Summary
The olfactory epithelium of the adult hamster (Mesocricetus auratus) was examined with the scanning electron microscope following olfactory nerve axotomy. Axotomy results in retrograde degeneration of mature olfactory neurons. Maximum degeneration was observed around day 4. During the degeneration period the epithelium consists primarily of supporting and basal cells. Microvillar columnar supporting cells were observed to have fine cellular processes extending from their lateral border to neighbouring cells. Supporting cells extended to the basal lamina where they terminated in foot-like processes of variable shapes (club, splay and hook). Basal cells which gave rise to new replacement olfactory neurons were observed near the basal lamina. They had a rough cellular surface covered with small granules and fine cellular extensions. Bowman's gland duct cells extended unbranched through the epithelium where they formed funnel duct openings covered with microvilli. During early recovery periods (5–30 days) the number of olfactory neurons in the lower epithelium region increased. We observed olfactory neurons with developing axon and dendritic processes. Specialized growth cone structures were seen at the tips. Olfactory neuron growth cones were elongated or club-shaped and had a ruffled membrane surface. Several thin filopodia extended from the growth cone and made contact with adjacent cells. At late recovery periods (35–120 days) there was a marked increase in the number of olfactory neurons within the middle and lower epithelium regions. Numerous dendritic processes extended to the epithelial surface and terminated in knob-like ciliated structures. Olfactory axons passed basally, forming small intra-epithelial bundles that penetrated the basal lamina then fasciculated into larger bundles within the lamina propria.
This study provides detailed three-dimensional observations of the olfactory epithelium following neuron injury, and describes neural degenerative changes, replacement of olfactory neurons, development and maturation. In addition, we describe the structure and basal attachment of supporting cells and their glial-like relation with olfactory neurons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Breipohl, W., Bijuank, G. J. &Zipfel, H. P. (1973) Scanning electron microscopy of olfactory receptors inCarassius auratus.Zeitschrift für Zellforschung and mikroskopische Anatomie 138, 439–54.
Breipohl, W., Zippel, H. P., Ruckert, K. &Oggolter, H. (1976) Morphologische und elektrophysiologische Studien zur Struktur und Funktion des Olfakhoresaken und experimentellen Bedingungen.Beitr Elektronenmikrosk Direktabb Oberfl 9, 561–84.
Cancalon, P. (1982) Degeneration and regeneration of olfactory cells induced by ZnSO4 and other chemicals.Tissue and Cell 14, 717–33.
Cancalon, P. (1983) Influence of a detergent on the catfish olfactory mucosa.Tissue and Cell 15, 245–58.
Connors, B. W., Bernardo, L. S. &Price, D. A. (1984) Carbon dioxide sensitivity of dye coupling among glia and neurons of the neocortex.Journal of Neuroscience 4, 1324–30.
Costanzo, R. M. (1984) Comparison of neurogenesis and cell replacement in the hamster olfactory system with and without a target (olfactory bulb).Brain Research 307, 295–301.
Costanzo, R. M. &Graziadei, P. P. C. (1983) A quantitative analysis of changes in the olfactory epithelium following bulbectomy in hamster.Journal of Comparative Neurology 215, 370–81.
Costanzo, R. M. &Morrison, E. E. (1987) The capacity for neurogenesis and axon reconnection persists in the old adult nervous system.Society for Neuroscience Abstracts 13, 1664.
Costanzo, R. M. &Morrison, E. E. (1989) Three-dimensional scanning electron microscopic study of the normal hamster olfactory epithelium.Journal of Neurocytology 18, 381–9.
Grafstein, B. &McQuarie, I. G. (1978) Role of the nerve cell body in axonal regeneration. InNeuronal Plasticity (edited byCotman, C. W.), pp. 155–95. New York: Raven Press.
Graziadei, P. P. C. (1971) Topographical relations between olfactory neurons.Zeitschrift für Zellforschung und mikroskopische Anatomie 118, 449–66.
Graziadei, P. P. C., Levine, R. R. &Monti-Graziadei, G. A. (1979) Plasticity of connections of the olfactory sensory neurons: regeneration into the forebrain following bulbectomy in the neonatal mouse.Neuroscience 4, 713–27.
Graziadei, P. P. C. &Metcalf, J. (1971) Autoradiographic and ultrastructural observations on the frog olfactory mucosa.Zeitschrift für Zellforschung and mikroskopische Anatomie 116, 305–18.
Graziadei, P. P. C. &Monti-Graziadei, G. A. (1978) The olfactory system: A model for the study of neurogenesis and axon regeneration in mammals. InNeuronal Plasticity (edited byCotman, C. W.), pp. 131–53. New York: Raven Press.
Graziadei, P. P. C. &Monti-Graziadei, G. A. (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons.Journal of Neurocytology 8, 1–18.
Ichikawa, M. &Ueda, K. (1977) Fine structure of the olfactory epithelium in the gold fish,Carassius auratus.Cell and Tissue Research 183, 445–55.
Masukawa, L. M., Hedlund, B. &Shepherd, G. M. (1985) Changes in the electrical properties of olfactory epithelial cells in the tiger salamander after olfactory nerve transection.Journal of Neuroscience 5, 136–41.
Matulionis, D. H. (1976) Light and electron microscopic study of the degeneration and early regeneration of olfactory epithelium in the mouse.American Journal of Anatomy 145, 79–99.
Matulionis, D. H., Breipohl, W. &Bhatangar, K. P. (1982) Degeneration and regeneration of olfactory epithelium in the mouse. A scanning electron microscopic study.Annals of Otology, Rhinology and Laryngology (Suppl.)89, 1–12.
Meller, K. (1979) Scanning electron microscope studies on the development of the nervous systemin vivo andin vitro.International Review of Cytology 56, 23–56.
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.
Moulton, D. G. (1974) Dynamics of cell populations in the olfactory epithelium.Annals of the New York Academy of Science 237, 52–61.
Rafols, J. A. &Getchell, T. V. (1983) Morphological relations between the receptor neurons, sustentacular cells and Schwann cells in the olfactory mucosa of the salamander.Anatomical Record 206, 87–101.
Samanen, D. W. &Forbes, W. B. (1984) Replication and differentiation of olfactory receptor neurons following axotomy in the adult hamster: a morphometric analysis of postnatal neurogenesis.Journal of Comparative Neurology 225, 201–11.
Seymour, R. M. &Berry, M. (1975) Scanning and transmission electron microscopic studies of interkinectic nuclear migration in the cerebral vesicles of the rat.Journal of Comparative Neurology 160, 105–26.
Simmons, P. A., Rafols, J. A. &Getchell, T. V. (1981) Ultrastructural changes in olfactory receptor neurons following olfactory nerve section.Journal of Comparative Neurology 197, 237–57.
Trotier, D. &MacLeod, P. (1986) Intracellular recordings from salamander olfactory supporting cells.Brain Research 374, 205–11.
Wang, R. T. &Halpern, M. (1980) Scanning electron microscopic studies of the surface morphology of the vomeronasal epithelium and olfactory epithelium of garter snakes.American Journal of Anatomy 157, 399–128.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Morrison, E.E., Costanzo, R.M. Scanning electron microscopic study of degeneration and regeneration in the olfactory epithelium after axotomy. J Neurocytol 18, 393–405 (1989). https://doi.org/10.1007/BF01190842
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01190842