The progression of deafferentation as a retrograde reaction to hypoglossal nerve injury

Springer Science and Business Media LLC - Tập 24 - Trang 763-774 - 1995
Rosemary C. Borke1, Robert S. Bridwell1, Martin E. Nau1
1Department of Anatomy and Cell Biology, Uniformed Services University of the Health Sciences, Bethesda, USA

Tóm tắt

This study examined the fate of axon terminals of one of the major sources of hypoglossal afferents, the spinal V nucleus, after XIIth nerve resection in adult Sprague-Dawley rats. In order to anterogradely label trigemino-hypoglossal projections, small quantities of horse radish peroxidase were pressure-injected into the ipsilateral dorsal (mandibular) portion of the spinal V nucleus two days before the animals were killed. Survival periods ranged from 5 to 33 days after nerve injury (dpo). Axonal injury produced relative changes in the association of labelled axon terminals to structures in the hypoglossal nucleus on the injured side. The proportion of horse radish peroxidase-labelled spinal V nucleus terminals with spherical vesicles (S-terminals) that were unapposed to hypoglossal somata or dendrites increased rapidly and reached maximal levels by 11 dpo. By contrast, the isolation of labelled terminals with pleomorphic/flattened vesicles (P/F-terminals) from postsynaptic structures began later, advanced at a slower rate and did not attain maximal levels until 20 dpo. S-terminals not apposed to neuronal cell parts increased at a rate of 2.2 times greater than unapposed P/F-terminals. In addition, at peak levels, the proportion of labelled S-terminals that were detached from somata and dendrites was significantly greater than unapposed, labelled P/F-terminals. Axotomy did not alter the caliber of the labelled axon terminals. However, by 29 days after axotomy, the average diameter of dendrites remaining in contact with SPVN terminals was 1/3 the diameter of dendrites of uninjured neurons apposed to labelled axon terminals. These findings provide the morphological correlate for physiological and pharmacological evidence that the effectiveness of excitatory and inhibitory synapses are down-regulated in a coordinated manner after hypoglossal nerve injury.

Tài liệu tham khảo

Blinzinger, K. &Kreutzberg, G. W. (1968) Displacement of synaptic terminals from regenerating motoneurons by microglial cells.Zeitschrift fur Zellforschung und mikroskopische Anatomie. 85, 145–57. Boone, T. B. &Aldes, L. D. (1984) Synaptology of the hypoglossal nucleus in the rat.Experimental Brain Research 57, 22–32. Borke, R. C. (1982) Perisomatic changes in the maturing hypoglossal nucleus after axon injury.Journal of Neurocytology 11, 463–85. Borke, R. C. &Nau, M. E. (1985) The ultrastructural identification of reticulo-hypoglossal axon terminals anterogradely labeled with horseradish peroxidase.Brain Research 337, 127–32. Borke, R. C. &Nau, M. E. (1986) Factors affecting the ultrastructural pattern of anterograde labeling in axon terminals with HRP.Brain Research Bulletin 16, 259–65. Borke, R. C. &Nau, M. E. (1987) The ultrastructural morphology and distribution of trigemino-hypoglossal axon terminals anterogradely labeled with horseradish peroxidase.Brain Research 422, 235–41. Borke, R. C., Nau, M. E. &Ringler, R. L., JR. (1983) Brain stem afferents of the hypoglossal nucleus.Brain Research 269, 47–55. Borke, R. C., Nau, M. E. &Newman, D. B. (1988) Reticulo- and trigemino-hypoglossal connections: a quantitative comparison of ultrastructural substrates.Brain Research Bulletin 21, 795–803. Chen, D. H. (1978) Qualitative and quantitative study of synaptic displacement in chromatolyzed spinal motoneurons of the cat.Journal of Comparative Neurology 177, 635–64. Connaughton, M., Priestly, J. V., Sofroniew, M. V., Eckstein, F. &Cuello, A. C. (1986) Inputs to motoneurones in the hypoglossal nucleus of the rat: light and electron microscopic immunocytochemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies.Neuroscience 17, 205–22. Delgado-Garcia, J. M., Del Pozo, F., Spencer, R. F. &Baker, R. (1988) Behavior of neurons in the abducens nucleus of the alert cat-Ill. Axotomized motoneurons.Neuroscience 24, 143–60. Eugene, D. &Taxi, J. R. (1991) Effects of axotomy on synaptic transmission and structure in frog sympathetic ganglia,Journal of Neurocytology 20, 404–19. Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study.Journal of Anatomy 93, 420–33. Hamberger, A., Hansson, H. A. &Sjöstrand, J. (1970) Surface structure of isolated neurons: detachment of nerve terminals during axon regeneration.Journal of Cell Biology 47, 319–31. Itoh, K., Konishi, A., Nomura, S., Mizuno, N., Nakamura, Y. &Sugimoto, T. (1979) Application of coupled oxidation reaction to electron microscopic demonstration of horseradish peroxidase: cobalt-glucose oxidase method.Brain Research 175, 341–6. Johnson, I. P. &Sears, T. A. (1989) Ultrastructure of axotomized alpha and gamma motoneurons in the cat thoracic spinal cord.Neuropathology and Applied Neurobiology 15, 149–63. Kreutzberg, G. W., Graeber, M. B. &Streit, W. J. (1989) Neuron-glial relationship during regeneration of motorneurons.Metabolic Brain Disease 4, 81–5. Kuno, M. &Llinas, R. (1970a) Enhancement of synaptic transmission by dendritic potentials in chromatolysed motoneurones of the cat.Journal of Physiology 210, 807–21. Kuno, M. &Llinas, R. (1970b) Alterations in synaptic action in chromatolysed motoneurones of the cat.Journal of Physiology 210, 823–38. Lieberman, A. R. (1971) The axon reaction: a review of the principal features of perikaryal responses to axon injury.International Review of Neurobiology 14, 49–124. Lieberman, A. R. (1974) Some factors affecting retrograde neuronal responses to axonal lesions. InEssays on the Nervous System (edited byBellairs, R. &Gray, E. G.) pp. 71–105. Oxford: Clarendon Press. Lowe, A. A. (1981) The neural regulation of tongue movements.Progress in Neurobiology 15, 295–344. Matthews, M. R. &Nelson, V. H. (1975) Detachment of structurally intact nerve endings from chromatolytic neurons of the superior cervical ganglion during the depression of synaptic transmission induced by postganglionic axotomy.Journal of Physiology 245, 91–135. Neiss, W. F., Lichius, O. G., Angelov, D. N., Gunkel, A. &Stennert, E. (1992) The hypoglossal-facial anastomosis as model of neuronal plasticity in the rat.Annals of Anatomy 174, 419–33. Porter, R. (1967) The synaptic basis of a bilateral lingualhypoglossal reflex in cats.Journal of Physiology 190, 611–27. Purves, D. (1975) Functional and structural changes in mammalian sympathetic neurones following interruption of their axons.Journal of Physiology 252, 429–63. Purves, D. &Lichtman, J. W. (1978) Formation and maintenance of synaptic connections in autonomic ganglia.Physiological Review 58, 821–62. Rotter, A., Birdsall, N. J. M., Burgen, A. S. V., Field, P. M. &Raisman, G. (1977) Axotomy causes loss of muscarinic receptors and loss of synaptic contacts in the hypoglossal nucleus.Nature 266, 734–5. Rotter, A., Birdsall, N. J. M., Burgen, A. S. V., Field, P. M., Smolen, A. &Raisman, G. (1979) Muscarinic receptors in the central nervous system of the rat. IV. A comparison of the effects of axotomy and deafferentation on the binding of [3H] propylbenzilylcholine mustard and associated synaptic changes in the hypoglossal and pontine nuclei.Brain Research Review 1, 207–24. Rotter, A., Schultz, C. M. &Frostholm, A. (1984) Regulation of glycine receptors binding in the mouse hypoglossal nucleus in response to axotomy.Brain Research Bulletin 13, 487–92. Snedecor, G. W. &Cochran, W. G. (1980)Statistical Methods. Seventh Edition. Ames, IA: Iowa State University Press. Sumner, B. E. H. (1975a) A quantitative analysis of the response of presynaptic boutons to postsynaptic motor neuron axotomy.Experimental Neurology 46, 605–15. Sumner, B. E. H. (1975b) A quantitative analysis of boutons with different types of synapse in normal and injured hypoglossal nuclei.Experimental Neurology 49, 406–17. Sumner, B. E. H. (1975c) A quantitative study of subsurface cisterns and their relationships in normal and axotomized hypoglossal motoneurons.Experimental Brain Research 22, 175–83. Sumner, B. E. H. &Sutherland, F. I. (1973) Quantitative electron microscopy on the injured hypoglossal nucleus in the rat.Journal of Neurocytology 2, 315–28. Svensson, M. &Aldskogius, H. (1993) Synaptic density of axotomized hypoglossal motorneurons following pharmacological blockade of the microglial cell proliferation.Experimental Neurology 120, 123–31. Svensson, M., Tornqvist, E., Aldskogius, H. &Cova, J. (1991) Synaptic detachment from hypoglossal neurons after different types of nerve injury in the cat.Journal fuer Hirnforschung 32, 547–52. Takasu, N. &Hashimoto, P. H. (1988) Morphological identification of an interneuron in the hypoglossal nucleus of the rat: a combined Golgi-electron microscopic study.Journal of Comparative Neurology 271, 461–71. Takasu, N., Nakatani, T., Arikuni, T. &Kimura, H. (1987) Immunocytochemical localization of γ-aminobutyric acid in the hypoglossal nucleus of the macaque monkey, Macaca fuscata: a light and electron microscopic study.Journal of Comparative Neurology 263, 42–53. Takata, M. (1981) Lingually induced inhibitory postsynaptic potentials in hypoglossal motoneurons after axotomy.Brain Research 224, 165–9. Takata, M. (1982) Inhibitory postsynaptic potentials evoked in hypoglossal motoneurons by lingual nerve stimulation.Experimental Neurology 75, 103–11. Takata, M. &Nagahama, T. (1983) Synaptic efficacy of inhibitory synapses in hypoglossal motoneurons after transection of the hypoglossal nerves.Neuroscience 10, 23–9. Takata, M., Shohara, E. &Fujita, S. (1984) The excitability of hypoglossal motoneurons undergoing chromatolysis.Neuroscience 5, 413–19. Takata, M., Tomomune, N., Nagahama, T., Tomioka, S. &Nakajo, N. (1990) Synaptic efficacy of inhibitory synapses and repetitive firing in the reinnervating trigeminal and hypoglossal motoneurons.Neuroscience 36, 785–92. Titmus, M. J. &Faber, D. S. (1990) Axotomy-induced alterations in the electrophysiological characteristics of neurons.Progress in Neurobiology 35, 1–51. Travers, J. B. &Norgren, R. (1983) Afferent projections to the oral motor nuclei in the rat.Journal of Comparative Neurology 220, 280–93. Vaughan, D. W. (1994) Effects of peripheral axotomy on presynaptic axon terminals with GABA-like immunoreactivity.Anatomical Record 238, 248–62. Watson, W. E. (1974) Cellular responses to axotomy and to related procedures.British Medical Bulletin 30, 112–15. Winer, B. J. (1971)Statistical Principles in Experimental Design.Second Edition. New York: McGraw-Hill.