Summary
Over the years, investigators have noticed, in a wide variety of species of vertebrates, large numbers of cells migrating from the olfactory placode to the forebrain. These cells were considered to be Schwann cells or ganglion cells of the terminalis nerve. Recently, immunocytochemical localization studies have shown that many of these migrating cells contain luteinizing hormone-releasing hormone (LHRH), a brain peptide that regulates reproductive functions by evoking the release of luteinizing hormone and follicle-stimulating hormone from the anterior pituitary gland. The origin of LHRH cells in the epithelium of the medial olfactory placode, their migration across the nasal septum and into the forebrain, with branches of the terminalis nerve, also a derivative of the medial part of the olfactory placode, has led to some interesting speculations, from evolutionary and physiological perspectives, about the origin of these cells and the role of the terminalis nerve in their migration.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Barry, J., Characterization and topography of LHRH neurons in the human brain. Neurosci. Lett.3 (1976) 287–291.
Bedford, E. A., The early history of the olfactory nerve in swine. J. comp. Neurol.14 (1904) 390–410.
Bossy, Y., Development of olfactory and related structures in staged human embryos. Anat. Embryol.161 (1980) 225–236.
Brookover C., The peripheral distribution of the nervus terminalis in an infant. J. comp. Neurol.28 (1917) 349–360.
Brown, J. W., Developmental history of nervus terminalis in embryos of insectivorous bats. Anat. Rec.196 (1980) 23–35.
Brunjes, P. C., and Frazier, L. L., Maturation and plasticity in the olfactory system of vertebrates. Brain Res. Rev.11 (1986) 1–45.
Buhl, E. H., and Oelschlager, H. A., Ontogenetic development of the nervus terminalis in toothed whales. Anat. Embryol.173 (1986) 285–294.
Burr, H. S., The effects of removal of the nasal pits inAmblystoma embryos. J. exp. Zool.20 (1916) 27–51.
Cuschieri, A., and Bannister, L. H., The development of the olfactory mucosa in the mouse: light microscopy. J. Anat.119 (1975) 277–286.
Demski, L., and Northcutt, R. G., The terminal nerve: a new chemosensory system in vertebrates? Science220 (1983) 435–437.
Farbman, A. I., and Squinto, L. M., Early development of olfactory receptor cell axons. Dev. Brain Res.19 (1985) 205–213.
Graziedei, P. P. C., Levine, R. R., and Monti Graziedei, G. A., Plasticity of connections of the olfactory sensory neuron: regeneration into the forebrain following bulbectomy in the neonatal mouse. Neuroscience4 (1979) 713–727.
Graziedei, P. P. C., Levine, R. R., and Monti Graziedei, G. A., Regeneration of olfactory bulb axons and synapse formation in the forebrain after bulbectomy in neonatal mice. Proc. natl Acad. Sci. USA75 (1978) 5230–5234.
Guillemin, R., Peptides in the brain: The new endocrinology of the neuron. Science202 (1978) 390–402.
Halpern-Sebold, L. R., and Schreibman, M. P., Ontogeny of centers containing luteinizing hormone-releasing hormone in the brain of the platyfish (Xiphophorus maculatus) as determined by immunocytochemistry. Cell Tiss. Res.229 (1983) 75–84.
Humphrey, T., Correlations between the development of the hippocampal formation and differentiation of the olfactory bulbs. Ala. J. med. Sci.3 (1966) 235–269.
Jacobson, M., Histogenesis and morphogenesis of the central nervous system, in: Developmental Neurobiology, 2nd edn, pp. 57–114. Plenum Press, New York 1979.
Jennes, L. and Stumpf, W. E., Luteinizing hormone-releasing hormone (LHRH) systems in the brain of the golden hamster. Cell Tiss. Res.209 (1980) 239–256.
Jennes, L., Prenatal development of the gonadotropin-releasing hormone-containing systems in rat brain. Brain Res.482 (1989) 97–108.
Kallmann, F., Schoenfeld, W. A., and Barrera, S. E., The genetic aspects of primary eunuchoidism. Am. J. ment. Defic.48 (1944) 203–236.
Klein, S. L., and Graziedei, P. P. C., The differentiation of the olfactory placode inXenopus laevis: a light and electron microscope study. J. comp. Neurol.217 (1983) 17–30.
Larsell, O., Studies on the nervus terminalis: mammals. J. comp. Neurol.30 (1918) 3–68.
Larsell, O., The nervus terminalis. Ann. Otol. Rhinol. Laryng.59 (1950) 414–435
Lejour, M., Activité de quatre enzymes dephosphorylants au cours de la morphogenèse du palais primaire chez le rat (phosphatase alcaline, phosphatase acide, ATP- et AMP-ases). Arch. Biol. (Liege)78 (1967) 389–450.
Locy, W. A., On a newly recognized nerve connected with the forebrain of the selachian. Anat. Anz.26 (1905) 33–63.
Magrassi, L., and Graziedei, P. P. C., Interaction of the transplanted olfactory placode with the optic stalk and the diencephalon inXenopus laevis embryos. Neuroscience15 (1985) 903–921.
Mendoza, A. S., Breipohl, W., and Miragall, F., Cell migration from the chick olfactory placode: a light and electron microscope study. J. Embryol. exp. Morphol.69 (1982) 47–59.
Milaire, J., Histochemical aspects of organogenesis in vertebrates. Part I. The sense organs, in: Handbuch der Histochemie, vol. VIII, Suppl. Part 3, pp. 61–74. Gustav Fischer Verlag, Stuttgart 1974.
Moss, R. L. and McCann, S. M., Induction of mating behavior in rats by luteinizing hormone-releasing factor. Science181 (1973) 177–179.
Munz, H., and Class, B., The terminal nerve and its development in teleost fishes, in: The Terminal Nerve (Nervus Terminalis): Structure, Function and Evolution. Eds L. S. Demski and M. Schwanzel-Fukuda. Annls N.Y. Acad. Sci.519 (1987) 50–59.
Muske, L., and Moore, F. L., Luteinizing hormone-releasing hormone immunoreactive neurons in the amphibian brain are distributed along the course of the nervus terminalis, in: The Terminal Nerve (Nervus Terminalis) Structure, Function and Evolution. Eds L. S. Demski and M. Schwanzel-Fukuda. Annls N. Y. Acad. Sci.519 (1987) 433–446.
Muske, L., and Moore, F. L., The nervus terminalis in amphibians: anatomy, chemistry and relationship with the hypothalamic gonadotropin-releasing hormone system. Brain Behav. Evol.32 (1988) 141–148.
Oelschlager, H. A., and Buhl, E. H., Development and rudimentation of the peripheral olfactory system in the harbor porpoisePhocoena Phocoena (Mammalia: Cetacea). J. Morph.184 (1985) 351–360.
O'Rahilly, R., the early development of the nasal pit in staged human embryos. Anat. Rec.157 (1972) 380.
Paulin, C., Dubois, M. P., Barry, J., and Dubois, P. M., Immunofluorescence study of LH-RH producing cells in the human fetal hypothalamus. Cell Tiss. Res.182 (1977) 341–345.
Pearson, A. A., The development of the nervus terminalis in man. J. comp. Neurol.75 (1941) 39–66.
Pearson, A. A., The development of the olfactory nerve in man. J. comp. Neurol.75 (1941) 199–217.
Pfaff, D. W., Luteinizing hormone-releasing factor potentiates lordosis behavior in hypophysectomized ovariectomized female rats. Science182 (1973) 1148–1149.
Ridgway, S. H., Demski, L. S., Bullock, T. H., and Schwanzel-Fukuda, M., The terminal nerve in odontocete cetaceans, in: The Terminal Nerve (Nervus Terminalis): Structure, Function and Evolution. Eds L. S. Demski and M. Schwanzel-Fukuda. Annls N.Y. Acad. Sci.519 (1987) 201–212.
Roth, J., LeRoith, D., Shiloach, J., Rosenzweig, J. L., Lesniak, M. A., and Havrankova, J., The evolutionary origins of hormones, neurotransmitters and other extracellular chemical messengers. New Engl. J. Med.306 (1982) 523–527.
Ronnekeiv, O., and Resco, J. A., Ontogeny of gonadotropin-releasing hormone-containing neurons in early fetal development of rhesus macaques. Endocrinology126 (1990) 498–511.
Schally, A. V., Arimura, A., Kastin, A. J., Matsuo, H., Baba, Y., Redding, T. W., Nair, R. M. G., and Debelchuk, L., Gonadotropin-releasing hormone: one polypeptide regulates secretion of luteinizing hormone and follicle-stimulating hormone. Science173 (1971) 1036–1038.
Schwanzel-Fukuda, M., and Silverman, A.-J., The nervus terminalis of the guinea pig: a new luteinizing hormine-releasing hormone (LHRH) neuronal system. J. comp. Neurol.191 (1980) 213–225.
Schwanzel-Fukuda, M., Robinson, J. A., and Silverman, A.-J., The fetal development of the luteinizing hormone-releasing hormone (LHRH) neuronal systems of the guinea pig brain. Brain Res. Bull.7 (1981) 293–315.
Schwanzel-Fukuda, M., Morrell, J. I., and Pfaff, D. W., Ontogenesis of neurons producing luteinizing hormone-releasing hormone (LHRH) in the rat. J. comp. Neurol.238 (1985) 348–364.
Schwanzel-Fukuda, M., Fadem, B. H., Garcia, M. S., and Pfaff, D. W., Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the brain and nervus terminalis of the adult and early neonatal gray short-tailed opossum (Monodelphis domestica). J. comp. Neurol.276 (1988) 44–60.
Schwanzel-Fukuda, M., Garcia, M. S., Morrell, J. I., and Pfaff, D. W., Distribution of luteinizing hormone-releasing hormone in the nervus terminalis and brain of the mouse detected by immunocytochemistry. J. comp. Neurol.255 (1985) 231–244.
Schwanzel-Fukuda, M., and Pfaff, D. W., A proposed migratory route for luteinizing hormone-releasing hormone (LHRH) neurons from the medial olfactory placode to the forebrain in the mouse. Soc. Neurosci. Abstr.14 (1988) 984.
Schwanzel-Fukuda, M., and Pfaff, D. W., Origin of luteinizing hormone-releasing hormone neurons. Nature (Lond.)338 (1989) 161–164.
Schwanzel-Fukuda, M., Bick, D., and Pfaff, D. W., Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Molec. Brain Res.6 (1989) 311–326.
Sherwood, N., The GnRH family of peptides. Trends Neurosci.10 (1987) 129–132.
Silverman, A.-J., The gonadotropin-releasing hormone (GnRH) Neuronal Systems: Immunocytochemistry, in: The Physiology of Reproduction, pp. 1283–1304. Eds E. Knobil and J. Neill. Raven Press, New York 1988.
Stout, R. P., and Graziedei, P. P. C., Influence of the olfactory placode on the development of the brain inXenopus laevis (Daudin). I. Axonal growth and connections of the transplanted olfactory placode. Neuroscience5 (1980) 2175–2186.
Van Campenhout, E., Le développement du système nerveux cranien chez le poulet. Arch. Biol.48 (1937) 611–666.
Wesolowski, H., Morphological and histochemical studies on the development of the olfactory epithelium in the hen. Folia biol.18 (1970) 71–80.
Wirsig, C. R., and Leonard, C. M., Terminal nerve damage impairs the mating behavior of the male hamster. Brain Res.417 (1987) 293–303.
Witkin, J. W., Luteinizing hormone-releasing hormone (LHRH) in olfactory systems in primates, in: The Terminal Nerve (Nervus Terminalis): Structure, Function and Evolution. Eds L. S. Demski and M. Schwanzel-Fukuda. Annls N.Y. Acad. Sci.519 (1987) 174–183.
Witkin, J. W., and Silverman, A.-J., Luteinizing hormone-releasing hormone (LHRH) in rat olfactory systems. J. comp. Neurol.218 (1983) 426–432.
Wray, S., Nieburgs, A., and Elkabes, S., Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode. Dev. Brain Res.46 (1989) 309–318.
Wray, S., Grant, P., and Gainer, H., Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc. natl Acad. Sci. USA86 (1989) 8132–8136.
Zheng, L. M., Pfaff, D. W., and Schwanzel-Fukuda, M., Electron microscopic identification of luteinizing hormone-releasing hormone (LHRH) immunoreactivity in olfactory placode-derived neurons. Soc. Neurosci. Abstr.15 (1989) 1015.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Schwanzel-Fukuda, M., Pfaff, D.W. The migration of luteinizing hormone-releasing hormone (LHRH) neurons from the medial alfactory placode into the medial basal forebrain. Experientia 46, 956–962 (1990). https://doi.org/10.1007/BF01939389
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF01939389