Nimodipine-accelerated hypoglossal sprouting prevents the postoperative hyperinnervation of target muscles after hypoglossal-facial anastomosis in the rat

Restorative Neurology and Neuroscience

Volumn 11, Issue 1-2, 1997, Pages 109-121

  Angelova, Doychin N ^a   Neiss, Wolfram F ^a   Gunkel, Andreas ^b   Streppel, Michael ^a   Guntinas Lichius, Orlando ^a   Stennert, Eberhard ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Facial nerve; Hypoglossal nerve; Nerve suture; Neuron number; Nimodipine; Rat; Retrograde tracing

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; NIMODIPINE; PLACEBO;

ANASTOMOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FACIAL NERVE; FEMALE; HISTOCHEMISTRY; HYPOGLOSSAL NERVE; MUSCLE INNERVATION; NERVE SPROUTING; NONHUMAN; ORAL DRUG ADMINISTRATION; PRIORITY JOURNAL; RAT;

EID: 0030944627     PISSN: 09226028     EISSN: None     Source Type: Journal    
DOI: 10.3233/rnn-1997-111212     Document Type: Article

References (80)

1. Ahlijanian, M.K., Westenbroek, R.E. and Catterall, W.A., Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord, and retina, Neuron, 4 (1990) 819-832.
2. Angelov, D.N., Gunkel, A., Stennert, E. and Neiss, W.F., Recovery of original nerve supply after hypoglossal-facial anastomosis causes permanent motoric hyperinnervation of the whiskerpad muscles in the rat, J. Comp. Neurol., 338 (1993) 214-224.
3. Angelov, D.N., Gunkel, A., Stennert, E. and Neiss, W.F., Immunocytochemical evidence for accelerated neuronal recovery after peripheral nerve axotomy and nimodipine treatment in rats. 5th Int. Symp. Neural Regeneration, (Abstr.) Asilomar, California (1993) P26.
4. Angelov, D.N., Neiss, W.F., Gunkel, A., Guntinas-Lichius, O. and Stennert, E., Axotomy induces intranuclear immunolocalization of neuron-specific enolase (NSE) in facial and hypoglossal neurons of the rat, J. Neurocytol., 23 (1994) 218-233.
5. Angelov, D.N., Neiss, W.F., Streppel, M., Andermahr, J., Mader, K. and Stennert, E., Nimodipine accelerates axonal resprouting after facial nerve suture. J. Neurosci., 16 (1996) 1041-1048.
6. Anglister, L., Farber, J.C., Shahar, A. and Grinvald, A., Localization of calcium sensitive calcium channels along developing neurites: Their possible role in regulating neurite elongation, Dev. Biol., 94 (1982) 351-365.
7. Anonsen, C.K., Trachy, R.E., Hibbert, J. and Cummings, C.W., Assessment of facial reinnervation by use of chronic electromyographic monitoring, Otolaryngol. Head. Neck. Surg., 94 (1986) 32-36.
8. Bär, P.R., Traber, J., Schuurman, T. and Gispen, W.H., CNS and PNS effects of nimodipine. J. Neural. Transm. Suppl., 31., (1990) 55-71.
9. 3H]nimodipine, Proc. Natl. Acad. Sci. USA, 80 (1983) 2356-2360.
10. Blinzinger, K. and Kreutzberg, G.W., Displacement of synaptic terminals from regenerating motoneurons by microglial cells, Z. Zellforsch. Mikrosk. Anal., 85 (1968) 145-157.
11. Brushart, T.M.E., Stimulation of regenerative sprouting enhances preferential motor reinnervation (PMR), Soc. Neurosci. Abstr., 20 (1994) 1268.
12. Buller, A.J., Eccles, J.C. and Eccles, R.M., Inteactions between motoneurons and muscles in respect of their characteristic speeds of their responses, J. Physiol., 150 (1960) 417-439.
13. Carmignoto, G., Finesso, M., Siliprandi, R. and Gorio, A., Muscle reinnervation - I. Restoration of transmitter release mechanisms, Neuroscience, 8 (1983) 393-401.
14. Chen, Y.S., Yanagihara, N. and Murakami, S., Change in the facial nerve innervation following hypoglossal-facial anastomosis. An animal study, Acta Otolaryngol., 114 (1994) 637-642.
15. Choi, D.W., Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage, Trends Neurosci., 11 (1988) 465-469.
16. Coggeshall, R.E. and Lekan, H.A., Methods for determining numbers of cells and synapses: A case for more uniform standards of review, J. Comp. Neurol., 364 (1996) 6-15.
17. Covault, J. and Sanes, J.R., Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles, Proc. Natl. Acad. Sci. USA, 82 (1985) 4544-4548.
18. Dennis, M.J. and Miledi, R., Characteristics of transmitter release at regenerating frog neuromuscular junctions, J. Physiol., 239 (1974) 571-594.
19. Fields, D.R., Guthrie, P.B., Russel, J.T., Kater, S.B., Malhotra, B.S. and Nelson, P.G., Accomodation of mouse DRG growth cones to electrically induced collapse: kinetic analysis of calcium transients and set-point theory, J. Neurobiol., 24 (1993) 1080-1098.
20. Flumerfelt, B.A., Kiernan, J.A., Krcek, J.P. and Sholdice, J., Reinnervation of skeletal muscle in the tongue by preganglionic parasympathetic vagal neurons, J. Anat., 146 (1986) 117-130.
21. Gispen, W.H., Schuurman, T. and Traber, J., Nimodipine and neural plasticity in the peripheral nervous system of adult and aged rats. In: M. Morad, W. Nayler, S. Kazda and M. Schramm (Eds.), The Ca 2 + channel: Structure, Function and Implications. Springer, Berlin, 1988, pp. 491-502.
22. Gordon, T., Mechanisms for functional recovery of the larynx after surgical repair of injured nerves, J. Voice, 8 (1994a) 70-78.
23. Gordon, T., To what extent can poor functional recovery of denervated muscles be attributed to incomplete as opposed to inappropriate reinnervation after surgical repair of severed nerves, Eur. Arch. Otorhinolaryngol., Suppl., (1994b) S21-S23.
24. Gordon, T., Stein, R.B. and Thomas, C.K., Innervation and function of hind-limb muscles in the cat after cross-union of the libial and peroneal nerves, J. Physiol., 374 (1986) 429-441.
25. Graeber, M.B. and Kreutzberg, G.W., Delayed astrocyte reaction following facial nerve axotomy, J. Neurocytol., 17 (1988) 209-220.
26. Grothe, C. and Unsicker, K., Basic fibroblast gowth factor in the hypoglossal system: specific retrograde transport, trophic, and lesion-related responses, J. Neurosci. Res., 32 (1992) 317-328.
27. Gruart, A., Gunkel, A., Neiss, W.F., Stennert, E. and Delgado-Garcia, J.M., Adaptability of adult mammalian motoneurons to new motor tasks. In: T. Mergner and F. Hlavacka (Eds.), Multisensory Control of Posture, Plenum, New York, 1995, pp. 15-20.
28. Gruart, A., Gunkel, A., Neiss, W.F., Angelov, D.N., Stennert, E. and Delgado-Garcia, J.M., Eye blink responses following hypoglossal-facial anastomosis in the cat, Neuroscience, 73 (1996) 233-247.
29. Gundersen, H.J.G., Stereology of arbitrary particles. J. Microsc., 143 (1986) 3-45.
30. Guntinas-Lichius, O., Mockenhaupt, J., Stennert, E. and Neiss, W.F., Simplified nerve cell counting in the rat brainstem with the physical disector using a drawing microscope, J. Microsc., 172 (1993) 177-180.
31. Guntinas-Lichius, O., Neiss, W.F., Gunkel, A. and Stennert, E., Differences in glial, synaptic and motoneuron responses in the facial nucleus of the rat brainstem following facial nerve resection and nerve suture reanastomosis, Eur. Arch. Otorhinolaryngol., 251 (1994) 410-417.
32. Guntinas-Lichius, O. and Neiss, W.F., Comparison of empirical and estimated efficiency in neuron counting by the physical disector and in volume measurement by Cavalieri's method, Acta Stereol., 15 (1996) 131-139.
33. Guntinas-Lichius, O., Martinez-Portillo, F.J., Schulte, E., Stennert, E. and Neiss, W.F., The influence of nimodipine on chromatolysis of motoneurons following axotomy with and without reinnervation: a quantitative image analysis, Neurosci. Res. Commun., 19 (1996) 101-107.
34. Guntinas-Lichius, O., Martinez-Portillo, F.J., Lebek, J., Angelov, D.N., E., Stennert, E. and Neiss, W.F., Nimodipine maintains in vivo the increase in GFAP and enhances the astroglial ensheathment of surviving motoneurons in the rat following permanent target deprivation. (submitted).
35. Hammerschlag, P.E., Hypoglossal facial nerve anastomosis for correction of facial nerve paralysis following cerebello-pontine angle surgery. In: J. Ransohoff (Ed.), Modern Techniques in Surgery, Vol. 37, Mount Kisco, New York 1987, pp. 2-12.
36. Hell, J.W., Westenbroek, R.E., Warner, C., Ahlijanian, M.K., Prystay, W., Gilbert, M.M., Snutch, T.P. and Cattereall, W.A., Identification and differentiial subcellular localization of the neuronal class C and class D L-type calcium channel α - subunits. J. Cell Biol., 123 (1993) 949-962.
37. Hofer, M.M. and Barde, Y-A., Brain derived neurotrophic factor prevents neuronal death in vivo, Nature, 331(1988) 261-262.
38. Ingram, D.K., Joseph, J.A., Spangler, E.L., Roberts, D., Hengemihle, J. and Fanelli, R., Chronic nimodipine treatment in aged rats: analysis of motor and cognitive effects and muscarinic-induced striatal dopamine release, Neurobiol. Aging, 15 (1994) 55-61.
39. Kater, S.B. and Mills, L.R., Regulation of growth cone behaviour by calcium, J. Neurosci., 11 (1991) 891-899.
40. 2+ regulation of the neural growth cone. Trends Neurosci., 11 (1988) 315-320.
41. Kazda, S., Garthoff, B. and Luckhaus, G., Prevention of acute and chronic cerebrovascular damage with nimodipine in animal experiments. In: E. Betz, K. Deck and F. Hoffmeister (Eds.), Nimodipine: Pharmacological and Clinical Properties, Schattauer, Stuttgart, 1985, pp. 31-43.
42. Krebs, C., Angelov, D.N., Guntinas-Lichius, O., Stennert, E. and Neiss, W.F., Nimodipine reduces the CNS macrophage antigen expression after axotomy, Ann. Anal. Suppl. (Abstr.) 178 (1996) 303-304.
43. Lebek, J., Fackeldey, V., Veh, R.W., Stennert, E. and Neiss, W.F., Inhibitory innervation of hypoglossal and facial nucleus by GABAergic and glycinergic axosomatic synapses, Eur. J. Neurosci. Suppl. (Abstr.), 6 (1993) 1075.
44. Lewis, M.E., Neff, N.T., Contreras, P.C., Stong, D.B., Oppenheim, R.W., Grebow, P.E. and Vaught, J.L., Insulin-like growth factor I: potential for treatment of motor neuronal disorders, Exp. Neurol., 124 (1993) 73-88.
45. Mabe, H., Nagai, H., Takagi, T., Umemura, S. and Ohno, M., Effect of nimodipine on cerebral functional and metabolic recovery following ischemia in the rat brain, Stroke, 17 (1986) 501-505.
46. Martinez-Portillo, F.J., Guntinas-Lichius, O., Gunkel, A., Stennert, E. and Neiss, W.F., Influence of nimodipine on astroglial response following axotomy of the facial or hypoglossal nerve in the rat. Ann. Anat. Suppl. (Abstr.), 175 (1993) 200-201.
47. Martinez-Portillo, F.J., Guntinas-Lichius, O., Gunkel, A., Stennert, E. and Neiss, W.F., The effect of nimodipine on microglial response after hypoglossal-facial anastomosis in the rat, Proc. 21st Göttingen Neurobiology Conference, (Abstr.), Georg Thieme, New York, 1993, pp. 686.
48. Mattson, M.P. and Kater, S.B., Calcium regulation of neurite elongation and growth cone motility, J. Neurosci., 7 (1987) 4034-4043.
49. May, M., Sorol, S.M. and Mester, S.J., Hypoglossal-facial nerve interpositional-jump graft for facial reanimation without tongue atrophy, Otolaryngol. Head Neck Surg., 104 (1991) 818-825.
50. McArdle, J.J. and Albuquerque, X.E., A study of the reinnervation of fast and slow mammalian muscles, J. Gen. Physiol., 61 (1973) 1-23.
51. McQuarrie, I.G. and Jacob, J.M., Conditioning nerve crush accelerates cytoskeletal protein transports in sprouts that form after a subsequent crush, J. Comp. Neurol., 305 (1991) 139-147.
52. Mesulam, M.-M., Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents, J. Histochem. Cytochem., 26 (1978) 106-117.
53. Meyer, F.B., Calcium, neuronal hyperexcitability and ischemic injury. Brain Res. Rev., 14 (1989) 227-243.
54. Neiss, W.F., Guntinas-Lichius, O., Angelov, D.N., Gunkel, A. and Stennert, E., The hypoglossal-facial anastomosis as model of neuronal plasticity in the rat, Ann. Anat., 174 (1992) 419-433.
55. Neiss, W.F., Angelov, D.N., Gunkel, A. and Stennert, E., Nimodipine accelerates the sprouting of axotomized motoneurons following hypoglossal-facial anastomosis in the rat, 2nd Int. Neurotrauma Symp., 4-9 July 1993, Glasgow, Scotland, J. Neurotrauma, (Abstr.), 10 (1993) 55.
56. Nyakas, C., Buwalda, B., Kramers, R.J.K., Traber, J. and Luiten, P.G.M., Postnatal development of hippocampal and neocortical cholinergic and serotonergic innervation in rat: effects of nitrite-induced prenatal hypoxia and nimodipine treatment, Neuroscience, 59 (1994) 541-559.
57. Regan, R.F. and Choi, D.W., The effect of NMDA, AMPA/ kainate, and calcium channel anatagonists on traumatic cortical neuronal injury in culture, Brain Res., 633 (1994) 236-242.
58. Saper, C.B., Any way you cut it: A new journal policy for the use of unbiased counting methods, J. Comp. Neurol., 364 (1996) 5.
59. Schanne, F.A.X., Kane, A.B., Young, E.E. and Farber, J.L., Calcium dependence of toxic cell death: a final common pathway. Science, 206 (1979) 700-702.
60. Schneider, I., Gunkel, A., Stennert, E. and Neiss, W.F., Development of the nerve conduction velocity after hypoglossal-facial anastomosis: an electromyographic study. Eur. Arch. Otorhinolaryngol. Suppl. (Abstr.), (1994) S392.
61. Schuurman, T., Klein, H., Beneke, M. and Traber, J., Nimodipine and motor deficits in the aged rat, Neurosci. Res. Commun., 1 (1987) 9-15.
62. Seeburger, J.L. and Springer, J.E., Experimental rationale for the therapeutic use of neurotrophins in amyotrophic lateral sclerosis, Exp. Neurol., 124 (1993) 64-72.
63. Sendtner, M., Kreutzberg, G.W. and Thoenen, H., Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy, Nature, 345 (1990) 440-441.
64. Sendtner, M., Stöckli, K.A. and Thoenen, H., Synthesis and localization of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration, J. Cell Biol., 118 (1992) 139-148.
65. Sher, E., Biancardi, E., Passafaro, M. and Clementi, F., Physiopathology of neuronal voltage-operated calcium channels, FASEB J., 5 (1991) 2677-2683.
66. Siesjo, B., Cell damage in the brain: a speculative synthesis, J. Cerebr. Blood Flow Metab., 1 (1981) 155-185.
67. Simon, R.P., Griffiths, T., Evans, M.C., Swane, J.H. and Meldrum, B.S., Calcium overload in selectively vulnerable neurons of the hippocampus during and after ischemia: an electron microscopic study in the rat, J. Cerebr. Blood Flow Metab., 4 (1984) 350-361.
68. Stennert, E., Hypoglossal facial anastomosis: Its significance for modern facial surgery. II. Combined approach in extratemporal facial nerve reconstruction, Clin. Plast. Surg., 6 (1979) 471-486.
69. Sumner, A.J., Aberrant reinnervation, Muscle and Nerve, 13 (1990) 801-803.
70. Sumner, B.E.H. and Sutherland, F.I., Quantitative electron microscopy on the injured hypoglossal nucleus in the rat, J. Neurocytol., 2 (1983) 315-328.
71. Takata, M., Shohara, E. and Fujita, S., The excitability of hypoglossal motoneurons undergoing chromatolysis, Neuroscience, 5 (1980) 413-419.
72. Titmus, M.J. and Faber, D.S., Axotomy-induced alterations in the electrophysiological characteristics of neurons, Progr. Neurobiol., 35 (1990) 1-51.
73. Uematsu, D., Greenberg, J.H., Hickey, W.F. and Reivich, M., Nimodipine attenuates both increase in cytosolic free calcium and histologie damage following focal cerebral ischemia and reperfusion in cats, Stroke, 20 (1989) 1531-1537.
74. Van den Kerckhoff, W. and Drewes, L.R., Transfer of the Ca-antagonists nifedipine and nimodipine across the blood-brain barrier and their regional distribution in vivo. J. Cerebr. Blood Flow Metab. (Suppl I), 5 (1985) 459-460.
75. Van der Zee, C.E.E.M., Schuurman, T., Traber, J. and Gispen, W.H., Oral administration of nimodipine accelerates functional recovery following peripheral nerve damage in the rat, Neurosci. Lett., 83 (1987) 143-148.
76. Van der Zee, C.E.E.M., Schuurman, T., Gerritsen van der Hoop, R., Traber, J. and Gispen, W.H., Beneficial effect of nimodipine on peripheral nerve function in aged rats, Neurobiol. Aging, 11 (1990) 451-456.
77. Van der Zee, C.E.E.M., Brakkee, J.H. and Gispen, W.H., Putative neurotrophic factors and functional recovery from peripheral nerve damage in the rat, Br. J. Pharmacol., 103 (1991) 1041-1046.
78. Varon, S., Factors promoting the growth of the nervous system, Neuroscience, 3 (1985) 62.
79. Wadworth, A.N. and McTavish, D., Nimodipine. A review of its pharmacological properties and therapeutic efficacy in cerebral disorders, Drugs Aging, 2 (1992) 262-286.
80. Yellin, H., Neural regulation of enzymes in muscle fibers of red and white muscle, Exp. Neurol., 19 (1967) 92-103.