Summary
High-voltage transmission electron microscopy and cryo-ultramicrotomy together with scanning electron microscopy and some conventional transmission electron microscopy of ultrathin sections have been applied to the mucous surfaces of bovine olfactory and respiratory epithelia. Distal segments of olfactory cilia tend to run in parallel and could be followed over distances up to about 30 μm using high-voltage electron microscopy. This technique and scanning electron microscopy showed that on average 12–13 of such cilia could be observed per nerve ending. After correction for obscured cilia this number becomes about 17. High-voltage micrographs and micrographs made from sections prepared with a cryo-ultramicrotome showed the presence of electron-lucent pockets inside the olfactory mucus. The latter technique also showed that the mucus itself is not fibrous, but rather a continuum varying in electron density. The mucus layer contains various granular structures. Ciliary and microvillar membranes appear thicker with cryo-ultramicrotomy than when the sections are prepared with conventional techniques. The cores of the axonemal microtubules in olfactory as well as in respiratory cilia are darkly stained with this technique. Vesicles present inside the nerve endings are also darkly stained. Dimensions and some other numerical values of interest in olfaction are presented.
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Allen, R.D.: A reinvestigation of cross-sections of cilia. J. Cell Biol. 37, 825–831 (1968)
Altner, H., Kolnberger, I.: The application of transmission electron microscopy on the study of the olfactory epithelium of vertebrates. In: Methods in olfactory research (D.G. Moulton, A. Turk and J.W. Johnston, Jr., eds.), pp. 163–190. London: Acad. Press 1975
Andres, K.H.: Neue morphologische Grundlagen zur Physiologie des Riechens und Schmeckens. Arch. Oto-Rhino-Laryng. 210, 1–41 (1975)
Andrews, P.M.: A scanning electron microscopic study of the extra pulmonary respiratory tract. Amer. J. Anat. 139, 399–423 (1974)
Barber, V.C.: Cilia in sense organs. In: Cilia and flagella (M.A. Sleigh, ed.), pp. 403–433. London: Acad. Press 1974
Beeston, B.E.P.: High voltage electron microscopy of biological specimens: some practical considerations. J. Microsc. (Oxf.) 98, 402–416 (1972)
Bernhard, W., Viron, A.: Improved techniques for the preparation of ultrathin frozen sections. J. Cell Biol. 49, 731–746 (1971)
Blank, D.L., Gesteland, R.C., Jansyn, E.M., Wagner, A.L.: Stimulus-related activity of olfactory receptor cilia. Fed. Proc. 37, 398, Abstr. 976 (1978)
Boisvieux-Ulrich, E., Sandoz, D., Chailly, B.: A freeze-fracture and thin section study of the ciliary necklace in quail oviduct. Biol. Cell. 30, 245–252 (1977)
Breipohl, W., Bijvank, G.J., Pfefferkorn, G.: Scanning electron microscopy of various sensory receptor cells in different vertebrates. In: Scanning electron microscopy, Vol 7 (O. Johari and I. Corvin, eds.), pp. 557–564. Chicago: IIT Res. Inst. 1974
Breipohl, W., Bijvank, G.J., Zippel, H.P.: Rastermikroskopische Untersuchungen der olfaktorischen Rezeptoren im Riechepithel des Goldfisches (Carassius auratus). Z. Zellforsch. 138, 439–454 (1973)
Breipohl, W., Fernández, M.: Scanning electron microscopic investigations of olfactory epithelium in the chick embryo. Cell Tiss. Res. 183, 105–114 (1977)
Bronshtein, A.A.: Odour receptors of vertebrates. Monograph. Leningrad: Acadamy of Sciences USSR; Institute of comparative physiology and biochemistry 1977
Bronshtein, A.A., Minor, A.V.: The regeneration of olfactory flagella and restoration of electroolfactogram after treatment of the olfactory mucosa with Triton X-100. Tsitologya (SSSR) 19, 33–39 (1977)
Busuttil, A., More, I.A.R., McSeveney, D.: A reappraisal of the ultrastructure of the human respiratory nasal mucosa. J. Anat. (Lond.) 124, 445–458 (1977)
Caprio, J., Raderman-Little, R.: Scanning electron microscopy of the channel catfish olfactory lamellae. Tissue & Cell 10, 1–9 (1978)
Cavalier-Smith, T.: Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J. Cell Sci. 16, 529–556 (1974)
Chapman, D., Wallach, D.F.H.: Recent physical studies of phospholipids and natural membranes. In: Biological membranes. Physical fact and function (D. Chapman, ed.), pp. 125–202. London: Acad. Press 1968
DeLorenzo, A.J.D.: The olfactory neuron and the blood-brain barrier. In: Taste and smell in vertebrates (G.E.W. Wolstenholme and J. Knight, eds.), pp. 151–176. London: J. & A. Churchill1970
Dirksen, R.E.: Centriole morphogenesis in developing ciliated epithelium of the mouse oviduct. J. Cell Biol. 51, 286–302 (1971)
Dodd, G.H.: The adenosine triphosphate activities of the olfactory mucosae of some common animals. Comp. Biochem. Physiol. 36, 633–637 (1970)
Dodson, H.C.: Ultrastructural and autoradiographic studies of the mammalian olfactory system. Ph.D. Thesis Guy's Hospital Medical School 1975
Echlin, P.: Sputter coating techniques for scanning electron microscopy. In: Scanning electron microscopy, Vol. 8 (O. Johari and I. Corvin, eds.), pp. 217–224. Chicago: IIT Res. Inst. 1975
Farvard, P., Carasso, N.: The preparation and observation of thick biological sections in the high voltage electron microscope. J. Microsc. (Oxf.) 97, 59–81 (1973)
Franks, F., Asquith, M.H., Hammond, C.C., Skaer, H. le B., Echlin, P.: Polymeric cryoprotectants in the preservation of biological ultrastructure. I. Low temperature states of aqueous solutions of hydrophilic polymers. J. Microsc. (Oxf.) 110, 223–238 (1977)
Gasser, H.S.: Olfactory nerve fibers. J. gen. Physiol. 39, 473–496 (1956)
Gilula, N.B., Satir, P.: The ciliary necklace. A ciliary membrane specilization. J. Cell Biol. 53, 494–509 (1972)
Glauert, A.M.: The high voltage electron microscope in biology. J. Cell Biol. 63, 717–748 (1974)
Glauert, A.M., Glauert, R.H.: Araldite as an embedding medium for electron microscopy. J. biophys. biochem. Cytol. 4, 191–194 (1958)
Glees, P., Spoerri, P.E.: Surface processes of olfactory receptors. Cell Tiss. Res. 188, 149–152 (1978)
Graziadei, P.P.C.: The olfactory mucosa of vertebrates. In: Handbook of sensory physiology, Vol. IV: Chemical senses, part 1: Olfaction (L.M. Beidler, ed.), pp. 27–58. Berlin-Heidelberg-New York: Springer 1971
Graziadei, P.P.C.: The ultrastructure of vertebrates olfactory mucosa. In: The ultrastructure of sensory organs (I. Friedman, ed.), pp. 267–305. Amsterdam: North-Holland Publ. Co. 1973
Graziadei, P.P.C.: The olfactory organ of vertebrates: A survey. In: Essays on the nervous system (R. Bellairs and E.G. Gray, eds.), pp. 191–222. Oxford: Clarendon Press 1974
Graziadei, P.P.C.: Application of scanning electron microscopy and autoradiography in the study of olfactory mucosa. In: Methods in olfactory research (D.G. Moulton, A. Turk and J.W. Johnston, Jr., eds.), pp. 191–240. London: Acad. Press1975
Graziadei, P., Bannister, L.H.: Some observations on the fine structure of the olfactory epithelium in the domestic duck. Z. Zellforsch. 80, 220–228 (1967)
Heist, H.E., Mulvaney, B.D., Landis, D.J.: Odor sensing cell ultrastructure by electron microscopy. Final report Air Force Scientific Research Contract No. AF49(638)-1618. Hopkins, Minnesota: Honeywell Inc. Corporate Research Center 1967
Holley, A., MacLeod, P.: Transduction et codage des informations olfactives chez les vertébrés. J. Physiol. (Paris) 73, 725–828 (1977)
Ichikawa, M., Ueda, K.: Fine structure of the olfactory epithelium in the goldfish, Carassius auratus. Cell Tiss. Res. 183, 445–455 (1977)
Karnovsky, M.J.: A formaldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137A-138A (1965)
Kerjaschki, D.: Some freeze-etching data on the olfactory epithelium. In: Olfaction and taste, Vol. VI (J. LeMagnen and P. MacLeod, eds.), pp. 75–85. London and Washington: Information Retrieval Ltd. 1978
Kerjaschki, D., Hörandner, H.: The development of mouse olfactory vesicles and their cell contacts: A freeze-etching study. J. Ultrastruct. Res. 54, 420–444 (1976)
Kind, J., Krieg, J.: Unfixierte Cytomembranen in Gefrierultradünnschnitten. Cytobiology 7, 145–151 (1973)
Koyama, N., Sawada, K., Kurihara, K.: Isolation and some properties of plasma membranes from bovine olfactory epithelium. Biochim. biophys. Acta (Amst.) 241, 42–48 (1971)
Kratzing, J.E.: The olfactory mucosa of the sheep. Aust. J. biol. Sci. 23, 447–458 (1970)
Kuhn III, C., Engleman, W.: The structure of the tips of mammalian respiratory cilia. Cell Tiss. Res. 186, 491–498 (1978)
Lenz, H.: The human olfactory surface in the scanning electron microscope. Acta oto-laryng. (Stockh.) 84, 145–154 (1977)
Lewis, E.R., Nemanic, M.K.: Critical point drying techniques. In: Scanning electron microscopy, Vol. 6 (O. Johari and I. Corvin, eds.), pp. 768–774. Chicago: IIT Res. Inst. 1973
Locke, M., Krishnan, N.: Hot alcoholic phosphotungstic acid and uranyl acetate as routine stains for thick and thin sections. J. Cell Biol. 50, 550–557 (1971)
Locke, M., Krishnan, N., McMahon, J.T.: A routine method for obtaining high contrast without staining sections. J. Cell Biol. 50, 540–544 (1971)
Luftig, R.B., Wehrli, E., McMillan, P.N.: The unit membrane: A re-evaluation. Life Sci. 21, 285–300 (1977)
Markham, R., Frey, S., Hills, G.J.: Methods for the enhancement of image detail and accentuation of structure in electron microscopy. Virology 20, 88–102 (1963)
Masson, C., Kouprach, S., Giachetti, I., MacLeod, P.: Relation between intramembranous particle density of frog olfactory cilia and E.O.G. response. In: Olfaction and taste, Vol VI (J. LeMagnen and P. MacLeod, eds.), p. 195. London and Washington: Information Retrieval Ltd. 1978
Menco, B.P.M.: A qualitative and quantitative investigation of olfactory and nasal respiratory mucosal surfaces of cow and sheep based on various ultrastructural and biochemical methods. Communications Agricultural University, Wageningen 77–13, 1–157 (1977)
Menco, B.P.M.: Freeze-etch morphology of olfactory and respiratory nasal hairlets in rat, cow and frog. In: Olfaction and taste, Vol. VI (J. LeMagnen and P. MacLeod, eds.), p. 199. London and Washington: Information Retrieval Ltd. 1978
Menco, B.P.M., Dodd, G.H., Davey, M., Bannister, L.H.: Presence of membrane particles in freezeetched bovine olfactory cilia. Nature (Lond.) 263, 597–599 (1976)
Moran, D.T., Carter Rowley III, J., Zill, S.N., Varela, F.G.: The mechanism of sensory transduction in a mechanoreceptor. J. Cell Biol. 71, 832–847 (1976)
Moran, D.T., Varela, F.H., Carter Rowley III, J.: Evidence for active role of cilia in sensory transduction. Proc. nat. Acad. Sci. (Wash.) 74, 793–797 (1977)
Negus, V.: The comparative anatomy and physiology of the nose and paranasal sinuses. Edinburgh: E. & S. Livingstone 1958
Nermut, M.V.: Negative staining. In: Methodensammlung der Elektronenmikroskopie (G. Schimmel and W. Vogell, eds.), 3.1.2.3. Stuttgart: Wissenschaftliche Verlagsgesellschaft 1973
Nørrevang, A., Wingstrand, K.G.: On the occurrence and structure of choanocyte-like cells in some Echinoderms. Acta zool. (Stockh.) 51, 249–270 (1970)
Ottoson, D., Shepherd, G.M.: Experiments and concepts in olfactory physiology. In: Progress in brain research Vol. 23, Sensory mechanisms (Y. Zotterman, ed.), pp. 83–138. Amsterdam: Elsevier Publ. Co. 1967
Pitelka, D.R.: Basal bodies and root structures. In: Cilia and flagella (M.A. Sleigh, ed.), pp. 437–469. London: Acad. Press 1974
Poulsen, J., Tos, M.: Goblet cells in the developing human nose. Acta oto-laryng. (Stockh.) 80, 434–442 (1975)
Poynder, T.M.: Transduction mechanisms in chemoreception. London: Information Retrieval Ltd. 1974
Saetersdal, T.S., Myklebust, R., Engedal, H., Ødegaarden, S.: Substructure of inner mitochondrial membranes of myocardial cells as shown by cryo-ultramicrotomy. Cell Tiss. Res. 186, 13–24 (1978)
Seifert, K.: Die Ultrastruktur des Riechepithels beim Makrosmatiker. Eine elektronenmikroskopische Untersuchung. Normale und Pathologische Anatomie, Heft 21 (W. Bargmann and W. Doerr, eds.). Stuttgart: Georg Thieme Verlag 1970
Spoendlin, H.: Auditory, vestibular, olfactory and gustatory organs. In: Ultrastructure of the peripheral nervous system and sense organs. Atlas of normal and pathologic anatomy (J. Bischoff, ed.), pp. 173–326, 447. Stuttgart: Georg Thieme Verlag 1970
Summers, K.: The role of flagellar structures in motility. Biochim. biophys. Acta (Amst.) 416, 153–168 (1975)
Tokuyasu, K.T.: Membranes as observed in frozen sections. J. Ultrastruct. Res. 55, 281–287 (1976)
Usukura, J., Yamada, E.: Observations on the membrane fine structure of the newt olfactory cell by freeze replica method. Zool. Mag. (Tokyo) 84, 339 (1975)
Usukura, J., Yamada, E.: Observations on the cytolemma of the olfactory receptor cell in the newt. 1. Freeze replica analysis. Cell Tiss. Res. 188, 83–98 (1978)
Venable, J.H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965)
Vinnikov, Ya.A.: Sensory reception. Cytology, molecular mechanisms and evolution. In: Molecular biology, biochemistry and biophysics, Vol. 17 (A. Kleinzeller, G.F. Springer and H.G. Wittman, eds.). Berlin-Heidelberg-New York: Springer 1974
Vogel, F.: Cryo-ultramicrotomie — eine alternative Präparationsmethode zur konventionellen Objektpräparation in der Elektronenmikroskopie. Acta histochem. (Jena) Suppl. 17, 297–306 (1976
Vogel, F.: Ultrastructure of unfixed plasma membranes in ultrathin frozen sections. J. Microsc. (Oxf.) 110, 277–280 (1977)
Yamamoto, M.: An electron microscopic study of the olfactory mucosa in the bat and rabbit. Arch. histol. jap. 38, 359–412 (1976)
Yamamoto, M., Ueda, K.: Comparative morphology of fish olfactory epithelium-I. Salmoniformes. Bull. Jap. Soc. Sci. Fish. 43, 1163–1174 (1977)
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Menco, B.P.M., Leunissen, J.L.M., Bannister, L.H. et al. Bovine olfactory and nasal respiratory epithelium surfaces. Cell Tissue Res. 193, 503–524 (1978). https://doi.org/10.1007/BF00225347
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DOI: https://doi.org/10.1007/BF00225347