Neurobiology pp 165-173 | Cite as
The Vomeronasal Organ
Abstract
The vomeronasal (VN) organ of Jacobson is the receptor organ of the accessory olfactory system (AOS). The VN organ consists mainly of an olfactory epithelium (OE) and a vascular pump. The OE is characterised by the presence of primary receptor neurons whose axons form the VN nerve and contact the secondary neurons in the AO bulb (AOB). Hence the neural outflow goes to brain structures controlling the pituitary-gonadal axis and the reproductive behaviour. The adequate stimuli for the VN organ are volatile as well as non-volatile substances. They are driven toward the primary VN neurons through a blind ended canal, the VN canal, by the vascular pump. The VN system is important in chemical communication within the species and the majority of the effects driven by the activity of this system in mammals gather under the umbrella of reproduction. The evidence from molecular biology, biochemistry, histology, physiology and behaviour studies singles out the VN system as a distinct system when compared to the main olfactory system.
Keywords
Olfactory Epithelium Mitral Cell Main Olfactory Bulb Vomeronasal Organ Accessory Olfactory BulbPreview
Unable to display preview. Download preview PDF.
References
- Abe, H., Watanabe, M. and Kondo, H. (1992). Developmental changes in expression of a calcium-binding protein (spot 35 — calbindin) in the Nervus terminalis and the vomeronasal and olfactory receptor cells. Acta Otolaryngol Stockh. 112, 862–871.PubMedCrossRefGoogle Scholar
- Bacchini, A., Gaetani, E. and Cavaggioni, A. (1992). Pheromone binding proteins of the mouse, Mus musculus. Experientia 48, 419–421.PubMedCrossRefGoogle Scholar
- Bannister, L.H. and Dodson, H.C. (1992). Endocytic pathways in the olfactory and vomeronasal epithelia of the mouse: ultrastructure and uptake of tracers. Microsc. Res. Tech. 23, 128–141.PubMedCrossRefGoogle Scholar
- Barber, P.C. and Raisman, G. (1978). Replacement of receptor neurones after transection of the vomeronasal nerves in the adult mouse. Brain Res. 147, 297–313.PubMedCrossRefGoogle Scholar
- Baum, M.J. and Everitt, B.J. (1992). Increased expression of c-fos in the medial preoptic area after mating in male rats: role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience 50, 627–646.PubMedCrossRefGoogle Scholar
- Bean, N.J. and Wysocki, C.J. (1989). Vomeronasal organ removal and female mouse aggression: the role of experience. Physiol. Behav. 45, 875–882.PubMedCrossRefGoogle Scholar
- Bhatnagar, K.P. and Wible, J.R. (1994). Observations on the vomeronasal organ of the Colugo cynocephalus. Acta Anatomica 151, 43–48.PubMedCrossRefGoogle Scholar
- Bocskei, Z., Groom, C.R., Flower, D.R., Wright, C.E., Phillips, S.E.V., Cavaggioni, A., Findlay, J.B.C. and North, A.C.T. (1992). Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature 360, 186–188.PubMedCrossRefGoogle Scholar
- Brennan, P., Kaba, H. and Keverne, E.B. (1990). Olfactory recognition: a simple memory system. Science 250, 1223–1226.PubMedCrossRefGoogle Scholar
- Brennan, P.A., Hancock, D. and Keverne, E.B. (1992). The expression of the immediate-early genes c-fos, egr-1 and c-jun in the accessory olfactory bulb during formation of an olfactory memory in mice. Neuroscience 49, 277–284.PubMedCrossRefGoogle Scholar
- Broman, I. (1920). Das Organon vomero-nasale Jacobsoni — ein Wassergeruchorgan! Anat. Hefte, 1 Abt., H. 174, 137–191.Google Scholar
- Burton, P.R., Coogan, M.M. and Borror, C.A. (1990). Vomeronasal and olfactory nerves of adult and larval bull frogs: I. Axons and the distribution of their glomeruli. J. Comp. Neurol. 292, 614–623.PubMedCrossRefGoogle Scholar
- Clark, A.J., Ghazal, P., Bingham, R.W., Barrett, D. and Bishop J.O. (1985). Sequence structures of a mouse major urinary protein gene and pseudogene compared. The EMBO J. 4, 3159–3165.Google Scholar
- Collado, P., Segovia, S., Cales, J. M., Perez-Laso, C., Rodriguez-Zafra, M., Guillamon, A. and Valencia, A. (1992). Female’s DHT controls sex differences in the rat bed nucleus of the accessory olfactory tract. Neuroreport. 3, 327–329.PubMedCrossRefGoogle Scholar
- Cooper, G.J. and Bhatnagar, K.P. (1976). Comparative anatomy of the vomeronasal complex in bats. J. Anat. 122, 571–601.PubMedGoogle Scholar
- Coppola, D.M., Budde, J. and Millar L. (1993). Vomeronasal duct has a protracted postnatal development in the mouse. J. Morphol. 218, 59–64.PubMedCrossRefGoogle Scholar
- Daikoku, S., Daikoku-Ishido, H., Okamura, Y., Chikamori-Aoyama, M. and Yokote, R. (1991). Further evidence of the presence of rat embryonic hypothalamic factors that induce the differentiation of gonadotropic hormone-releasing hormone-containing secretory neurons. Anat. Rec. 230, 539–550.PubMedCrossRefGoogle Scholar
- Danty, E., Cornuet, J.M. and Masson C. (1994). Honeybees have putative olfactory receptor proteins similar to those of vertebrates. C. R. Acad. Sci. Paris 317, 1073–1079.PubMedGoogle Scholar
- Doty, R.L. (1986). Odor-guided behavior in mammals. Experientia 42, 257–271.PubMedCrossRefGoogle Scholar
- Dudley, C.A. and Moss, R.L. (1995). Electrophysiological evidence for glutamate as a vomeronasal receptor cell neurotransmitter. Brain Res 675, 208–214.PubMedCrossRefGoogle Scholar
- Eisthen, H.L. (1992). Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates. Microsc. Res. Tech. 23, 1–21.PubMedCrossRefGoogle Scholar
- Fleming, A.S., Gavorth, K. and Sarker, J. (1992). Effects of transections to the vomeronasal nerves or the main olfactory bulbs on the initiation and long-term retention of maternal behavior in primiparous rats. Behav. Neural. Biol. 57, 177–188.PubMedCrossRefGoogle Scholar
- Franceschini, F., Sbarbati, A. and Zancanaro, C. (1991). The vomeronasal organ in the frog, Rana esculenta. An electron microscopy study. J. Submicrosc. Cytol. Pathol. 23, 221–231.PubMedGoogle Scholar
- Garcia-Velasco, J. and Mondragon M. (1991). The incidence of the vomeronasal organ in 1000 human subjects and its possible clinical significance. J. Steroid Biochem. Mol. Biol. 39, 561–563.PubMedCrossRefGoogle Scholar
- Gaupp, E. (1904). Anatomie des Frosches. Vieweg Verlag, Braunschweig, 673.Google Scholar
- Getchell, T.V., Margolis, F.L. and Getchell M.L. (1984). Perireceptor and receptor events in vertebrate olfaction. Progress in Neurobiology 23, 317–345.PubMedCrossRefGoogle Scholar
- Halpern, M. and Kubie, J.L. (1984). The role of the ophidian vomeronasal system in species-typical behavior. TINS December 1984, 472–477.Google Scholar
- Halpern, M. (1987). The organization and function of the vomeronasal system. Am. Rev. Neurosci. 10,325–365.CrossRefGoogle Scholar
- Harrison, D.(1987). Preliminary thoughts on the incidence, structure and function of the mammalian vomeronasal organ. Acta Otolaryngol. (Stockholm) 103, 489–495.Google Scholar
- Hatanaka, T. (1992). The mouse vomeronasal organ a sex pheromone receptor? Chemical Signals in Vertebrates VI, edited by R.L. Doty and D. Muller-Schwarze, Plenum Press, New York, 27–31.Google Scholar
- Hatton, G.I. and Yang, Q.Z. (1990). Activation of excitatory amino acid inputs to supraoptic neurons. I. Induced increases in dye-compling in lactating, but not virgin or male rats. Brain Res. 513, 264–269.PubMedCrossRefGoogle Scholar
- Henzel, W.J., Rodriguez, H., Singer, A.G., Stults, J. T., Macrides, F., Agosta, W.C. and Niall, H. J. (1988). The primary structure of aphrodisin. Biol. Chem. 263, 16682–16687.Google Scholar
- Ichikawa, M., Osada, T. and Ikai, A. (1992). Bandeiraea simplicifolia lectin I and Vicia villosa agglutinin bind specifically to the vomeronasal axons in the accessory olfactory bulb of the rat. Neurosci. Res. 13, 73–79.PubMedCrossRefGoogle Scholar
- Johnson, E.W., Eller, P.M., Jafek, B.W. and Norman, A.W. (1992). Calbindin-like immuno-reactivity in two peripheral chemosensory tissues of the rat: taste buds and the vomeronasal organ. Brain Res. 572, 319–324.PubMedCrossRefGoogle Scholar
- Jones, F.M., Pfeiffer, C. and Asashima, M. (1994). Ultrastructure of the olfactory organ of the newt Cynopspirrhogaster. Annals of Anatomy 176, 269–275.PubMedCrossRefGoogle Scholar
- Kaba, H., Hayashi, Y, Higuchi, T. and Nakanishi S. (1994). Induction of an olfactory memory by the activation of a metabotropic glutamate receptor. Science 265, 262–264.PubMedCrossRefGoogle Scholar
- Kaba, H., Rosser, A. E. and Keverne, E.B. (1988). Hormonal enhancement of neurogenesis and its relationsship to the duration of olfactory memory. Neuroscience 24, 93–98.PubMedCrossRefGoogle Scholar
- Keverne, E. (1983). Pheromonal influences on the endocrine regulation of reproduction. TINS, September 1983, 381–384.Google Scholar
- Khew-Goodall, Y., Grillo, M., Getchell, M.L., Danho, W., Getchell, T.V. and Margolis, F.L. (1991). Vomeromodulin, a putative pheromone transporter: cloning, characterization, and cellular localization of a novel glycoprotein of lateral nasal gland. FASEB J. 5, 2976–2982.PubMedGoogle Scholar
- Kishimoto, J., Keverne, E.B. and Emson, P.C. (1993). Calretinin, calbindin-D28k and parvalbumin — like immunoreactivity in mouse chemoreceptor neurons. Brain Res. 610, 325–329.PubMedCrossRefGoogle Scholar
- Koch, M. (1990). Effects of tratment with estradiol and parental experience on the number and distribution of estrogen-binding neurons in the ovariectomized mouse brain. Neuroendocrinology 51, 505–514.PubMedCrossRefGoogle Scholar
- Krishna, N.S., Getchell, M.L. and Getchell, T.V. (1992). Differential distribution of gamma-glutamyl cycle molecules in the vomeronasal organ of rats. Neuroreport 3, 551–554.PubMedCrossRefGoogle Scholar
- Krishna, N.S.R., Getchell, M.L. and Getchell, T.V. (1994). Expression of the putative pheromone and odorant transporter vomeromodulin messenger-RNA and protein in nasal chemosensory mucosae. J. Neurosci. Res. 39, 243–259.PubMedCrossRefGoogle Scholar
- Li, C.S., Kaba, H., Saito, H. and Seto, K. (1992). Oestrogen infusions into the amygdala potentiate excitatory transmission from the accessory olfactory bulb to tuberoinfundibular arcuate neurones in the mouse. Neurosci. Lett. 143, 48–50.PubMedCrossRefGoogle Scholar
- Masson, C. and Mustaparta, H. (1990). Chemical information processing in the olfactory system of insects. Physiological Reviews 70, 199–245.Google Scholar
- Meek, L.R., Lee, T.M., Rogers, E.A. and Hernandez, R.R. (1994). Effect of vomeronasal organ removal on behavioural estrus and mating latency. Biology of Reproduction 51, 400–404.PubMedCrossRefGoogle Scholar
- Mendoza, A.S. and Szabo, K. (1988). Developmental studies on the rat vomeronasal organ: vascular pattern and neuroepithelial differentiation. II. Electon microscopy. Brain Res. 467, 259–268.PubMedGoogle Scholar
- Mennella, J. A. and Moltz, H. (1988). Infanticide in the male rat: the role of vomeronasal organ. Physiol. Behav. 42, 303–306.PubMedCrossRefGoogle Scholar
- Meredith, M. (1994). Chronic recording of vomeronasal pump activation in awake behaving hamsters. Physiol. Behav. 56, 345–354.PubMedCrossRefGoogle Scholar
- Meredith M. and Howard, G. (1992). Intracerebro-ventricular LHRH relieves deficits due to vomeronasal organ removal. Brain Res. Bull. 29, 75–79.PubMedCrossRefGoogle Scholar
- Meredith, M. and Fernandez-Fewell, G. (1994). Vomeronasal system, LHRH and sex behavior. Psychoneuroendocrinology 19, 657–672.PubMedCrossRefGoogle Scholar
- Milligan, S.R. (1980). Pheromones and rodent reproductive physiology. Symp. Zool. Soc. Lond. 45, 251–275.Google Scholar
- Miyawaki, A., Matsushita, F., Ryo, F. and Mikoshiba, K. (1994). Possible pheromone-carrier function of two lipocalin proteins in the vomeronasal organ. The EMBO J. 13, 5835–5842.Google Scholar
- Modney, B.K., Yang Q.Z. and Hatton, G.I. (1990). Activation of excitatory amino acid inputs to supraoptic neurons. II. Increased dye-coupling in maternally behaving virgin rats. Brain Res. 513, 270–273.PubMedCrossRefGoogle Scholar
- Moran, D.T., Jafek, B.W. and Rowley, J. C. (1991). The vomeronasal (Jacobson’s) organ in man: ultrastructure and frequency of occurrence. J. Steroid Biochem. Mol. Biol. 39, 545–552.PubMedCrossRefGoogle Scholar
- Mucignat-Caretta, C., Caretta, A. and Cavaggioni, A. (1995). Acceleration of puberty onset in female mice by male urinary proteins. J. Physiol. (London) 486.2, 517–522.Google Scholar
- Ngai, J., Dowling, M.M., Buck, L., Axel, R. and Chess A. (1993). The family of genes coding odorant receptors in the channel catfish. Cell 72, 657–666.PubMedCrossRefGoogle Scholar
- Pelosi P. (1994). Odorant binding proteins. Critical Reviews in Biochemistry and Molecular Biology 29, 199–228.PubMedCrossRefGoogle Scholar
- Robertson, D.H.L., Beynon, R.J. and Evershed, R.P. (1993). Extraction, characterisation, and binding analysis of two pheromonally active ligands associated with the major urinary protein of the house mouse (Mus musculus) J. Chem. Ecol. 19, 1405–1414.CrossRefGoogle Scholar
- Romero, P.R., Beltramino, C.A. and Carrer, H.F. (1990). Participation of the olfactory system in the control of approach behavior of the female rat to the male. Physiol. Behav. 47, 685–690.PubMedCrossRefGoogle Scholar
- Saito, T.R., Igarashi, N., Hokao, R., Wakafuji, Y. and Takahashi, K.W. (1990). Nursing behavior in lactating rats-the role of the vomeronasal organ. Jikken-Dobutsu 39, 109–111.PubMedGoogle Scholar
- Sansom, C.E., North, A.C.T. and Sawyer L. (1994). Structural analysis and classification of lipocalins and related proteins using a profile-search method. Biochimica et Biophysica Acta 1208, 247–255.PubMedCrossRefGoogle Scholar
- Satoda, M., Takagi, S., Ohta, K., Hirata, T. and Fujiama, T. (1995). Differential expression of 2 cell-surface proteins, neuropilin and plexin in Xenopus olfactory axon subclasses. J. Neurosci. 15, 942–955.PubMedGoogle Scholar
- Schilling, A., Serviere, J. Gendrot, G. and Perret, M. (1990). Vomeronasal activation by urine in the primate Microcebus murinus: a 2 DG study. Exp. Brain Res. 81, 609–618.PubMedCrossRefGoogle Scholar
- Schmidt, A. and Roth G. (1990). Central olfactory and vomeronasal pathways in salamanders. J. Hirnforsh. 31, 543–553.Google Scholar
- Schwanzel-Fukuda, M., Zheng, L.M., Bergen, H., Weesner, G. and Pfaff, D.W. (1992). LHRH neurons: functions and development. Prog. Brain Res. 93, 189–201.PubMedCrossRefGoogle Scholar
- Segovia, S. and Guillamon, A. (1982). Effect of sex steroids on the development of the vomeronasal organ in the rat. Developmental Brain Res. 5, 209–212.CrossRefGoogle Scholar
- Segovia, S. and Guillamon, A. (1993). Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res. Rev. 18, 51–74.PubMedCrossRefGoogle Scholar
- Singer, A.G., Clancy, A.N., Macrides, F., Agosta, W. C. and Bronson, F.H. (1988). Chemical properties of a female mouse pheromone that stimulates gonadotropin secretion in males. Biol. Reprod. 38, 193–199.PubMedCrossRefGoogle Scholar
- Stensaas, L.J., Lavker, R.M., Monti-Bloch, L., Grosser, B.I. and Berliner, D.L. (1991). Ultrastructure of the human vomeronasal organ. J. Steroid Biochem. Mol. Biol. 39, 553–560.PubMedCrossRefGoogle Scholar
- Stoddart, D.M. (1980). The ecology of vertebrate olfaction. Champman and Hall, London and New York.CrossRefGoogle Scholar
- Vandenbergh, J.G., Finlayson, J.S., Dobrogosz, W.J., Dells, S.S. and Kost, T.A. (1976). Chromatographic separation of puberty accelerating pheromone from male mouse urine. Biology of reproduction 15, 260–265.PubMedCrossRefGoogle Scholar
- Von Bartheld, C.S., Claas, B., Munz, H. and Meyer, D.L. (1988). Primary olfactory projections and the Nervus terminalis in the African lung fish: implications for the phytogeny of cranial nerves. Am. J. Anat. 182, 325–334.CrossRefGoogle Scholar
- Wang, D., Jiang, X.C., Chen, P., Inouchi, J. and Halpern, M. (1993). Chemical and immunological analysis of prey-derived vomeronasal stimulants. Brain. Behav. Evol. 41, 246–254.PubMedCrossRefGoogle Scholar
- Wang, H.J. and Tsai, Y.F. (1991). Effects of male rat urine on norepinerphine levels in the accessory olfactory bulb of young and aged female rats. Proc. Natl. Sci. Counc. Repub. China 15, 160–164.Google Scholar
- Wysocki, C.J. and Lepri, J.J. (1991). Consequences of removing the vomeronasal organ. J. Steroid Biochem. Mol. Biol. 39, 661–669.PubMedCrossRefGoogle Scholar
- Wysocki, C. J., Wellington, J. L. and Beauchamp, G.K., (1980). Access of urinary nonvolatiles to the mammalian vomeronasal organ. Science 207, 781–783.PubMedCrossRefGoogle Scholar
- Wysocki, C.J. and Meredith M. (1987). The vomeronasal system. In: “Neurobiology of taste and Smell.” Finger T.E. and Silver W.L. eds, John Wiley and Sons, 125–151.Google Scholar