Altered sensory input improves the accuracy of muscle reinnervation

Restorative Neurology and Neuroscience

Volumn 20, Issue 1-2, 2002, Pages 1-14

  Skouras, Emmanouil ^a   Popratiloff, Anastas ^a   Guntinas Lichius, Orlando ^a   Streppel, Michael ^a   Rehm, Klaus E ^a   Neiss, Wolfram F ^a   Angelov, Doychin N ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FAST BLUE; FLUOROGOLD;

ACCURACY; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LABELING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FACIAL NERVE; FACIAL NERVE SURGERY; FEMALE; INFRAORBITAL NERVE; MOTONEURON; MUSCLE REINNERVATION; NERVE ANASTOMOSIS; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NERVE SUTURE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY STIMULATION; TRIGEMINAL NERVE; VIBRISSA;

ACTION POTENTIALS; ANASTOMOSIS, SURGICAL; ANIMALS; AXONS; BEHAVIOR, ANIMAL; ELECTROPHYSIOLOGY; FACIAL NERVE; FEMALE; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE REGENERATION; NEURONS, AFFERENT; RATS; RATS, WISTAR; VIBRISSAE;

EID: 0036032973     PISSN: 09226028     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (90)

1. H. Aldskogius and L. Thomander, Selective reinnervation of somatotopically appropriate muscles after facial nerve transection and regeneration in the neonatal rat, Brain. Res. 375 (1986), 126-134.
2. A.A. Al-Majed, C.M. Neumann, T.M. Brushart and T. Gordon, Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration, J. Neurosci. 20 (2000), 2602-2608.
3. D.N. Angelov, A. Gunkel, E. Stennert and W.F. Neiss, Recovery of original nerve supply after hypoglossal-facial anastomosis causes permanent motor hyperinnervation of the whisker-pad muscles in the rat, J. Comp. Neurol. 338 (1993), 214-224.
4. D.N. Angelov, W.F. Neiss, M. Streppel, J. Andermahr, K. Mader and E. Stennert, Nimodipine accelerates axonal sprouting after surgical repair of rat facial nerve, J. Neurosci. 16 (1996), 1041-1048.
5. D.N. Angelov, W.F. Neiss, A. Gunkel, M. Streppel, O. Guntinas-Lichius and E. Stennert, Nimodipine-accelerated hypoglossal sprouting prevents the postoperative hyperinnervation of target muscles after hypoglossal-facial anastomosis in the rat, Restor. Neurol. Neurosci. 11 (1997), 109-121.
6. D.N. Angelov, E. Skouras, O. Guntinas-Lichius, M. Streppel, A. Popratiloff, M. Walther, J. Klein, E. Stennert and W.F. Neiss, Contralateral trigeminal nerve lesion reduces polyneuronal muscle innervation after facial nerve repair in rats. Eur. J. Neurosci. 11 (1999) 1369-1378.
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. J. Arvidsson, Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP, J. Comp. Neurol. 211 (1982), 84-92.
9. R.S. Baker, M.W. Stava, K.R. Nelson, P.J. May, M.D. Huffman and J.D. Porter, Aberrant reinnervation of facial musculature in a subhuman primate: A correlative analysis of eyelid kinematics, muscle synkinesis, and motoneuron localization, Neurology 44 (1994), 2165-2173.
10. P. Banfai, Die angewandte klinische anatomie des nervus facialis. II. Die anastomosen, HNO 24 (1976), 289-294.
11. J.J. Baumel, Trigeminal-facial nerve communications. Their function in facial muscle innervation and reinnervation, Arch. Otolaryngol. 99 (1974), 34-44.
12. K. Blinzinger and G.W. Kreutzberg, Displacement of synaptic terminals from regenerating motoneurons by microglial cells, Z. Zellforsch. Mikrosk. Anat. 85 (1968), 145-157.
13. M. Bratzlavsky and H. vander Eecken, Altered synaptic organization in facial nucleus following facial nerve regeneration: An electrophysiological study in man, Ann. Neurol. 2 (1977), 71-73.
14. M.C. Brown, R.L. Holland, W.G. Hopkins and R.J. Keynes, An assessment of the spread of the signal for terminal sprouting within and between muscles, Brain Res. 210 (1981), 145-151.
15. M.C. Brown and W.G. Hopkins, Role of degenerating axon pathways in regeneration of mouse soleus motor axons, J. Physiol. 318 (1981), 365-373.
16. T.M. Brushart, Motor axons preferentially reinnervate motor pathways, J. Neurosci. 13 (1993), 2730-2738.
17. T.M. Brushart and M.M. Mesulam, Alteration in connections between muscle and anterior horn motoneurons after peripheral nerve repair, Science 208 (1980), 603-605.
18. T.M. Brushart and W.A. Seiler, Selective reinnervation of distal motor stumps by peripheral motor axons, Exp. Neurol. 97 (1987), 289-300.
19. T.M. Brushart, E.W. Henry and M.M. Mesulam, Reorganization of muscle afferent projections accompanies peripheral nerve regeneration, Neuroscience 6 (1981), 2053-2061.
20. T.M. Brushart, J. Gerber, P. Kessens, Y.-G. Chen and R.M. Royall, Contributions of pathway and neuron to preferential motor reinnervation, J. Neurosci. 18 (1998), 8674-8681.
21. G.E. Carvell and D.J. Simons, Biometric analyses of vibrissal tactile discrimination in the rat, J. Neurosci. 10 (1990), 2638-2648.
22. G.E. Carvell, D.J. Simons, S.H. Lichtenstein and P. Bryant, Electromyographic activity of mystacial pad musculature during whisking behaviour in the rat, Somatosens. Mot. Res. 8 (1991), 159-164.
23. J.M. Castro-Lopes, I. Tavares and A. Coimbra, GABA decreases in the spinal cord dorsal horn after peripheral neurectomy, Brain. Res. 620 (1993), 287-291.
24. N.L. Chiaia, Z. Allen E. Carson, G. Macdonald and R.W. Rhoades, Neonatal infraorbital nerve transection in rat results in peripheral trigeminal sprouting, J. Comp. Neurol. 274 (1988), 101-114.
25. + channel accumulation on axolemma of afferent endings in nerve end neuromas in Apteronotus, Neurosci. Lett. 102 (1989), 149-154.
26. J.T. Dodd and T.M. Jessell, Axon guidance and the patterning of neuronal projections in vertebrates, Science 242 (1988), 692-699.
27. J. Dörfl, The musculature of the mystacial vibrissae of the white mouse, J. Anat. 135 (1982), 147-154.
28. J. Dörfl, The innervation of the mystacial region of the white mouse. A topographical study, J. Anat. 142 (1985), 173-184.
29. S. Dohm, M. Streppel, O. Guntinas-Lichius, P. Pesheva, R. Probstmeier, M. Walther, W.F. Neiss, E. Stennert and D.N. Angelov, Local application of extracellular matrix proteins fails to reduce the number of axonal branches after varying reconstructive surgery on the rat facial nerve, Restor. Neurol. Neurosci. 16 (2000), 117-126.
30. I.D. Duncan and G.J. Baker, Experimental crush of the equine recurrent laryngeal nerve: A study of normal and aberrant reinnervation, Am. J. Vet. Res. 48 (1987), 431-438.
31. R.S. Erzurumlu and H.P. Killackey, Efferent connections of the brainstem trigeminal complex with the facial nucleus of the rat, J. Comp. Neurol. 188 (1979), 75-86.
32. J.C. Eccles, B. Libet and R.R. Young, The behaviour of chromatolyzed motoneurons studied by intracellular recording, J. Physiol. 143 (1958), 11-40.
33. E. Esslen, Electromyographic findings on two types of misdirection of regenerating axons, EEG Clin. Neurophysiol. 12 (1960), 738-741.
34. P.J. Evans, J.R. Bain, S.E. Mackinnon, A.P. Makino and D.A. Hunter, Selective reinnervation: A comparison of recovery following microsuture and conduit nerve repair, Brain. Res. 559 (1991), 315-321.
35. J.H. Ferguson, Hemifacial spasm and the facial nucleus, Ann. Neurol. 4 (1978), 97-103.
36. S.Y. Fu and T. Gordon, The cellular and molecular basis of peripheral nerve regeneration, Mol. Neurobiol. 14 (1997), 67-116.
37. H.J. Gundersen, Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson, J. Microsc. 143 (1986), 3-45.
38. O. Guntinas-Lichius, J. Mockenhaupt, E. Stennert and W.F. Neiss, Simplified nerve cell counting in the rat brainstem with the physical dissector using a drawing-microscope, J. Microsc. 172 (1993), 177-180.
39. O. Guntinas-Lichius and W.F. Neiss, Comparison of empirical and estimated efficiency in neuron counting by the physical dissector and in volume measurement by Cavalieri's method, Acta Stereol. 15 (1996), 131-139.
40. O. Guntinas-Lichius, K. Effenberger, D.N. Angelov, J. Klein, M. Streppel, E. Stennert and W.F. Neiss, Contributing factors to better functional recovery after inevitable delayed nerve repair: Enhanced regeneration through the predegenerated distal nerve stump, Exp. Neurol. 162 (2000), 98-111.
41. C. Harsh, S.J. Archibald and R.D. Madison, Double labeling of saphenous nerve neurone pools: A model for determining the accuracy of axon regeneration at the single neuron level, J. Neurosci. Meths. 39 (1991), 123-129.
42. R. Hennig and E. Dietrichs, Transient reinnervation of antagonistic muscles by the same motoneuron, Exp. Neurol. 130 (1994), 331-336.
43. C.F. Hinrichsen and C.D. Watson, Brain stem projections to the facial nucleus of the rat, Brain Behav. Evol. 22 (1983), 153-163.
44. M. Isokawa-Akesson and B.R. Komisaruk, Difference in projections to the lateral and medial facial nucleus: Anatomically separate pathways for rhythmical vibrissa movement in rats, Exp. Brain Res. 65 (1987), 385-398.
45. M. Ito and M. Kudo, Reinnervation by axon collaterals from single facial motoneurons to multiple muscle targets following axotomy in the adult guinea pig, Acta Anat. 151 (1994), 124-130.
46. M.F. Jacquin, D. Woerner, A.M. Szczepanik, V. Riecker, R.D. Mooney and R.W. Rhoades, Structure-function relationships in rat brainstem subnucleus interpolaris. I. Vibrissa primary afferents, J. Comp. Neurol. 243 (1986), 266-279.
47. M.F. Jacquin, D.S. Zahm, T.A. Henderson, J.P. Golden, E.M. Johnson, W.E. Renehan and B.G. Klein, Structure-function relationships in rat brainstem subnucleus interpolaris. X. Mechanisms underlying enlarged spared whisker projections after infraorbital nerve injury at birth, J. Neurosci. 13 (1993), 2946-2964.
48. C.-B. Jeng and R.E. Cogeshall, Regeneration of axons in tributary nerves, Brain Res. 310 (1984), 107-121.
49. J. Kimura and L.W. Lyon, Orbicularis oculi reflex in the Wallenberg syndrome: Alteration of the late reflex by lesions of the spinal tract and nucleus of the trigeminal nerve, J. Neurol. Neurosurg. Psychiatry 35 (1972), 228-233.
50. J. Kimura, R.L. Rodnitzky and S.H. Okawara, Electrophysiologic analysis of aberrant regeneration after facial nerve paralysis, Neurology 25 (1975), 989-993.
51. B.G. Klein, W.E. Renehan, M.F. Jacquin and R.W. Rhoades, Anatomical consequences of neonatal infraorbital nerve transection upon the trigeminal ganglion and vibrissa follicle nerves in the adult rat, J. Comp. Neurol. 268 (1988), 469-488.
52. B.R. Komisaruk, Synchrony between limbic system theta activity and rhythmical behaviour in rats, J. Comp. Physiol. Psychol. 70 (1970), 482-492.
53. A.R. Lieberman, The axon reaction: A review of the principle features of the perikaryal response to axon injury, Int. Rev. Neurobiol. 14 (1971), 49-125.
54. F.M. Love and W.J. Thompson, Glial cells promote muscle reinnervation by responding to activity-dependent postsynaptic signals, J. Neurosci. 19 (1999), 10390-10396.
55. S.E. Mackinnon, A.L. Dellon, G. Lundborg, A.R. Hudson and D.A. Hunter, A study of neurotrophism in a primate model, J. Hand Surg. 11-A (1986), 888-894.
56. S.E. Mackinnon, A.L. Dellon and J.P. Obrien, Changes in nerve fiber diameters distal to a nerve repair in the rat sciatic nerve model, Muscle Nerve 14 (1991), 1116-1122.
57. R.D. Madison, S.J. Archibald and T.M. Brushart, Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons, J. Neurosci. 16 (1996), 5698-5703.
58. R.D. Madison, S.J. Archibald, R. Lacin and C. Krarup, Factors contributing to preferential motor reinnervation in the primate peripheral nervous system, J. Neurosci. 19 (1999), 11007-11016.
59. L.M. Mendell, Modifiability of spinal synapses, Physiol. Rev. 64 (1984), 260-324.
60. L.M. Mendell, J.B. Munson and J.G. Scott, Alterations of synapses on axotomized motoneurones, J. Physiol. 255 (1976), 67-79.
61. C. Molander and H. Aldskogius, Directional specificity of regenerating neurons after peripheral nerve crush or transection and epineurial suture: A sequential double-labeling study in the rat, Restor. Neurol. Neurosci. 4 (1992), 339-344.
62. A.R. Moller and P.J. Jannetta, Blink reflex in patients with hemifacial spasm. Observations during microvascular decompression operations, J. Neurol. Sci. 72 (1986), 171-182.
63. L. Montserrat and M. Benito, Facial synkinesis and aberrant regeneration of facial nerve, Adv. Neurol. 49 (1988), 211-224.
64. C.J. Moran and J.G. Neely, Patterns of facial nerve synkinesis, Laryngoscope 106 (1996), 1491-1496.
65. J. Morris, A.R. Hudson and G. Weddell, Study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy. II. The development of the "regenerating unit", Z. Zellforsch. Mikrosk. Anat. 124 (1972), 103-130.
66. B.L. Munger and W.E. Renehan, Degeneration and regeneration of peripheral nerve in the rat trigeminal system: III. Abnormal sensory reinnervation of rat guard hairs following nere transection and crush, J. Comp. Neurol. 283 (1989), 169-176.
67. T. Naumann, W. Härtig and M. Frotscher, Retrograde tracing with Fluoro-Gold: Different methods of tracer detection at the ultrastructural level and neurodegenerative changes of back-filled neurons in ling-term studies, J. Neurosci. Meths. 103 (2000), 11-21.
68. M. Ochi, M. Wakasa, Y. Ikuta and W.H. Kwong, Nerve regeneration in predegenerated basal lamina graft: The effect of duration of predegeneration on axonal extension, Exp. Neurol. 128 (1994), 216-225.
69. A.D. Owen and M.M. Bird, Role of glutamate in the regulation of the outgrowth and motility of neurites from mouse spinal cord neurons in culture, J. Anat. 191 (1997), 301-307.
70. G. Pinganaud, I. Bernat, P. Buisseret and C. Buisseret-Delmas, Trigeminal projections to hypoglossal and facial motor nuclei in the rat, J. Comp. Neurol. 415 (1999), 91-104.
71. A.S. Popratiloff, W.F. Neiss, E. Skouras, M. Streppel, O. Guntinas-Lichius and D.N. Angelov, Evaluation of muscle reinnervation employing pre- and post-axotomy injections of fluorescent retrograde tracers, Brain Res. Bull. 54 (2001), 115-123.
72. F.L. Rice, E. Kinnman, H. Aldskogius, O. Johansson and J. Arvidsson, The innervation of the mystacial pad of the rat as revealed by PGP 9.5 immunofluorescence, J. Comp. Neurol. 337 (1993), 366-385.
73. M.M. Rich and J.W. Lichtman, In vivo visualization of pre- and postsynaptic change during synapse elimination in reinnervated mouse muscle, J. Neurosci. 9 (1989), 1781-1805.
74. R.W. Roades, G.R. Belford and H.P. Killackey, Receptive field properties of rat VPM neurons before and after selective kainic acid lesions of the trigeminal brainstem complex, J. Neurophysiol. 57 (1987), 1577-1600.
75. R.W. Roades, H.L. Enfiejian, N.L. Chiaia, G.J. Macdonald, M.W. Miller, P. McCann and C.M. Goddard, Birthdates of trigeminal ganglion cells contributing axons to the infraorbital nerve and specific vibrissal follicles in the rat, J. Comp. Neurol. 307 (1991), 163-175.
76. K. Sadjadpour, Postfacial palsy phenomena: Faulty nerve regeneration or ephaptic transmission? Brain Res. 95 (1975), 403-406.
77. K. Semba and M.D. Egger, The facial "motor" nerve of the rat: Control of vibrissal movement and examination of motor and sensory components, J. Comp. Neurol. 247 (1986), 144-158.
78. K. Semba, H. Szechtman and B.R. Komisaruk, Synchrony among rhythmical facial tremor, neocortical "alpha" waves, and thalamic non-sensory neuronal bursts in intact awake rats, Brain Res. 195 (1980), 281-298.
79. G.D. Shawe, On the number of branches formed by regenerating nerve fibers, Br. J. Surg. 42 (1954), 474-488.
80. Y.J. Son, J.T. Trachtenberg and W.J. Thompson, Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions, Trends Neurosci. 19 (1996), 280-285.
81. M. Streppel, D.N. Angelov, O. Guntinas-Lichius, R.D. Hilgers, J.D. Rosenblatt, E. Stennert and W.F. Neiss, Slow axonal regrowth but extreme hyperinnervation of target muscle after suture of the facial nerve in aged rats, Neurobiol. Aging 19 (1998), 83-88.
82. A.J. Sumner, Aberrant reinnervation, Muscle Nerve 13 (1990), 801-803.
83. M.J. Titmus and D.S. Faber, Axotomy-induced alterations in the electrophysiological characteristics of neurons, Prog. Neurobiol. 35 (1990), 1-51.
84. J.T. Trachtenberg and W.J. Thompson, Schwann cell apoptosis ad developing neuromuscular junctions is regulated by glial growth factor, Nature 379 (1996), 174-177.
85. J.B. Travers and R. Norgren, Afferent projections to the oral motor nuclei in the rat, J. Comp. Neurol. 220 (1983), 280-298.
86. J. Valls-Sole and E.S. Tolosa, Blink reflex excitability cycle in hemifacial spasm, Neurology 39 (1989), 1061-1066.
87. E.D. Vaughan and D. Richardson, Facial nerve reconstruction following ablative parotid surgery, Br. J. Oral Maxillofac. Surg. 31 (1993), 274-280.
88. W.I. Welker, Analysis of sniffing of the albino rat, Behaviour 22 (1964), 223-244.
89. C.J. Woolf, P. Shortland and R.R. Coggeshall, Peripheral nerve injury triggers central sprouting of myelinated afferents, Nature 355 (1992), 75-78.
90. Q. Zhao, L.B. Dahlin, M. Kanje, G. Lundborg and S.-B. Lu, Axonal projections and functional recovery following fascicular repair of the rat sciatic nerve with Y-tunneled silicone chambers, Restor. Neurol. Neurosci. 4 (1992), 13-19.