Summary
The present anatomical findings point to the existence of a separate subdivision of the olfactory system whose connections are quite different from the principal part. The main olfactory bulb has olfactory afferents from the receptors of the general olfactory mucosa, while the accessory bulb has afferents from receptors in the vomeronasal organ. The main bulb projects to the olfactory tubercle and pyriform cortex, while the accessory bulb projects to the amygdala. In turn these areas are further related with the medial forebrain bundle in the case of the pyriform cortex and olfactory tubercle, and with the medial preoptic area and medial hypothalamus in the case of the amygdala. The main and accessory olfactory bulbs are further distinguished by their centrifugal connections, the main bulb receiving fibres from the olfactory tubercle passing through the lateral olfactory tract, and the accessory olfactory bulb receiving fibres from the amygdala through the stria terminalis. The centrifugals to the accessory olfactory bulb resemble those to the main bulb in that both appear to terminate upon granule cells, although further projections to the external plexiform layer or to the periglomerular region have not been demonstrated for the accessory bulb. By virtue of its neural connections the accessory olfactory system is ideally placed to mediate the effects of olfactory stimuli on reproduction.
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References
Aron, C., Roos, J., Asch, G.: Effect of removal of the olfactory bulbs on mating activity and ovulation in the rat. Neuroendocrinology 6, 109–117 (1969).
Bruce, H.M.: Pheromones. Brit. med. Bull. 26, 10–13 (1970).
— Parrott, D.M.V.: Role of olfactory sense in pregnancy block by strange males. Science 131, 1526 (1960).
Cajal, S. Ramón y: Histologie du système nerveux de l'homme et des vertébrés. Paris: Maloine 1911.
Colonnier, M.: Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9, 268–287 (1968).
Cowan, W.M., Raisman, G., Powell, T.P.S.: The connexions of the amygdala. J. Neurol. Neurosurg. Psychiat. 28, 137–151 (1965).
Cragg, B.G.: Centrifugal fibers to the retina and olfactory bulb, and the composition of the supraoptic commissures in the rabbit. Exp. Neurol. 5, 406–427 (1962).
Dennis, B.J., Kerr, D.I.B.: An evoked potential study of centripetal and centrifugal connections of the olfactory bulb in the cat. Brain Res. 11, 373–396 (1968).
De Olmos, J.S.: A cupric-silver method for impregnation of terminal axon degeneration and its further use in staining granular argyrophilic neurons. Brain Behav. Evol. 2, 213–237 (1969).
De Olmos, J.S. The projection field of the stria terminalis in the rat brain. An experimental study with silver techniques. Ph. D. Thesis, University of Iowa, January 1971. Dissertation Abstracts. In the press.
Diamond, J., Gray, E.G., Yasargil, G.M.: The function of the dendritic spine: an hypothesis. In: Excitatory Synaptic Mechanisms, pp. 213–222. Ed. by J. Jansen and P. Andersen. Oslo: Scandinavian University Books 1970.
Gandelman, R., Zarrow, M.X., Denenberg, V.H., Myers, M.: Olfactory bulb removal eliminates maternal behavior in the mouse. Science 171, 210–211 (1971).
Girgis, M., Goldby, F.: Secondary olfactory connexions and the anterior commissure in the coypu, Myocastor coypus. J. Anat. (Lond.) 101, 33–44 (1967).
Heimer, L.: Synaptic distribution of centripetal and centrifugal nerve fibres in the olfactory system of the rat. An experimental anatomical study. J. Anat. (Lond.) 103, 413–432 (1968).
—: The secondary olfactory connections in mammals, reptiles, and sharks. Ann. N.Y. Acad. Sci. 167, 129–146 (1969).
— Larsson, K.: Mating behaviour of male rats after olfactory bulb lesions. Physiol. Behav. 2, 207–209 (1967).
— Nauta, W.J.H.: The hypothalamic distribution of the stria terminalis in the rat. Brain Res. 13, 284–297 (1969).
Herrick, C.J.: The connections of the vomeronasal nerve, accessory olfactory bulb, and amygdala in Amphibia. J. comp. Neurol. 33, 213–280 (1921).
Hetherington, A.W., Ranson, S.W.: Hypothalamic lesions and adiposity in the rat. Anat. Rec. 78, 149–172 (1940).
Kappers, C.U.A., Huber, G.C., Crosby, E.C.: The comparative anatomy of the nervous system of vertebrates, including man. New York: The Macmillan Co. 1936.
Lawton, I.E., Sawyer, C.H.: Role of amygdala in regulating LH secretion in the adult female rat. Amer. J. Physiol. 218, 622–625 (1970).
Leonard, C.M., Scott, J.W.: Origin and distribution of the amygdalofugal pathways in the rat: an experimental neuroanatomical study. J. comp. Neurol. 141, 313–330 (1971).
Lohman, A.H.M., Lammers, H.J.: On the connections of the olfactory bulb and the anterior olfactory nucleus in some mammals. Progr. Brain Res. 3, 149–162 (1963).
— Mentink, G.M.: The lateral olfactory tract, the anterior commissure and the cells of the olfactory bulb. Brain Res. 12, 396–413 (1969).
Murphy, M., Schneider, G.E.: Olfactory bulb removal eliminates mating behavior in the male golden hamster. Science 167, 302–304 (1970).
Negus, V.E.: The organ of Jacobson. J. Anat. (Lond.) 90, 515–519 (1956).
Orbach, J., Kling, A.: Effect of sensory deprivation on onset of puberty, mating, fertility and gonadal weights in rats. Brain Res. 3, 141–149 (1966).
Parkes, A.S., Bruce, H.M.: Olfactory stimuli in mammalian reproduction. Science 134, 1049–1054 (1961).
Powell, T.P.S., Cowan, W.M., Raisman, G.: The central olfactory connexions. J. Anat. (Lond.) 99, 791–813 (1965).
Price, J.L., Powell, T.P.S.: An experimental study of the origin and the course of the centri fugal fibres to the olfactory bulb in the rat. J. Anat. (Lond.) 107, 215–238 (1970a).
—: An electron-microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemisphere. J. Cell Sci. 7, 157–188 (1970b).
—: The morphology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 91–124 (1970c).
Raisman, G., Field, P.M.: Sexual dimorphism in the preoptic area of the rat. Science 173, 731–733 (1971).
Rall, W., Shepherd, G.M., Reese, T.S., Brightman, M.W.: Dendro-dendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44–56 (1966).
Scalia, F.: A review of recent experimental studies on the distribution of the olfactory tracts in mammals. Brain Behav. Evol. 1, 101–123 (1968).
Shepherd, G.M.: The olfactory bulb as a simple cortical system: experimental analysis and functional implications. In: The Neurosciences, Second Study Program, pp. 539–552. Ed. by F.O. Schmitt. New York: The Rockefeller University Press 1970.
Uchizono, K.: Inhibitory and excitatory synapses in vertebrate and invertebrate animals. In: Structure and Function of Inhibitory Neuronal Mechanisms, pp. 33–59. Ed. by C. von Euler, S. Skoglund and U. Söderberg. Oxford: Pergamon Press 1968.
Valenstein, E.S., Cox, V.C., Kakolewski, J.W.: Sex differences in hyperphagia and body weight following hypothalamic damage. Ann. N.Y. Acad. Sci. 157, 1030–1048 (1969).
Velasco, M.E., Taleisnik, S.: Release of gonadotropins induced by amygdaloid stimulation in the rat. Endocrinology 84, 132–139 (1969).
White, L.E., jr.: Olfactory bulb projections of the rat. Anat. Rec. 152, 465–480 (1965).
Whitten, W.K.: Is the vomeronasal organ a sex chemoreceptor in mice? In: Second Asia and Oceania Congress of Endocrinology, Sydney, 1963.
—: Pheromones and mammalian reproduction. Advan. Reprod. Physiol. 1, 155–177 (1966).
Winans, S.S., Scalia, F.: Amygdaloid nucleus: new afferent input from the vomeronasal organ. Science 170, 330–331 (1970).
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Raisman, G. 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 (1972). https://doi.org/10.1007/BF00235035
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DOI: https://doi.org/10.1007/BF00235035