Summary
Axotomy at the level of thelamina cribrosa in rat induces rapid degeneration of the olfactory sensory axons in the bulb. The phenomenon, which is limited to the layer of olfactory fibres and to the glomeruli of the bulb, can be observed as early as 15–24 h after surgery, and peaks at 3–4 days. The glomeruli located in the rostro-ventral portion of the bulb are affected first, and the process extends to the dorso-caudal portion with a delay of 12–24 h. Reactive hypertrophy of the glia coincides with removal of the degenerating terminals, and is maximal 48 h after axotomy.
Axotomy does not preclude reinnervation of the bulb by axons originating from new, reconstituted neurons in the olfactory neuroepithelium. These new axons begin to reach the periphery of the bulb approximately at the 20th day post-operative and then reinnervate the glomeruli. The rostro-ventral portion of the bulb is the first to be reinvaded by the new axons. The glomeruli reacquire a morphological pattern similar to controls between 20 and 30 days.
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References
Berger, B. (1971) Formes diverses de dégénérescence des boutons synaptiques dans la glomérule olfactif de lapin après lésion du nerf olfactif.Brain Research 33, 218–22.
Clark, W. E. LeGros (1951) The projection of the olfactory epithelium on the olfactory bulb in the rabbit.Journal of Neurology, Neurosurgery and Psychiatry 14, 1–10.
Costanzo, R. M. &Mozell, M. M. (1976) Electrophysiological evidence for a topographical projection of the nasal mucosa onto the olfactory bulb of the frog.Journal of General Physiology 68, 297–312.
Costanzo, R. M. &O'connell, R. J. (1978) Spatially organized projections of hamster olfactory nerves.Brain Research 139, 327–32.
Costanzo, R. M. &O'Connell, R. J. (1979) Receptive fields of second order neurones in the olfactory bulb of the hamster.Journal of Physiology (in press).
Estable-Puig, J. F. &DeEstable, R. F. (1969) Acute ultrastructural changes in the rat olfactory glomeruli after peripheral deafferentation.Experimental Neurology 24, 592–602.
Fifková, E. (1975) Two types of terminal degeneration in the molecular layer of the dentate fascia following lesion of the entorhinal cortex.Brain Research 96, 169–75.
Graziadei, P. P. C. (1973) Cell dynamics in the olfactory mucosa.Tissue and Cell 5, 113–31.
Graziadei, P. P. C. (1975) Neuronal plasticity in the vertebrate olfactory receptor organ.Tenth International Congress of Antomy, Tokyo, p. 45.
Graziadei, P. P. C. &DeHan, R. S. (1973) Neuronal regeneration in frog olfactory epithelium.Journal of Cell Biology 59, 525–30.
Graziadei, P. P. C., Levine, R. R. &Monti graziadei, G. A. (1978) Regeneration of olfactory axons and synapse formation in the forebrain after bulbectomy in neonatal mice.Proceedings of the National Academy of Sciences (U.S.A.) 75, 5230–4.
Graziadei, P. P. C., Levine, R. R. &Monti Graziadei, G. A. (1979) Plasticity of connections of the olfactory sensory neuron: Regeneration into the forebrain following bulbectomy in neonatal mouse.Neuroscience 4, 713–27.
Graziadei, P. P. C. &Monti Graziadei, G. A. (1978a) The olfactory system: A model for the study of neurogenesis and axon regeneration in mammals. InNeuronal Plasticity (edited byCotman, C. W.), pp. 131–153. New York: Raven Press.
Graziadei, P. P. C. &Monti Graziadei, G. A. (1978b) Continuous nerve cell renewal in the olfactory system. InHandbook of Sensory Physiology (edited byJacobson, M.), Vol. IX, pp. 55–83. Berlin, Heidelberg, New York: Springer-Verlag.
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.
Graziadei, P. P. C. &Okano, M. (1979) Neuronal degeneration and regeneration in the olfactory epithelium of pigeon following transection of the first cranial nerve.Acta anatomica 104, 220–36.
Harding, J., Graziadei, P. P. C., Monti Graziadei, G. A. &Margolis, F. L. (1977a) Denervation in the primary olfactory pathway of mice. IV. Biochemical and morphological evidence for neuronal replacement following nerve section.Brain Research 132, 11–28.
Harding, J. W., Donlan, K., Chen, H. &Wright, J. (1977b) Behavioral and biochemical support of olfactory neuron replacement.Proceedings of the Society for Neuroscience, Seventh Annual Meeting Anheim, California. No. 230, Vol. 3 (abstract).
Hinds, J. W. &Hinds, P. L. (1972) Reconstruction of dendritic growth cones in neonatal mouse olfactory bulb.Journal of Neurocytology 1, 169–87.
Hornung, D. E. &Mozell, M. M. (1977) Factors influencing the differential absorption of odorant molecules across the olfactory mucosa.Journal of General Physiology 69, 343–61.
Land, L. J. (1973) Localized projection of olfactory nerves to rabbit olfactory bulb.Brain Research 63, 153–66.
Land, L. J., Eager, R. P. &Shepherd, G. M. (1970) Olfactory nerve projections to the olfactory bulb in rabbit: Demonstration by means of a simplified ammoniacal silver degenration method.Brain Research 23, 250–4.
Land, L. J. &Shepherd, G. M. (1974) Autoradiographic analysis of olfactory receptor projections in the rabbit.Brain Research 70, 506–10.
Matthews, D. A., Cotman, C. W. &Lynch, G. (1976) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration.Brain Research 115, 1–21.
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.
Monti Graziadei, G. A., Margolis, F. L., Harding, J. W. &Graziadei, P. P. C. (1977) Immunocytochemistry of the olfactory marker protein.Journal of Histochemistry and Cytochemistry 25, 1311–6.
Moulton, G. G. (1976) Spatial patterning of response to odors in the peripheral olfactory system.Physiological Reviews 56, 578–93.
Oley, N., DeHan, R. S., Tucker, D., Smith, J. C. &Graziadei, P. P. C. (1975) Recovery of function and structure following transection of the primary olfactory nerves in pigeon.Journal of Comparative Physiology and Psychology 88, 477–95.
Pinching, A. J. &Powell, T. P. S. (1972) A study of terminal degeneration in the olfactory bulb of the rat.Journal of Cell Science 10, 585–619.
Samanen, D. W. &Graziadei, P. P. C. (1979) Maintenance and plasticity of the mouse olfactory glomerulus after partial bulbectomy.Anatomical Record 193, 673 (abstract).
Sternberger, L. A., Hardy, P. H., Jr., Cuculis, J. J. &Meyer, H. G. (1970) The unlabeled antibody enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes.Journal of Histochemistry and Cytochemistry 18, 315–33.
Westrum, L. E. (1973) Early signs of terminal degeneration in the spinal trigeminal nucleus following rhizotomy.Journal of Neurocytology 2, 189–215.
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Graziadei, P.P.C., Monti Graziadei, G.A. Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of thefila olfactoria in rat. J Neurocytol 9, 145–162 (1980). https://doi.org/10.1007/BF01205155
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DOI: https://doi.org/10.1007/BF01205155