Skip to main content

The Biochemistry of Olfactory Neurons: Stages of Differentiation and Neuronal Subsets

  • Chapter

Abstract

The sensory neurons of the olfactory epithelium demonstrate two remarkable characteristics. First, although each individual neuron has a restricted (yet broadly tuned) sensitivity to odorants, as a population they are capable of transducing literally millions of odorants and, in response to these odorants, generating differential patterns of neuronal activity that permit the discrimination of olfactory stimuli by higher centers. The selective responsivity of individual neurons, in combination with the breadth of sensitivity provided by the population of neurons in aggregate, is highly reminiscent of the immune system. However, odorant receptor molecules have not yet been unambiguously identified, and the generation of odorant response diversity during neuronal development is poorly understood as a consequence (see the chapter by Anholt in the present volume). Second, olfactory neurons are the only neurons in the mature mammalian nervous system that can be replaced when they die. A population of stem cells is present in the olfactory epithelium from which new neurons can differentiate to substitute for those sensory cells that die as a consequence of damage, either mechanical or chemical, or at the end of their “natural” lifespan.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akeson, R.A., and S.L. Haines (1989). Rat olfactory cells and a central nervous system neuronal subpopulation share a cell surface antigen. Brain Res., 488: 202–212.

    PubMed  CAS  Google Scholar 

  • Allen, W.K., and R. Akeson (1985a). Identification of a cell surface glycoprotein family of olfactory receptor neurons with a monoclonal antibody. J. Neurosci., 5: 284–296.

    PubMed  CAS  Google Scholar 

  • Allen, W.K., and R. Akeson (1985b). Identification of an olfactory receptor neuron subclass: Cellular and molecular analysis during development. Dev. Biol., 109: 393–401.

    PubMed  CAS  Google Scholar 

  • Astic, L., and D. Saucier (1983). Ontogenesis of the functional activity of guineapig olfactory bulb: Autoradiography study with the 2-deoxyglucose method. Dev. Brain Res., 10: 257–263.

    Google Scholar 

  • Astic, L., and D. Saucier (1986). Anatomical mapping of the neuroepithelial projection to the olfactory bulb in the rat. Brain Res. Bull., 16: 445–454.

    PubMed  CAS  Google Scholar 

  • Astic, L., D. Saucier, and A. Holley (1987). Topographical relationships between olfactory receptor cells and glomerular foci in the rat olfactory bulb. Brain Res., 424: 144–152.

    PubMed  CAS  Google Scholar 

  • Astic, L., J. LePendu, R. Mollicone, D. Saucier, and R. Oriol (1989). Cellular expression of H and B Antigens in the rat olfactory system during development. J. Comp. Neurol., 289: 386–394.

    PubMed  CAS  Google Scholar 

  • Barber, P.C. (1989). Ulex Europeus Agglutinin I binds exclusively to primary olfactory neurons in the rat nervous system. Neuroscience, 30: 1–9.

    PubMed  CAS  Google Scholar 

  • Beeley, J.G. (1985). Glycoprotein and Proteoglycan Techniques, in R.H. Burdon and P.H. van Knippenberg (Eds), Laboratory Techniques in Biochemistry and Molecular Biology. New York: Plenum.

    Google Scholar 

  • Benson, T.E., G.D. Burd, C.A. Greer, D.M.D. Landis, and G.M. Shepherd (1985). High-resolution 2-deoxyglucose autoradiography in quick frozen slabs of neonatal rat olfactory bulbs. Brain Res., 339: 67–78.

    PubMed  CAS  Google Scholar 

  • Brockes, J.P. (1989). Retinoids, homeobox genes, and limb morphogenesis. Neuron, 2: 1285–1294.

    PubMed  CAS  Google Scholar 

  • Brown, D., L.-M. Garia-Sequra, and L. Orci (1984). Carbonic anhydrase is present in olfactory receptor cells. Histochemistry, 80: 307–309.

    PubMed  CAS  Google Scholar 

  • Calof, A.L., and D.M. Chikaraishi (1989). Analysis of neurogenesis in a mammalian neuroepithelium: Proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron, 3: 115–127.

    PubMed  CAS  Google Scholar 

  • Camara, C.G., and J.W. Harding (1984). Thymidine incorporation in the olfactory epithelium of mice: Early exponential response induced by olfactory neurectomy. Brain Res., 308: 63–68.

    PubMed  CAS  Google Scholar 

  • Carr, V.M., A.I. Farbman, M.S. Lidow, L.M. Colletti, J.L. Hempstead, and J.I. Morgan (1989). Developmental expression of reactivity to monoclonal antibodies generated against olfactory epithelia. J. Neurosci., 9: 1179–1198.

    PubMed  CAS  Google Scholar 

  • Chuah, M.I., and A.I. Farbman (1983). Olfactory bulb increases marker protein in olfactory receptor cells. J. Neurosci., 3: 2197–2205.

    PubMed  CAS  Google Scholar 

  • Clancy, A.N., T.A. Schoenfeld, and F. Margolis (1985). Topographic organization of peripheral input to the hamster main olfactory bulb. Chem. Senses, 10: 399–400.

    Google Scholar 

  • Cochard, P., and D. Paulin (1984). Initial expression of neurofilaments and vimentin in the central and peripheral nervous system of the mouse embryo in vivo. J. Neurosci., 4: 2080–2094.

    PubMed  CAS  Google Scholar 

  • Coopersmith, R., S.R. Henderson, and M. Leon (1986). Odor specificity of the enhanced neural response following early odor experience in rats. Brain Res., 392: 191–197.

    PubMed  CAS  Google Scholar 

  • Costanzo, R.M., and M.M. Mozell(1976). Electrophysiological evidence for a topographical projection of the nasal mucosa onto the olfactory bulb of the frog. J. Gen. Physiol., 68: 297–312.

    PubMed  CAS  Google Scholar 

  • Costanzo, R.M., and R.J. O’Connell (1978). Spatially organized projections of hamster olfactory nerves. Brain Res., 139: 327–332.

    PubMed  CAS  Google Scholar 

  • Costanzo, R.M., and P.P.C. Graziadei (1983). A quantitative analysis of changes in the olfactory epithelium following bulbectomy in hamster. J. Comp. Neurol., 215: 370–381.

    PubMed  CAS  Google Scholar 

  • Couly, G.F., and N.M. LeDouarin (1985). Mapping of the early neural primordium in quail-chick chimeras. I. Developmenlal relationships between placodes, facial ectoderm, and prosencephalon. Dev. Biol., 110: 422–439.

    PubMed  CAS  Google Scholar 

  • Croul-Ottman, C.E., and P.C. Brunjes (1988). NADPH diaphorase staining within the developing olfactory bulbs of normal and unilaterally odor-deprived rats. Brain Res., 460: 323–328.

    PubMed  CAS  Google Scholar 

  • Cusehieri, A., and L.H. Bannister (1975). The development of the olfactory mucosa in the mouse: Light microscopy. J. Anat., 119: 277–286.

    Google Scholar 

  • Dodd, J., D. Solter, and T.M. Jessell (1984). Monoclonal antibodies against carbohydrates differentiation antigens identify subsets of primary sensory neurons. Nature, 311: 469–472.

    PubMed  CAS  Google Scholar 

  • Dodd, J., and T.M. Jessell (1985). Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal cord. J. Neurosci., 5: 3278–3294.

    PubMed  CAS  Google Scholar 

  • Dulbecco, R., R. Allen, S. Okada, and M. Bowman (1983). Functional changes of intermediate filaments in fibroblastic cells revealed by a monoclonal antibody. Proc. Natl. Acad. Sci. USA, 88: 1915–1918.

    Google Scholar 

  • Edelman, G.M., S. Hoffman, C.-M. Chuong, J.-P. Thiery, R. Brackenbury, W.J. Gallin, M. Grumet, M.E. Greenberg, J.J. Hemperly, C. Cohen, and B.A. Cunningham (1983). Structure and modulation of neural cell adhesion molecules in early and late embryogenesis. Cold Spring Harbor. Symp. Quant. Biol., 48: 515–526.

    CAS  Google Scholar 

  • Edwards, D.A., R.A. Mather, and G.H. Dodd (1988). Spatial variation in response to odorants of the rat olfactory epithelium. Experientia, 44: 208–211.

    PubMed  CAS  Google Scholar 

  • Farbman, A.I. (1986). Prenatal development of mammalian olfactory receptor cells. Chem. Senses, 11: 3–18.

    Google Scholar 

  • Farbman, A.I., and F.L. Margolis (1980). Olfactory marker protein during ontogeny: immunohistochemical localization. Dev. Biol., 74: 111–121.

    Google Scholar 

  • Gesteland, R.C., R.A. Yancey, and A.I. Farbman (1982). Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience, 7: 3127–3136.

    PubMed  CAS  Google Scholar 

  • Graziadei, P.P.C., and G.A. Monti Graziadei (1979). Neurogenesis and neuron regeneration in the olfactory system of mammals. 1. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8: 1–18.

    PubMed  CAS  Google Scholar 

  • Hempstead, J.L., and J.I. Morgan (1985a). A panel of monoclonal antibodies to the rat olfactory epithelium. J. Neurosci., 5: 438–449.

    PubMed  CAS  Google Scholar 

  • Hempstead, J.L., and J.I. Morgan (1985b). Monoclonal antibodies reveal novel aspects of the biochemistry and organization of olfactory neurons following unilateral olfactory bulbectomy. J. Neurosci. 5: 2382–2387.

    PubMed  CAS  Google Scholar 

  • Hinds, J.W., P.L. Hinds, and N.A. McNelly (1984). An autoradiographic study of the mouse olfactory epithelium: Evidence for long-lived receptors. Anat. Rec., 210: 375–383.

    PubMed  CAS  Google Scholar 

  • Hynes, M.A., L.B. Buck, M. Gitt, S. Barondes, J. Dodd, and T.M. Jessell (1989). Carbohydrate recognition in neuronal development: structure and expression of surface oligosaccharides and beta-galactoside-binding lectins. CIBA. Found. Symp., 148: 189–210.

    Google Scholar 

  • Jourdan, F. (1982). Spatial dimension in olfactory coding: a representation of the 2-deoxyglucose patterns of glomerular labeling in the olfactory bulb. Brain Res., 240: 341–344.

    PubMed  CAS  Google Scholar 

  • Jourdan, R., A. Duveau, L. Astic, and A. Holley (1980). Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours. Brain Res., 188: 139–154.

    PubMed  CAS  Google Scholar 

  • Kent, P.F. (1990). The recording of odorant induced activity patterns from the olfactory mucosa using a voltage sensitive dye. Unpublished Ph.D. Thesis, SUNY Health Science Center, Syracuse.

    Google Scholar 

  • Key, B., and P.P. Giorgi (1986a). Selective binding of soybean agglutinin to the olfactory system of xenopus. Neuroscience, 18: 507–515.

    PubMed  CAS  Google Scholar 

  • Key, B., and P.P. Giorgi (1986b). Soybean agglutinin binding to the olfactory systems of the rat and mouse. Neurosci. Lett., 69: 131–136.

    PubMed  CAS  Google Scholar 

  • Kroczek, R.A., K.C. Gunter, R.N. Germain, and E.M. Shevach (1986). Thy-1 functions as a signal transduction molecule in T-lymphocytes and transfected B-lymphocytes. Nature, 322: 181–184.

    PubMed  CAS  Google Scholar 

  • Laing, D.G., H. Panhuber, E.A. Pittman, M.E. Willcox, and G.K. Eagleson (1985). Prolonged exposure to an odor or deodorized air alters size of mitral cells in the olfactory bulb. Brain Res., 336: 81–87.

    PubMed  CAS  Google Scholar 

  • Lancet, D., C.A. Greer, J.S. Kauer, and G.M. Shepard (1982). Mapping of odor-related neuronal activity in the olfactory bulb by high-resolution 2-deoxyglucose autoradiography. Proc. Natl. Acad. Sci. USA, 79: 670–674.

    PubMed  CAS  Google Scholar 

  • Lazarides, E. (1980). Intermediate filaments as mechanical integrators of cellular space. Nature, 283: 249–256.

    PubMed  CAS  Google Scholar 

  • LeGros Clark, W. (1957). Inquiries into the anatomical basis of olfactory discrimination. Proc. R. Soc. Med., 146: 299–319.

    Google Scholar 

  • Lidow, M.S., S.J. Kleene, and R.C. Gesteland (1986). Suppression of mitotic acitvity and synchronization of cell development in olfactory epithelium. Brain Res., 393: 145–162.

    PubMed  CAS  Google Scholar 

  • Lovell, M.A., B.W. Jafek, D.T. Moran, and J.C. Rowley, III (1982). Biopsy of human olfactory mucosa: An instrument and a technique. Arch. Otolarygol., 108: 247–249.

    CAS  Google Scholar 

  • Mackay-Sim, A., P. Shaman, and D.G. Moulton (1982). Topographic coding of olfactory quality: Odorant-specific patterns of epithelial responsivity in the salamander. J. Neurophysiol, 48: 584–596.

    PubMed  CAS  Google Scholar 

  • Margolis, F.L. (1985). Olfactory marker protein: from PAGE band to cDNA clone. Trends Neurosci., 8: 542–546.

    CAS  Google Scholar 

  • Margolis, F.L. (1988). Molecular cloning of olfactory-specific gene products. in F.L. Margolis and T.V. Getchall (Eds.) Molecular Neurobiology of the olfactory system. New York: Plenum, pp. 237–265.

    Google Scholar 

  • Matus, A. (1988). Micro tubule-associated proteins: Their potential role in determining neuronal morphology. Ann. Rev. Neurosci., 11: 29–44.

    PubMed  CAS  Google Scholar 

  • Mein, K.F., K.H. Pfenninger, and M. Willard (1986). Growth associated protein, GAP-43, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction that is enriched in growth cones. Proc. Natl. Acad. Sci. USA, 83: 3537–3541.

    Google Scholar 

  • Meiri, K.F., M. Willard, and M.I. Johnson (1988). Distribution and phosphorylation of the growth associated protein GAP-43 in regenerating sympathetic neurons in culture. J. Neurosci., 8: 3537–3542.

    Google Scholar 

  • Meiri, K.F., and P.R. Gordon-Weeks (1990). GAP-43 in growth cones is associated with areas of membrane that are tightly bound to substrate and is a component of a membrane skeleton subcellular fraction. J. Neurosci., 10: 256–266.

    PubMed  CAS  Google Scholar 

  • Meiri, K.F., and L.E. Bickerstaff, and J.E. Schwob (1991). Monoclonal antibodies show that Kinase C phosphorylation of GAP-43 during axonogenesis is both spatially and temporally restricted in vivo. J. Cell Biol., 112: 991–1005.

    PubMed  CAS  Google Scholar 

  • Menco, B.M. (1989). Electron-microscopic demonstration of olfactory-marker protein with protein G-gold in freeze-substituted, Lowicryl K11M-embedded rat olfactory-receptor cells. Cell Tiss. Res., 256: 275–281.

    CAS  Google Scholar 

  • Menco, B.M., and A.I. Farbman (1985). Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. J. Cell Sci., 78: 283–310.

    PubMed  CAS  Google Scholar 

  • Miragall, F., G. Kadmon, M. Husmann, and M. Schachner (1988). Expression of cell adhesion molecules in the olfactory system of the adult mouse: Presence of the embryonic form of N-CAM. Dev. Biol., 129: 516–531.

    PubMed  CAS  Google Scholar 

  • Mitchison, T., and M. Kirschner (1988). Cytoskeletal dynamics and nerve growth. Neuron, 1: 761–772.

    PubMed  CAS  Google Scholar 

  • Mollicone, R., J. Trojan, and R. Oriol (1985). Appearance of H and B antigens in primary sensory cells of the rat olfactory apparatus and inner ear. Dev. Brain Res., 17: 275–279.

    Google Scholar 

  • Monti Graziadei, G.A. (1983). Experimental studies on the olfactory marker protein. III. The olfactory marker protein in the olfactory neuroepithelium lacking connections with the forebrain. Brain Res., 262: 303–308.

    PubMed  CAS  Google Scholar 

  • Monti Graziadei, G.A., F.L. Margolis, J.W. Harding, and P.P.C. Graziadei (1977). Immunocytochemistry of the olfactory marker protein. J. Histochem. Cytochem., 25: 1311–1316.

    PubMed  CAS  Google Scholar 

  • Mori, K. (1987). Monoclonal antibodies (2C5 and 4C9) against lactorseries carbohydrates identify subsets of olfactory and vomeronasal receptor cells and their axons in the rabbit. Brain Res., 408: 215–221.

    PubMed  CAS  Google Scholar 

  • Mori, K., S.C. Fujita, K. Imamura, and K. Obata (1985). Immunohistochemical study of subclasses of olfactory nerve fibers and their projections to the olfactory bulb in the rabbit. J. Comp. Neurol., 242: 214–229.

    PubMed  CAS  Google Scholar 

  • Mori, K., K. Imamura, S.C. Fujita, and K. Obata (1987). Projections of two subclasses of vomeronasal nerve fibers to the accessory olfactory bulb in the rabbit. Neuroscience, 20: 259–278.

    PubMed  CAS  Google Scholar 

  • Mori, K., K. Imamura, and N. Onoda (1990). Signal processing in the rabbit olfactory bulb. Proceedings, ISOTX. In press.

    Google Scholar 

  • Morris, R.J. (1985). Thy-1 in developing nervous tissue. Dev. Neurosci., 7: 133–160.

    PubMed  CAS  Google Scholar 

  • Morris, R.J., and P.C. Barber (1983). Fixation of Thy-1 in nervous tissue for immunohistochemistry: A quantitative assessment of the effect of different fixation conditions upon retention of antigenicity and the cross-linking of Thy-1. J. Histochem. Cytochem., 31: 263–21A.

    PubMed  CAS  Google Scholar 

  • Moulton, D.G. (1976). Spatial patterning of response to odors in the peripheral olfactory system. Physiol. Rev., 56: 578–593.

    PubMed  CAS  Google Scholar 

  • Naessen, R. (1971). An enquiry of the morphological characteristics and possible changes with age in the olfactory region of man. Acta Otolaryngol., 71: 49–62.

    PubMed  CAS  Google Scholar 

  • Nakashima, T., C.P. Kimmelman, and J.B. Snow, Jr. (1984). Structure of human fetal and adult olfactory neuroepithelium. Arch. Otolaryngol., 110: 641–646.

    PubMed  CAS  Google Scholar 

  • Ophir, D., and D. Lancet (1988). Expression of intermediate filaments and desmoplakin in vertebrate olfactory mucosa. Anat. Rec., 221: 754–760.

    PubMed  CAS  Google Scholar 

  • Onoda, N. (1988a). Monoclonal antibody immunohistochemistry of rabbit olfactory receptor neurons during development. Neuroscience, 26: 1003–1012.

    PubMed  CAS  Google Scholar 

  • Onoda, N. (1988b). Monoclonal antibody immunohistochemistry of degenerative and renewal pattern in rabbit olfactory receptor neurons following unilateral olfactory bulbectomy. Neuroscience, 26: 1013–1022.

    PubMed  CAS  Google Scholar 

  • Onoda, N., and S.C. Fujita (1988). Monoclonal antibody immunohistochemistry of adult rabbit olfactory structures. Neuroscience, 26: 993–1002.

    PubMed  CAS  Google Scholar 

  • Osborn, M., E. Debus, and K. Weber (1984). Monoclonal antibodies specific for vimentin. Eur. J. Cell. Biol., 34: 137–143.

    PubMed  CAS  Google Scholar 

  • Panhuber, H., and D.G. Laing (1987). The size of mitral cells is altered whem rats are exposed to an odor from their day of birth. Dev. Brain Res., 34: 133–140.

    Google Scholar 

  • Panhuber, H., A. Mackay-Sim, and D.G. Laing (1987). Prolonged odor exposure causes cell shrinkage in the adult rat olfactory bulb. Dev. Brain Res., 31: 307–311.

    Google Scholar 

  • Pedersen, P.E., B. Friedman, R. Smith, C.A. Greer, G.M. Shepherd, and S. Hockfield (1987). Correlations between 2DG activity and monoclonal antibody staining in the olfactory system of the fetal rat. Soc. Neurosci. Abstr., 13: 363.

    Google Scholar 

  • Reinhard, E., R. Meier, W. Halfter, G. Rovelli, and D. Monard (1988). Detection of glia-derived nexin in the olfactory system of the rat. Neuron, 1: 387–394.

    PubMed  CAS  Google Scholar 

  • Riggot, M.J., and J.W. Scott (1989). Lectin labeling of rat olfactory bulb glomeruli. Soc. Neurosci. Abstr., 15: 926.

    Google Scholar 

  • Royet, J.P., G. Sicard, C. Souchier, and F. Jourdan (1987). Specificity of spatial patterns of glomerular activation in the mouse olfactory bulb: computer-assisted image analysis of 2-deoxyglucose autoradiogams. Brain Res., 417: 1–11.

    PubMed  CAS  Google Scholar 

  • Rutishauser, U., and T.M. Jessell (1988). Cell adhesion molecules in vertebrate neural development. Physiol. Rev., 68: 819–857.

    PubMed  CAS  Google Scholar 

  • Schoenfeld, T.A., L. McKerracher, R. Obar, and R.B. Vallee (1989). MAP 1A and MAP 1B are structurally related microtubule associated proteins with distinct developmental proteins in the CNS. J. Neurosci., 9: 1712–1730.

    PubMed  CAS  Google Scholar 

  • Schwarting, G.A., and J.E. Crandall (1989). Monoclonal antibodies to carbohydrate antigens identify subsets of olfactory and vomeronasal axons in the rat. Soc. Neurosci. Abstr., 15: 590.

    Google Scholar 

  • Schwartz, M.A., D.M. Chikaraishi, and J.S. Kauer (1989). Characterization of the precursor population in mouse olfactory epithelium after bulbectomy. Soc. Neurosci. Abstr., 15: 749.

    Google Scholar 

  • Schwob, J.E., and D.I. Gottlieb (1986). The primary olfactory projection has two chemically distinct zones. J. Neurosci., 6: 3393–3404.

    PubMed  CAS  Google Scholar 

  • Schwob, J.E., N.B. Farber, and D.I. Gottlieb (1986). Neurons of the olfactory epithelium in adult rats contain vimentin. J. Neurosci., 6: 208–217.

    PubMed  CAS  Google Scholar 

  • Schwob, J.E., and D.I. Gottlieb (1988). Purification and characterization of an antigen that is spatially segregated in the primary olfactory projection. J. Neurosci., 8: 3470–3480.

    PubMed  CAS  Google Scholar 

  • Schwob, J.E., K.E. Szumowski, and K.B. Brodie (1988). Differentiation of olfactory sensory neurons in the absence of their postsynaptic target. Soc. Neurosci. Abstr., 14: 1169.

    Google Scholar 

  • Schwob, J.E., and K.E. Szumowski (1989). Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. Soc. Neurosci. Abstr., 15: 749.

    Google Scholar 

  • Sicard, G. (1985). Olfactory discrimination of structurally related molecules: Receptor cell responses to camphoraceous odorants. Brain Res., 326: 203–212.

    PubMed  CAS  Google Scholar 

  • Sicard, G., and A. Holley (1984). Receptor cell responses to odorants: similarities and differences among odorants. Brain Res., 292: 283–296.

    PubMed  CAS  Google Scholar 

  • Skene, J.H.P. (1989). Axonal growth-associated proteins. Ann. Rev. Neurosci., 12: 127–156.

    PubMed  CAS  Google Scholar 

  • Smart, I.H.M. (1971). Location and orientation of mitotic figures in the developing mouse olfactory epithelium. J. Anat., 109: 243–251.

    PubMed  CAS  Google Scholar 

  • Smith, C.G. (1936). Pathologic change in olfactory nasal mucosa of albino rats with “stunted” olfactory bulbs. Arch. Otolaryngol., 25: 131–143.

    Google Scholar 

  • Stallcup, W.B., L.L. Beasley, and J.M. Levine (1985). Antibody against nerve growth factor—inducible large external (NILE) glycoprotein labels nerve fiber tracts in the developing nervous system. J. Neurosci., 5: 1090–1101.

    PubMed  CAS  Google Scholar 

  • Stewart, W.B., J.S. Kauer, and G.M. Shepherd (1979). Functional organization of rat olfactory bulb analysed by the 2-deoxyglucose method. J. Comp. Neurol., 185: 715–734.

    PubMed  CAS  Google Scholar 

  • Stewart, W.B., and P.E. Pedersen (1987). The spatial organization of olfactory nerve projections. Brain Res., 411: 248–258.

    PubMed  CAS  Google Scholar 

  • Talamo, B.R., R. Rudel, K.S. Kosik, V.M.-Y. Lee, S. Neff, L. Adelman, and J.S. Kauer (1989). Pathological changes in olfactory neurons in patients with Alzheimer’s disease. Nature, 337: 736–739.

    PubMed  CAS  Google Scholar 

  • Verhaagen, J., A.B. Oestreicher, W.H. Gispen, and F.L. Margolis (1989a). The expression of the growth associated protein B50/GAP 43 in the olfactory system of neonatal and adult rats. J. Neurosci., 9: 683–691.

    PubMed  CAS  Google Scholar 

  • Verhaagen, J., A.B. Oestricher, M. Grillo, Y.-S. Khew-Goodall, W.H. Gispen, and F.L. Margolis (1989b). Differential post-lesion expression of B-50/GAP-43 and olfactory marker protein in the olfactory system. Soc. Neurosci. Abstr., 15: 318.

    Google Scholar 

  • Viereck, C., R.P. Tucker, and A. Matus (1989). The adult rat olfactory system expresses microtubule-associated proteins found in the developing brain. J. Neurosci., 9: 3547–3557.

    PubMed  CAS  Google Scholar 

  • Vollrath, M., M. Altmannsberger, K. Weber, et al. (1985). An ultrastructural and immunohistological study of the rat olfactory epithelium: Unique properties of olfactory sensory cells. Differen. 29: 243–253.

    CAS  Google Scholar 

  • Wallis, I., L. Ellis, K. Suh, and K.H. Pfenninger (1985). Immunolocalization of a neuronal growth-dependent membrane glycoprotein. J. Cell Biol., 101: 1990–1998.

    PubMed  CAS  Google Scholar 

  • Willard, M.B., K. Meiri, and M. Glicksman (1985). Changes of state during neuronal development: Regulation of axon elongation. In G.M. Edelman, W.E. Gall, and W.M. Cowan (Eds.), Molecular Bases of Neural Development, New York: Wiley, pp. 341–362.

    Google Scholar 

  • Wysocki, C.J., K.M. Korries, and G.K. Beauchamp (1989). Ability to perceive androstenone can be acquired by ostensibly anosmic people. Proc. Natl. Acad. Sci. USA, 86: 7176–7980.

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer-Verlag New York Inc.

About this chapter

Cite this chapter

Schwob, J.E. (1992). The Biochemistry of Olfactory Neurons: Stages of Differentiation and Neuronal Subsets. In: Serby, M.J., Chobor, K.L. (eds) Science of Olfaction. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2836-3_4

Download citation

  • DOI: https://doi.org/10.1007/978-1-4612-2836-3_4

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7690-6

  • Online ISBN: 978-1-4612-2836-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics