Summary
Sensory neurons were examined in spinal ganglia of the rat 1 to 55 days after section of the plexus brachialis nerves. Only “light” neurons of the type A were investigated. Maximal reaction to axotomy was found 7 to 14 days after the operation. The majority of the axotomized perikarya developed central chromatolysis. In such neurons, Nissl bodies virtually disappeared from the central area of the neuron and formed a more or less continuous zone at the cell circumference. The cytocentrum became filled with large numbers of mitochondria, dense bodies and other organelles. Neurofilaments and microtubules were disarranged and ran at random among the accumulated particles. Microtubules were often more prominent in chromatolytic areas than neurofilaments. Both these organelles were rare in the peripheral areas filled with massed Nissl substance.
Part of the neurons that did not show typical chromatolysis contained increased numbers of neurofilaments among Nissl bodies dispersed throughout the cytoplasm. Neurofilaments were roughly arrayed in bundles up to several microns wide; they were linked by cross-bridges and separated by distances of about 500 Å. Microtubules were rarely found in the filamentous areas. However, they were numerous in the axon hillock and in the initial segment where they formed fascicles similar to those described in normal neurons of other types.
During the period from 14 to 55 days after axotomy, many perikarya recovering from chromatolysis contained enlarged bundles of neurofilaments with occasional microtubules among the restored Nissl bodies.
Mean diameters of sensory neurons, measured 7 to 55 days after axotomy, in no instance exceeded those of contralateral control neurons. It thus appears that sensory perikarya do not increase in size either during the chromatolytic process or during the period of recovery.
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References
Andres, K. H.: Untersuchungen über den Feinbau von Spinalganglien. Z. Zellforsch. 55, 1–48 (1961 a).
—: Untersuchungen über morphologische Veränderungen in Spinalganglien während der retrograden Degeneration. Z. Zellforsch. 55, 49–79 (1961 b).
Barondes, S. H., Samson, F. E., Jr., eds.: Axoplasmic transport. Neurosciences Res. Prog. Bull. 5, 307–419 (1967).
Barr, M. L., Hamilton, J. D.: A quantitative study of certain morphological changes in spinal neurons during axon reaction. J. comp. Neurol. 89, 93–121 (1948).
Barron, K. D., Oldershaw, J. B., Bernsohn, J.: Hydrolase cytochemistry of retrograde neuronal degeneration in feline lateral geniculate body. J. Neuropath. exp. Neurol. 25, 443–478 (1966).
Bodian, D.: An electron microscopic study of the monkey spinal cord. Bull. Johns Hopk. Hosp. 114, 13–119 (1964).
—, Mellors, R. C.: The regenerative cycle of motoneurons, with special reference to phosphatase activity. J. exp. Med. 81, 469–488 (1945).
Brattgard, S. O., Edström, J. E., Hydén, H.: The chemical changes in regenerating neurons. J. Neurochem. 1, 316–325 (1957).
Cammermeyer, J.: Differential response of two neuron types to facial nerve transection in young and old rabbits. J. Neuropath. exp. Neurol. 22, 594–616 (1963).
—: Species difference in acute retrograde neuronal reaction of the facial and hypoglossal nuclei. J. Hirnforsch. 11, 13–29 (1929).
Cole, M.: Retrograde degeneration of axon and soma in the nervous system. In: The structure and function of nervous tissue, G. H. Bourne, ed., 269–300. New York and London: Academic Press 1968.
Cragg, B. G.: What is the signal for chromatolysis? Brain Res. 23, 1–21 (1970).
Evans, D. H. L., Gray, E. G.: Changes in the fine structure of ganglia cells during chromatolysis. In: Cytology of nervous tissue. Proc. of the Anat. Society of Great Britain and Ireland, p. 71–74 (1961).
Geist, F. D.: Chromatolysis of efferent neurons. Arch. Neurol. Psychiat. (Chic.) 29, 88–103 (1933).
Hartmann, J. F.: Electronmicroscopy of motor nerve cells following section of axons. Anat. Rec. 118, 19–34 (1954).
Hirano, A., Dembitzer, H. M., Kuland, L. T.: The fine structure of some intraganglionic alterations. J. Neuropath. exp. Neurol. 27, 167–182 (1968).
Holtzmann, E., Novikoff, A. B., Villaverde, H.: Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum. J. Cell Biol. 33, 419–435 (1967).
Hudson, G., Lazarov, A., Hartmann, J.: A quantitative electron microscopic study of mitochondria in motor neurons following axonal section. Exp. Cell Res. 24, 440–456 (1961).
Hydén, H.: The neuron. In: The cell, vol. 2, Brachet, J. and Mirsky, A. F., eds., p. 214–234. New York: Academic Press 1960.
Kidd, M.: Alzheimer's disease—an electron microscopical study. Brain 87, 307–320 (1964).
Kirkpatrick, J. B.: Chromatolysis in the hypoglossal nucleus of the rat: an electron microscopic analysis. J. comp. Neurol. 132, 189–212 (1968).
Klatzo, I., Wiśniewski, H., Streicher, E.: Experimental production of neurofibrillary degeneration. I. Light microscopic observations. J. Neuropath. exp. Neurol. 24, 178–199 (1965).
Kohno, K.: Neurotubules contained within the dendrite and axon of Purkinje cell of frog. Bull. Tokyo med. dent. Univ. 11, 411–442 (1964).
Lampert, P., Blumberg, J. N., Pentschew, A.: An electron microscopic study of dystrophic axons in the gracile and cuneate nuclei of vitamin E-deficient rats. J. Neuropath. exp. Neurol. 23, 60–77 (1964).
Lentz, T. L.: Fine structure of sensory ganglion cells during limb regeneration of the newt Triturus. J. comp. Neurol. 131, 301–322 (1967).
—: Vesicle and granular content of sympathetic ganglion cells during limb regeneration of the newt Triturus. Z. Zellforsch. 102, 447–458 (1969).
Lieberman, A. R.: Absence of ultrastructural changes in ganglionic neurons after supranodose vagotomy. J. Anat. (Lond.) 104, 49–54 (1969).
—: Light and electron-microscope observations on the Golgi apparatus of normal and axotomized neurons. J. Anat. (Lond.) 104, 309–325 (1969).
- Axon reaction in vertebrate neurons, a review of some perikaryal responses and associated glial reactions induced by axonal injuries. Int. Rev. Neurobiol., in press.
Lubińska, L.: Axoplasmic streaming in regenerating and in normal nerve fibres. In: Progress in brain research (M. Singer and J. P. Schadé, eds.), vol. 13, p. 1–71. Amsterdam: Elsevier 1964.
Mackey, E. A., Spiro, D., Wiener, J.: A study of chromatolysis in dorsal root ganglia at the cellular level. J. Neuropath. exp. Neurol. 23, 508–526 (1964).
Murray, M., Grafstein, B.: Changes in the morphology and amino acid incorporation of regenerating goldfish optic neurons. Exp. Neurol. 23, 544–560 (1969).
Nissl, F.: Über die Veränderungen der Ganglienzellen am Facialiskern des Kaninchens nach Ausreißung der Nerven. Allg. Z. Psychiat. 48, 197–198 (1892).
Palay, S. L.: The structural basis for neural action. In: RNA and brain function: Memory and learning. Brain function, vol. 2, Brazier, M. A. B., ed., p. 69–108. Los Angeles: University of California Press 1964.
—, Palade, G. E.: The fine structure of neurons. J. biophys. biochem. Cytol. 1, 69–88 (1955).
—, Sotelo, C., Peters, A., Orkand, P. M.: The axon hillock and the initial segment. J. Cell Biol. 38, 193–201 (1968).
Pannese, E.: Detection of neurofilaments in the perikaryon of hypertrophic nerve cells. J. Cell Biol. 13, 451–461 (1962).
—: Investigation on the ultrastructural changes of the spinal ganglion neurons in the course of axon regeneration and cell hypertrophy. I. Changes during axon regeneration. Z. Zellforsch. 60, 711–740 (1963a).
—: Investigation on the ultrastructural changes of the spinal ganglion neurons in the course of axon regeneration and cell hypertrophy. II. Changes during cell hypertrophy and comparison between the ultrastructure of nerve cells of the same type under different functional conditions. Z. Zellforsch. 61, 561–586 (1963b).
Peters, A., Proskauer, Ch. C., Kaiserman-Abramof, I. R.: The small pyramidal neuron of the rat cerebral cortex. The axon hillock and initial segment. J. Cell Biol. 39, 604–619 (1968).
—, Vaughn, J. E.: Microtubules and filaments in the axons and astrocytes of early postnatal rat optic nerves. J. Cell Biol. 32, 113–119 (1967).
Porter, K. R., Bowers, M. B. and students: A study of chromatolysis in motor neurons of the frog Rana pipiens. J. Cell Biol. 19, 56–57A (1963).
Robertson, J. D., Bodenheimer, T. S., Stage, D. E.: The ultrastructure of Mauthner cell synapses and nodes in goldfish brains. J. Cell Biol. 19, 159–199 (1963).
Rosenbluth, J., Palay, S. L.: Electron microscopic observations on the interface between neurons and capsular cells in dorsal root ganglia of the rat. Anat. Rec. 136, 268 (1960).
—, Wissig, S. L.: The distribution of exogenous ferritin in toad spinal ganglia and the mechanism of its uptake by neurons. J. Cell Biol. 23, 307–325 (1964).
Scharf, J. H.: Sensible Ganglien, 485 S. Handbuch der mikroskopischen Anatomie des Menschen, IV/3. W. Bargmann, ed. Berlin-Göttingen-Heidelberg: Springer 1958.
Schmitt, F. O.: The molecular biology of neuronal fibrous proteins Neurosciences Res. Prog. Bull. 6, 119–144 (1968).
—: Fibrous proteins and neuronal structure. In: Cellular dynamics of the neuron, ed. S. H. Barondes. Symp. of the International Society for Cell Biology, vol. 8, 95–111. New York: Academic Press 1969.
—, Samson, F. E., Jr.: Neuronal fibrous proteins. Neurosciences Res. Prog. Bull. 6, 113–219 (1968).
Smith, K. R.: The fine structure of neurons of dorsal root ganglia after stimulating or cutting the sciatic nerve. J. comp. Neurol. 116, 103–115 (1961).
Takano, I.: Electron microscopic studies on retrograde chromatolysis in the hypoglossal nucleus and changes in the hypoglossal nerve following its severance and ligation. Okajimas Folia anat. jap. 40, 1–69 (1964).
Terry, R. D.: The fine structure of neurofibrillary tangles in Alzheimer's disease. J. Neuropath. exp. Neurol. 22, 629–642 (1963).
—, Gonatas, N. K., Weiss, M.: Ultrastructural studies in Alzheimer's presenile dementia. Amer. J. Path. 44, 269–297 (1964).
—, Peña, C.: Experimental production of neurofibrillary degeneration. II. Electron microscopy, phosphatase histochemistry, and electron probe analysis. J. Neuropath. exp. Neurol. 24, 200–210 (1965).
Watson, W. E.: An autoradiographic study of the incorporation of nucleic-acid precursor by neurons and glia during nerve regeneration. J. Physiol. (Lond.) 180, 741–753 (1965).
—: Observations on the nucleolar and total cell body nucleic acid of injured nerve cells. J. Physiol. (Lond.) 196, 655–676 (1968).
Wiśniewski, H., Karczewski, W., Wiśniewska, K.: Neurofibrillary degeneration of nerve cells after intracerebral injection of aluminium cream. Acta neuropath. (Berl.) 6, 211–219 (1966).
—, Shelanski, M. L., Terry, R. D.: Effects of mitotic spindle inhibitors on neurotubules and neurofilaments in anterior horn cells. J. Cell Biol. 38, 224–230 (1968).
—, Terry, R. D.: Experimental colchicine encephalopathy. I. Induction of neurofibrillary degeneration. Lab. Invest. 17, 577–587 (1968).
Zelená, J.: Bidirectional movements of mitochondria along axons of an isolated nerve segment. Z. Zellforsch. 92, 186–196 (1968).
—, Lubińská, L.: Early changes of acetylcholinesterase activity near the lesion in crushed nerves. Physiol. bohemoslov. 11, 261–268 (1962).
—, Gutmann, E.: Accumulation of organelles at the ends of interrupted axons. Z. Zellforsch. 91, 200–219 (1968).
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This project was supported by a grant from the Muscular Dystrophy Association of America, Inc. The main part of this study was done while the author was a Research Fellow in Anatomy at the Harvard Medical School, Boston. The author wishes to thank prof. S. L. Palay for his valuable advice and help received during her stay at the Department of Anatomy at the Harvard Medical School, under NIH training grant NBO5591.
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Zelená, J. Neurofilaments and microtubules in sensory neurons after peripheral nerve section. Z. Zellforsch. 117, 191–211 (1971). https://doi.org/10.1007/BF00330737
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DOI: https://doi.org/10.1007/BF00330737