFACTORY PATHWAYS; PHYLOGENY; VERTEBRATES;

AMPHIBIA; AVES; MAMMALIA; REPTILIA; VERTEBRATA;

EID: 79952609272     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.10-0316     Document Type: Review

References (103)

1. Adams, D. R. 1986. The bovine vomeronasal organ. Arch. Histol. Jpn. 49: 211-225.
2. Adams, D. R. and McFarland, L. Z. 1971. Septal olfactory organ in Peromyscus. Comp. Biochem. Physiol. 40A: 971-974.
3. Adams, D. R. and Wiekamp, M. D. 1984. The canine vomeronasal organ. J. Anat. 138: 771-790.
4. Barber, P. C. and Raisman, G. 1974. An autoradiographic investigation of the projection of the vomeronasal organ to the accessory olfactory bulb in the house mouse. Brain Res. 81: 21-30.
5. Beauchamp, G. K., Magnus, J. G., Shmunes, N. T. and Durham, T. 1977. Effects of olfactory bulbectomy on social behavior of male guinea pigs (Cavia porcellus). J. Comp. Physiol. Psych. 91: 336-346.
6. Bedini, C., Fiaschi, V. and Lanfranchi, A. 1976. Olfactory nerve reconstitution in the homing pigeon after resection: ultrastructural and electrophysiological data. Arch. Ital. Biol. 114: 1-22.
7. Bertmar, G. 1981. Evolution of vomeronasal organs in vertebrates. Evolution 35: 359-366.
8. Bhatnagar, K. P., Matulionis, D. and Breipohl, W. 1982. Fine structure of the vomeronasal neuroepithelium of bats. A comparative study. Acta Anat. 112: 158-177.
9. Brechbühl, J., Klaey, M. and Broillet, M. C. 2008. Grueneberg ganglion cells mediate alarm pheromone detection in mice. Science 321: 1092-1095.
10. Breipohl, W., Naguro, T. and Walker, D. G. 1989. The postnatal development of Masera's organ in the rat. Chem. Senses 14: 649-662.
11. Ciges, M., Labella, T., Gayoso, M. and Sanchez, G. 1977. Ultrastructure of the organ of Jacobson and comparative study with olfactory mucosa. Acta Otolaryngol. (Stockh.) 83: 47-58.
12. Clancy, A. N., Coquelin, A., Macrides, F., Gorski, R. A. and Noble, E. P. 1984. Sexual behavior and aggression in male mice: involvement of the vomeronasal system. J. Neurosci. 4: 2222-2229.
13. Cooper, J. G. and Bhatnagar, K. P. 1976. Comparative anatomy of the vomeronasal organ complex in bats. J. Anat. 122: 571-601.
14. Costanzo, R. M. and Morrison, E. E. 1989. Three-dimensional scanning electron microscopic study of the normal hamster olfactory epithelium. J. Neurocytol. 18: 381-391.
15. Cushieri, A. 1974. Enzyme histochemistry of the olfactory mucosa and vomeronasal organ in the mouse. J. Anat. 118: 477-490.
16. Eisthen, H. L., Wysocki, C. J. and Beauchamp, G. K. 1987. Behavioral responses of male guinea pigs to conspecific chemical signals following neonatal vomeronasal organ removal. Physiol. Behav. 41: 445-449.
17. Eloff, F. C. 1951. On the organ of Jacobson and the nasal floor cartilage in the chondrocranium of Galago senegalensis. Proc. Zool. Soc. Lond. 121: 651-655.
18. Estes, R. D. 1972. The role of the vomeronasal organ in mammalian reproduction. Mammalia 36: 315-341.
19. Farbman, A. and Margolis, F. 1980. Olfactory marker protein during ontogeny: immunohistochemical localization. Dev. Biol. 74: 205-215.
20. Fleischer, J., Schwarzenbacher, K., Besser, S., Hass, N. and Breer, H. 2006. Olfactory receptors and signalling elements in the Grueneberg ganglion. J. Neurochem. 98: 543-554.
21. Fleischer, J. and Breer, H. 2010. The Grueneberg ganglion: a novel sensory system in the nose. Histol. Histopathol. 25: 909-915.
22. Fleming, A., Vaccarino, F., Tambossee, L. and Chee, P. 1979. Vomeronasal and olfactory modulation of maternal behavior in the rat. Science 203: 372-374.
23. Franceschini, V., Lazzari, M., Revoltella, R. P. and Ciani, F. 1994. Histochemical study by lectin binding of surface glycoconjugates in the developing olfactory system of rat. Int. J. Devl. Neurosci. 12: 197-206.
24. Freitag, J., Krieger, J., Strotmann, J. and Breer, H. 1995. Two classes of olfactory receptors in Xenopus laevis. Neuron 15: 1383-1392.
25. Freitag, J., Ludwig, G., Andreini, I., Rössler, P. and Breer, H. 1998. Olfactory receptors in aquatic and terrestrial vertebrates. J. Comp. Physiol. A 183: 645-650.
26. Frisch, D. 1967. Ultrastructure of the mouse olfactory mucosa. Am. J. Anat. 121: 87-120.
27. Fuss, S. H., Omura, M. and Mombaerts, P. 2005. The Grueneberg ganglion of the mouse projects axons to glomeruli in the olfactory bulb. Eur. J. Neurosci. 22: 2649-2654.
28. Getchell, M. L. and Getchell, T. V. 1992. Fine structural aspects of secretion and extrinsic innervation in the olfactory mucosa. Microsc. Res. Tech. 23: 111-127.
29. Giannetti, N., Pellier, V., Oestreicher, A. B. and Astic, L. 1995. Immunocytochemical study of the differentiation process of the septal organ of Masera in developing rat. Dev. Brain Res. 84: 287-293.
30. Gomez, G. and Celii, A. 2008. The peripheral olfactory system of the domestic chicken: physiology and development. Brain Res. Bull. 76: 208-216.
31. Graziadei, P. P. and Bannister, L. H. 1967. Some observations on the fine structure of the olfactory epithelium in the domestic duck. Z. Zellforsch. Mikrosk. Anat. 80: 220-228.
32. Graziadei, P. P. and Okano, M. 1979. Neuronal degeneration and regeneration in the olfactory epithelium of pigeon following transection of the first cranial nerve. Acta Anat. (Basel) 104: 220-236.
33. Halpern, M. 1987. The organization and function of the vomeronasal system. Ann. Rev. Neurosci. 10: 325-362.
34. Harrison, D. 1987. Preliminary thoughts on the incidence, structure and function of the mammalian vomeronasal organ. Acta Otolaryngol. (Stockh.) 103: 489-495.
35. Hunter, A. J., Fleming, D. and Dixson, A. F. 1984. The structure of the vomeronasal organ and nasopalatine ducts in Aotus trivirgatus and some other primate species. J. Anat. 138: 217-226.
36. Huxley, J. S. 1923. Time relations in amphibian metamorphosis, with some general considerations. Sci. Prog. 17: 606-618
37. Huxley, J. S. 1942. Evolution: The Modern Synthesis, Allen and Unwin, London.
38. Jacobson, L. 1811. Fait à l'Institut, sur un mémoire de M. Jacobson, intitulé: description anatomique d'un organe observe dans les mammifères. Rapport par M. Cuvier. Ann. Mus. Hist. Nat. Paris 18: 412-424 (in French).
39. Jin, E. H., Peng, K. M., Wang, J. A., Du, A. N., Tang, L., Wei, L., Wang, Y., Li, S. H. and Song, H. 2008. Study of the morphology of the olfactory organ of African ostrich chick. Anat. Histol. Embryol. 37: 161-165.
40. Johnson, A., Josephson, R. and Hawke, M. 1985. Clinical and histological evidence for the presence of the vomeronasal (Jacobson's) organ in adult humans. J. Otolaryngol. 14: 71-79.
41. Jordan, J. 1972. The vomeronasal organ (of Jacobson) in primates. Folia Morphol. 31: 418-432.
42. Kaslin, J., Ganz, J. and Brand, M. 2008. Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans. R. Soc. Lond. B. Biol. Sci. 363: 101-122.
43. Kent, G. C. and Carr, R. K. 2001. Comparative Anatomy of the Vertebrates, 9th ed., McGraw-Hill, New York.
44. Kondoh, D., Yamamoto, Y., Nakamuta, N., Taniguchi, K. and Taniguchi, K. 2010. Lectin histochemical studies on the olfactory epithelium and vomeronasal organ in the Japanese striped snake, Elaphe quadrivirgata. J. Morphol. 271: 1197-1203.
45. Kratzing, J. E. 1970. The structure of the vomeronasal organ in the sheep. J. Anat. 108: 247-260.
46. Kratzing, J. E. 1978. The olfactory apparatus of the bandicoot (Isoodon macrourus): fine structure and presence of a septal olfactory organ. J. Anat. 125: 601-613.
47. Liu, C. Y., Fraser, S. E. and Koos, D. S. 2009. Grueneberg ganglion olfactory subsystem employs a cGMP signaling pathway. J. Comp. Neurol. 516: 36-48.
48. Loo, S. K. 1977. Fine structure of the olfactory epithelium in some primates. J. Anat. 123: 135-145.
49. Loo, S. K. and Kanagasuntheram, R. 1972. The vomeronasal organ in tree shrew and slow loris. J. Anat. 112: 165-172.
50. Lundh, B., Brockstedt, U. and Kristensson, K. 1989. Lectinbinding pattern of neuroepithelial and respiratory epithelial cells in the mouse nasal cavity. Histochem. J. 21: 33-43.
51. Ma, M. 2007. Encoding olfactory signals via multiple chemosensory systems. Crit. Rev. Biochem. Mol. Biol. 42: 463-480.
52. Mamasuew, K., Breer, H. and Fleischer, J. 2008. Grueneberg ganglion neurons respond to cool ambient temperatures. Eur. J. Neurosci. 28: 1775-1785.
53. Marshall, D. A. and Maruniak, J. A. 1986. Masera's organ responds to odorants. Brain Res. 366: 329-332.
54. Mendoza, A. S. 1986. The mouse vomeronasal glands: a light and electron microscopical study. Chem. Senses 11: 541-555.
55. Mora, O. A. and Criado, J. E. S. 1980. A pheromonal chemoreceptor in the rat: the vomeronasal organ. Phronesis 1: 305-312.
56. Moran, D. T., Jafek, B. W. and Rowley, J. C. III. 1991. The vomeronasal (Jacobson's) organ in man: ultrastructure and frequency of occurrence. J. Steroid Biochem. Mol. Biol. 39: 545-552.
57. Müller, H., Drenckhahn, D. and Haase, E. 1979. Comparative and quantitative ultrastructural study of the olfactory organs of four strains of domestic pigeons. Z. Mikrosk. Anat. Forsch. 93: 888-900.
58. Murphy, M. R. and Schneider, G. E. 1970. Olfactory bulb removal eliminates mating behavior in the male golden hamster. Science 167: 302-304.
59. Naguro, T. and Breipohl, W. 1982. The vomeronasal epithelia of NMRI mouse. A scanning electron microscopic study. Cell Tissue Res. 227: 519-534.
60. Nakajima, T., Shiratori, K., Ogawa, K., Tanioka, Y. and Taniguchi, K. 1998. Lectin-binding patterns in the olfactory epithelium and vomeronasal organ of the common marmoset. J. Vet. Med. Sci. 60: 1005-1011.
61. Nakajima, T., Sakaue, M., Kato, M., Ogawa, K. and Taniguchi, K. 1998. Immunohistochemical and enzyme-histochemical study on the accessory olfactory bulb of the dog. Anat. Rec. 252: 393-402.
62. Nakamuta, N., Yokoyama, N., Yamamoto, Y., Taniguchi, K. and Taniguchi, K. 2009. Lectin histochemical analysis of the olfactory bulbs in the barfin flounder (Verasper moseri). Anat. Histol. Embryol. 39: 67-73.
63. Nakamuta, S., Nakamuta, N. and Taniguchi, K. 2010. Ultrastructure of the olfactory epithelium in a flatfish, barfin flounder (Verasper moseri). J. Vet. Med. Sci. 72: 801-804.
64. Nakashima, T., Kimmelman, C. P. and Snow, J. B. Jr. 1984. Structure of human fetal and adult olfactory neuroepithelium. Arch. Otolaryngol. 110: 641-646.
65. Oikawa, T., Saito, H., Taniguchi, K. and Taniguchi, K. 2001. Immunohistochemical studies on the differential maturation of three types of olfactory organs in the rats. J. Vet. Med. Sci. 63: 759-765.
66. Oikawa, T., Shimamura, K., Saito, T. R. and Taniguchi, K. 1994. Fine structure of the vomeronasal organ in the chinchilla (Chinchilla laniger). Exp. Anim. 43: 487-497.
67. Oikawa, T., Suzuki, K., Saito, T. R., Takahashi, K. W. and Taniguchi, K. 1998. Fine structure of three types of olfactory organs in Xenopus laevis. Anat. Rec. 252: 301-310.
68. Polyzonis, B. M., Kafandaris, P. M., Gigis, P. I. and Demetriou, T. 1979. An electron microscopic study of human olfactory mucosa. J. Anat. 128: 77-83.
69. Powers, J. B. and Winans, S. S. 1975. Vomeronasal organ: critical role in mediating sexual behavior of the male hamster. Science 187: 961-963.
70. Pyrski, M., Koo, J. H., Polumuri, S. K., Ruknudin, A. M., Margolis, J. W., Schulze, D. H. and Margolis, F. L. 2007. Sodium/ calcium exchanger expression in the mouse and rat olfactory systems. J. Comp. Neurol. 501: 944-958.
71. Rodolfo-Masera, T. 1943. Su l'esistenza di un particolare organo olfattivo nel setto nasale della cavia e di altri roditori. Arch. Ital. Anat. Embriol. 48: 157-213 (in Italian).
72. Saito, S., Matsui, T., Kobayashi, N., Wakisaka, H., Mominoki, K., Matsuda, S. and Taniguchi, K. 2003. Lectin histochemical study on the olfactory organ of the newt, Cynopus pyrrhogaster, revealed heterogenous mucous environments in a single nasal cavity. Anat. Embryol. (Berl.) 206: 349-356.
73. Saito, S., Oikawa, T., Taniguchi, K. and Taniguchi, K. 2010. Fine structure of the vomeronasal organ in the grass lizard, Takydromus tachydromoides. Tissue Cell 42: 322-327.
74. Saito, S. and Taniguchi, K. 2000. Expression patterns of glycoconjugates in the three distinctive olfactory pathways of the clawed frog, Xenopus laevis. J. Vet. Med. Sci. 62: 153-159.
75. Saito, S., Yamamoto, Y., Mori, M., Amano, M., Yamanome, T., Taniguchi, K., Yamamori, K. and Taniguchi, K. 2004. Variety in histochemical characteristics of the olfactory receptor cells in a flatfish, barfin flounder (Verasper moseri). J. Vet. Med. Sci. 66: 1409-1412.
76. Sarnat, H. B. and Netsky, M. G. 1974. Evolution of the Nervous System, Oxford University Press, New York.
77. Schmid, A., Pyrski, M., Biel, M., Leinders-Zufall, T. and Zufall, F. 2010. Grueneberg ganglion neurons are finely tuned cold sensors. J. Neurosci. 30: 7563-7568.
78. Shantha, T. R. and Nakajima, Y. 1970. Histological and histochemical studies on the rhesus monkey (Macaca mulatta) olfactory mucosa. Z. Zellforsch. 103: 291-319.
79. Soeta, S., Izu, Y., Saito, T. R., Yamano, S. and Taniguchi, K. 2005. Differential expression of neurofilament 200-like immunoreactivity in the main olfactory and vomeronasal systems of the Japanese newt, Cynopus pyrrhogaster. J. Vet. Med. Sci. 67: 701-706.
80. Stensaas, L. J., Lavker, R. M., Monti-Broch, L., Grosser, B. I. and Berlinger, D. L. 1991. Ultrastructure of the human vomeronasal organ. J. Steroid Biochem. Mol. Biol. 39: 553-560.
81. Takami, S., Getchell, M. L. and Getchell, T. V. 1994. Lectin histochemical localization of galactose, N-acetylgalactosamine, and N-acetylglucosamine in glycoconjugates of the rat vomeronasal organ, with comparison to the olfactory and septal mucosae. Cell Tissue Res. 277: 211-230.
82. Taniguchi, K., Arai, T. and Ogawa, K. 1993. Fine structure of the septal olfactory organ of Masera and its associated gland in the golden hamster. J. Vet. Med. Sci. 55: 107-116.
83. Taniguchi, K., Matsusaki, Y., Ogawa, K. and Saito, T. R. 1992. Fine structure of the vomeronasal organ in the common marmoset (Callithrix jacchus). Folia Primatol. 59: 169-176.
84. Taniguchi, K. and Mikami, S. 1985. Fine structure of the epithelia of the vomeronasal organ of horse and cattle. A comparative study. Cell Tissue Res. 240: 41-48.
85. Taniguchi, K. and Mochizuki, K. 1982. Morphological studies on the vomeronasal organ in the golden hamster. Jpn. J. Vet. Sci. 44: 419-426.
86. Taniguchi, K. and Mochizuki, K. 1983. Comparative morphological studies on the vomeronasal organ in rats, mice and rabbits. Jpn. J. Vet. Sci. 45: 67-76.
87. Taniguchi, K., Saito, H., Okamura, M. and Ogawa, K. 1993. Immunohistochemical demonstration of protein gene product 9.5 (PGP 9.5) in the primary olfactory system of the rat. Neurosci. Lett. 156: 24-26.
88. Taniguchi, K., Saito, S., Oikawa, T. and Taniguchi, K. 2008. Phylogenic aspects of the amphibian dual olfactory system. J. Vet. Med. Sci. 70: 1-9.
89. Taniguchi, K. and Taniguchi, K. 2008. Embryonic and postnatal differentiation of olfactory epithelium and vomeronasal organ in the Syrian hamster. J. Vet. Med. Sci. 70: 57-64.
90. Taniguchi, K., Taniguchi, K. and Mochizuki, K. 1982. Comparative developmental studies on the fine structure of the vomeronasal sensory and the olfactory epithelia in the golden hamster. Jpn. J. Vet. Sci. 44: 881-890.
91. Taniguchi, K., Toshima, Y., Saito, T. R. and Taniguchi, K. 1996. Development of the olfactory epithelium and vomeronasal organ in the Japanese reddish frog, Rana japonica. J. Vet. Med. Sci. 58: 7-15.
92. Taniguchi, K., Toshima, Y., Saito, T. R. and Taniguchi, K. 1996. Development of the Bowman's and Jacobson's glands in the Japanese reddish frog, Rana japonica. J. Vet. Med. Sci. 58: 17-22.
93. Vaccarezza, O. L., Sepich, L. N. and Tramezzani, J. H. 1981. The vomeronasal organ of the rat. J. Anat. 132: 167-185.
94. Weiler, E. and Farbman, A. I. 2003. The septal organ of the rat during postnatal development. Chem. Senses 28: 581-593.
95. Weiler, E. and Benali, A. 2005. Olfactory epithelia differentially express neuronal markers. J. Neurocytol. 34: 217-240.
96. Winans, S. S. and Powers, L. B. 1977. Olfactory and vomeronasal deafferentation of male hamsters: histological and behavioral analysis. Brain Res. 126: 325-344.
97. Wysocki, C. J. 1979. Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci. Biobehav. Rev. 3: 301-341.
98. Wysocki, C. J., Nyby, J., Whitney, G., Beauchamp, G. K. and Katz, Y. 1982. The vomeronasal organ: primary role in mouse chemosensory gender recognition. Physiol. Behav. 29: 315-327.
99. Wysocki, C. J., Wellington, J. L. and Beauchamp, G. K. 1980. Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 207: 781-783.
100. Yamamoto, Y., Mori, M., Amano, M., Yamanome, T., Saito, S., Taniguchi, K., Yamamori, K. and Taniguchi, K. 2004. Morphogenesis of the olfactory pit in a flatfish, barfin flounder (Verasper moseri). J. Vet. Med. Sci. 66: 1275-1278.
101. Yamamoto, Y., Mori, M., Saito, S., Amano, M., Yamanome, T., Taniguchi, K., Oikawa, T., Yamamori, K. and Taniguchi, K. 2004. Differential expression of histochemical characteristics in the developing olfactory receptor cells in a flatfish, barfin flounder (Verasper moseri). J. Vet. Med. Sci. 66: 1609-1611.
102. Yokosuka, M., Hagiwara, A., Saito, T. R., Aoyama, M., Ichikawa, M. and Sugita, S. 2009. Morphological and histochemical study of the nasal cavity and fused olfactory bulb of the brown-eared bulbul, Hysipetes amaurotis. Zoolog. Sci. 26: 713-721.
103. Yokosuka, M., Hagiwara, A., Saito, T. R., Tsukahara, N., Aoyama, M., Wakabayashi, Y., Sugita, S. and Ichikawa, M. 2009. Histological properties of the nasal cavity and olfactory bulb of the Japanese jungle crow Corvus macrorhynchos. Chem. Senses 34: 581-593.