Skip to main content
Log in

Freeze-fracture study of the plasma membranes of the septal olfactory organ of Masera

  • Published:
Journal of Neurocytology

Summary

The olfactory border and the apical cell contacts of the organ of Masera (MO) of the mouse were investigated by freeze-fracture electron microscopy. The olfactory border is mainly composed of the terminals of receptor and supporting cells. Cells with thick microvillus-like projections, though less frequent than the other two cell types, also contribute to the border. Olfactory knobs show transitions between those displaying numerous cilia and those characterized by few or no cilia. The olfactory cilia have a typical necklace of 6–9 rows of particles. The eruption of developing cilia seems to be preceded by the formation of circular arrays of particles. The density of intramembranous particles (IMP) per μm2 in P- and E-faces of the ciliary membranes is 1095 ± 190 and 205 ± 65, respectively. In the microvilli of supporting cells, the density of IMP per μm2 is 1800 ± 270 for the P-face and 570 ± 135 for the E-face. At the base of the supporting cell microvilli, rod-shaped particles are observed. The lateral plasma membranes of these cells bear orthogonal arrays of particles. In the apical region of the MO neuroepithelium, extensive zonulae occludentes are present which seal the intercellular cleft. The zonulae occludentes between supporting and receptor cells are composed of 5–13 junctional strands, usually arranged in an elongate network. Zonulae occludentes between supporting cells are, in addition to the elongate network, also arranged in a mesh-like pattern. Gap junctions, both associated with the zonulae occludentes and independent of them, are occasionally found between supporting cells. The results obtained indicate that important similarities exist between the neuroepithelium of the MO and the olfactory epithelium proper, whereas remarkable differences exist between the MO and the vomeronasal neuroepithelium.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams, D. R. &McFarland, L. Z. (1971) Septal olfactory organ inPeromycus.Comparative Biochemistry and Physiology 40A, 971–4.

    Google Scholar 

  • Anders, J. J. &Brightman, M. W. (1979) Assemblies of particles in the cell membranes of developing, mature and reactive astrocytes.Journal of Neurocytology 8, 777–95.

    PubMed  Google Scholar 

  • Andres, K. H. (1969) Der olfaktorische Saum der Katze.Zeitschrift für Zellforschung und mikroskopische Anatomie 96, 250–74.

    Google Scholar 

  • Barber, P. C. &Raisman, G. (1978) Cell division in the vomeronasal organ of the adult mouse.Brain Research 141, 57–66.

    PubMed  Google Scholar 

  • Bojsen-Møller, F. (1975) Demonstration of terminalis, olfactory, trigeminal and perivascular nerves in the rat nasal septum.Journal of Comparative Neurology 159, 245–56.

    PubMed  Google Scholar 

  • Breipohl, W., Mendoza, A. S. &Miragall, F. (1980) Freeze-etching studies on the ciliary necklace in the rat and chick.Journal of Anatomy 130, 801–7.

    PubMed  Google Scholar 

  • Breipohl, W., Mendoza, A. S. &Miragall, F. (1982) Freeze-fracturing studies on the main and vomeronasal olfactory sensory epithelia in NMRI-mice. InOlfaction and Endocrine Regulation (edited byBreipohl, W.), pp. 309–22. London: IRL Press Ltd.

    Google Scholar 

  • Breipohl, W., Naguro, T. &Miragall, F. (1983) Morphology of the Masera organ in NMRI-mice.Verhandlungen der Anatomischen Gesellschaft (in press).

  • Brown, D. (1978) Freeze-fracture ofXenopus laevis kidney: rod-shaped particles in canalicular membrane of the collecting tubule flask cell.Journal of Ultrastructure Research 63, 35–40.

    PubMed  Google Scholar 

  • Brown, D. &Montesano, R. (1980) Membrane specialization in the rat epididymis. I. Rod-shaped intramembrane particles in the apical (mitochondria-rich) cell.Journal of Cell Science 45, 187–98.

    PubMed  Google Scholar 

  • Dalton, A. T. (1955) A chrome-osmium fixative for electron microscopy.Anatomical Record 121, 281.

    Google Scholar 

  • Eldrup, E., Møllgard, K. &Bindslev, N. (1980) Possible epithelial sodium channels visualized by freeze-fracture.Biochimica et Biophysica Acta 596, 152–7.

    PubMed  Google Scholar 

  • Graziadei, P. P. C. (1977) Functional anatomy of the mammalian chemoreceptor system. InChemical Signals in Vertebrates (edited byMüller-Schwarze, D. &Mozell, M. M.), pp. 435–54. New York: Plenum Press.

    Google Scholar 

  • Graziadei, P. P. C. &Monti Graziadei, G. A. (1978) Continuous nerve cell renewal in the olfactory system. InHandbook of Sensory Physiology, Vol. IX (edited byJacobson, M.), pp. 55–83. Berlin, Heidelberg, New York: Springer Verlag.

    Google Scholar 

  • Hatton, J. D. &Ellisman, M. H. (1981) The distribution of orthogonal arrays and their relationship to intercellular junctions in neuroglia of the freeze-fractured hypothalamo-neurohypophysial system.Cell and Tissue Research 215, 309–23.

    PubMed  Google Scholar 

  • Humbert, F., Pricam, C., Perrelet, A. &Orci, L. (1975) Specific plasma membrane differentiation in the cells of the kidney collecting tubule.Journal of Ultrastructure Research 52, 13–20.

    PubMed  Google Scholar 

  • Katz, S. &Merzel, J. (1977) Distribution of epithelia and glands of the nasal septum mucosa in the rat.Acta anatomica 99, 58–66.

    PubMed  Google Scholar 

  • Kerjaschki, D. &Hörandner, H. (1976) The development of mouse olfactory vesicles and their cell contacts: a freeze-etching study.Journal of Ultrastructure Research 54, 420–44.

    PubMed  Google Scholar 

  • Kerjaschki, D., Sleytr, U. &Stockinger, L. (1972) Oberflächenstrukturen der Riechköpfe des olfaktorischen Epithels im Gefrierätzbild.Naturwissenschaften 59, 314–15.

    PubMed  Google Scholar 

  • Kratzing, J. E. (1978) The olfactory apparatus of the bandicoot (Isoodon macrourus): fine structure and presence of a septal olfactory organ.Journal of Anatomy 125, 601–13.

    PubMed  Google Scholar 

  • Luciano, L. &Reale, E. (1979) A new morphological aspect of the brush cells of the mouse gallblader epithelium.Cell and Tissue Research 201, 37–44.

    PubMed  Google Scholar 

  • Menco, B. Ph. M. (1980a) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory epithelial surfaces of frog, ox, rat and dog. II. Cell apices, cilia and microvilli.Cell and Tissue Research 211, 5–29.

    PubMed  Google Scholar 

  • Menco, B. Ph. M. (1980b) Qualitative and quantitative freeze-fracture studies on olfactory and respiratory epithelial surfaces of frog, ox, rat and dog. IV. Ciliogenesis and ciliary necklaces (including high-voltage observations).Cell and Tissue Research 212, 1–16.

    PubMed  Google Scholar 

  • Miragall, F. (1983) Evidence for orthogonal arrays of particles in plasma membranes of olfactory and vomeronasal sensory neurons of vertebrates.Journal of Neurocytology 12, 567–76.

    PubMed  Google Scholar 

  • Miragall, F., Breipohl, W. &Bhatnagar, K. P. (1979) Ultrastructural investigation on the cell membranes of the vomeronasal organ in the rat: a freeze-etching study.Cell and Tissue Research 200, 397–408.

    PubMed  Google Scholar 

  • Miragall, F., Breipohl, W. &Mendoza, A. S. (1981) Morphological investigations on the rat vomeronasal organ.Verhandlungen der Anatomischen Gesellschaft 75, 967–8.

    Google Scholar 

  • Miragall, F. &Mendoza, A. S. (1982) Intercellular junctions in the rat vomeronasal neuroepithelium. A freeze-fracture study.Journal of Submicroscopic Cytology 14, 597–605.

    PubMed  Google Scholar 

  • Miragall, F., Mendoza, A. S. &Breipohl, W. (1983) Intercellular junctions of the main and vomeronasal olfactory sensory epithelia in rodents. A freeze-fracture study.Verhandlungen der Anatomischen Gesellschaft (in press).

  • Monti Graziadei, G. A. &Graziadei, P. P. C. (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy.Journal of Neurocytology 8, 197–213.

    PubMed  Google Scholar 

  • Moulton, D. G. (1974) Dynamics of cell populations in the olfactory epithelium.Annals of the New York Academy of Sciences 237, 52–61.

    PubMed  Google Scholar 

  • Moulton, D. G. &Beidler, L. M. (1967) Structure and function in the peripheral olfactory system.Physiological Reviews 47, 1–52.

    PubMed  Google Scholar 

  • Naguro, T. &Breipohl, W. (1982) The vomeronasal epithelia of NMRI mouse. A scanning electron-microscopic study.Cell and Tissue Research 227, 519–34.

    PubMed  Google Scholar 

  • Rehn, B., Breipohl, W., Schmidt, C., Schmidt, U. andEffenberger, F. (1981) Chemical blockade of olfactory perception by N-methyl-formimino-methylester in albino mice. II. Light microscopical investigations.Chemical Senses 6, 317–28.

    Google Scholar 

  • Rehn, B., Breipohl, W., Naguro, T. &Schmidt, U. (1982) Effect of N-methyl-formimino-methylester on the vomeronasal neuroepithelium of mice.Cell and Tissue Research 225, 465–8.

    PubMed  Google Scholar 

  • Rodolfo Masera, T. (1943) Su 1ésistenza di un particolare organo olfattivo nel setto nasale della cavia e di altri roditori.Archivio Italiano di Anatomia e di Embriologia 48, 157–212.

    Google Scholar 

  • Satir, B. H. &Satir, P. (1979) Partitioning of intramembrane particles during the freeze-fracture procedure. InFreeze-Fracture: Methods, Artifacts, and Interpretations (edited byRash, J. E. &Hudson, C. S.), pp. 43–9. New York: Raven Press.

    Google Scholar 

  • Schmidt, C., Schmidt, U. &Breipohl, W. (1980) Inhibited olfactory perception in laboratory mice by N-methyl-formimino-methylester. InOlfaction and Taste VI (edited byVan Der Starre, H.), p. 405. London: IRL Press Ltd.

    Google Scholar 

  • Usukura, T. &Yamada, E. (1978) Observations on the cytolemma of the olfactory receptor cell in the newt. I. Freeze replica analysis.Cell and Tissue Research 188, 83–98.

    PubMed  Google Scholar 

  • Wade, J. B. (1976) Membrane structural specialization of the toad urinary bladder revealed by freeze-fracture technique. II. The mitochondria-rich cell.Journal of Membrane Biology 29, 111–26.

    PubMed  Google Scholar 

  • Winans, S. S., Lehman, M. N. &Powers, T. B. (1982) Vomeronasal and olfactory C.N.S. pathways which control male hamster mating behaviour. InOlfaction and Endocrine Regulation (edited byBreipohl, W.), pp. 23–34. London: IRL Press Ltd.

    Google Scholar 

  • Wysocki, C. T. (1979) Neurobehavioral evidence for involvement of the vomeronasal system in mammalian reproduction.Neurosciences and Biobehavioral Reviews 3, 301–41.

    Google Scholar 

  • Wysocki, C. T., Wellington, T. L. &Beauchamp, G. K. (1980) Access of urinary nonvolatiles to the mammalian vomeronasal organ.Science 207, 781–3.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miragall, F., Breipohl, W., Naguro, T. et al. Freeze-fracture study of the plasma membranes of the septal olfactory organ of Masera. J Neurocytol 13, 111–125 (1984). https://doi.org/10.1007/BF01148321

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01148321

Keywords

Navigation