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Journal of Anatomy logoLink to Journal of Anatomy
. 1986 Jun;146:117–130.

Reinnervation of skeletal muscle in the tongue by preganglionic parasympathetic vagal neurons.

B A Flumerfelt 1, J A Kiernan 1, J P Krcek 1, J Sholdice 1
PMCID: PMC1166528  PMID: 2447049

Abstract

Reinnervation of the skeletal muscle in the tongue following vago-hypoglossal anastomosis was studied by means of retrograde labelling with horseradish peroxidase and anterograde labelling with the autoradiographic tracing method combined with acetylcholinesterase staining for motor endplates. The proximal stump of the transected vagus nerve was anastomosed to the distal stump of the transected hypoglossal nerve in the neck, or in the thorax below the emergence of the recurrent laryngeal fibres. After 2-3 months, reinnervation of the tongue by vagal fibres was studied. Control cases in which the hypoglossal nerve was transected, but anastomosis was not performed, revealed that innervation of the lingual muscle is derived entirely from the hypoglossal nerves. Following unilateral vago-hypoglossal anastomosis a reduced number of fine nerve fibres terminated in relation to the acetylcholinesterase-stained endplates on the side of the anastomosis. At no time were fibres on either side observed to form sprouts which crossed the midline. Horseradish peroxidase (HRP) was injected into the tongue to determine the origin of the fibres that reinnervated the lingual muscle following anastomosis. On the side of the anastomosis, HRP-labelled neurons were present within the dorsal motor nucleus of the vagus and were absent from the hypoglossal nucleus. When the anastomosis was performed in the neck, neurons within the nucleus ambiguous were also labelled with HRP, but this was not observed following anastomosis in the thorax below the recurrent laryngeal nerve. When tritiated amino acids were injected into the dorsal motor nucleus of the vagus, the motor endplates on the anastomosed side of the tongue were labelled autoradiographically. This labelling could not be abolished by transecting both hypoglossal nerves, confirming that the labelling was due to reinnervation by vagal fibres. It is concluded that anastomosis of the proximal end of the transected vagus nerve to the distal end of the transected hypoglossal nerve is followed by regeneration of the vagal fibres which cross the anastomosis and reinnervate the denervated motor endplates in the tongue. The cell bodies of origin are located within the dorsal motor nucleus of the vagus and are preganglionic parasympathetic neurons.

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Selected References

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  1. BROWN J. O., SATINSKY V. P. Functional restoration of the paralyzed diaphragm following the cross-union of the vagus and phrenic nerves. Am J Med Sci. 1951 Dec;222(6):613–622. doi: 10.1097/00000441-195112000-00001. [DOI] [PubMed] [Google Scholar]
  2. Bennett M. R., McLachlan E. M., Taylor R. S. The formation of synapses in mammalian striated muscle reinnervated with autonomic preganglionic nerves. J Physiol. 1973 Sep;233(3):501–517. doi: 10.1113/jphysiol.1973.sp010320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Calaresu F. R., Faiers A. A., Mogenson G. J. Central neural regulation of heart and blood vessels in mammals. Prog Neurobiol. 1975;5(1):1–35. doi: 10.1016/0301-0082(75)90006-4. [DOI] [PubMed] [Google Scholar]
  4. Coget J., Rousseau J. P. Reinnervation of striated muscle by peripheral vagal fibres cut above or below the nodose ganglion in the cat and rabbit. J Physiol. 1983 Feb;335:481–493. doi: 10.1113/jphysiol.1983.sp014545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cowan W. M., Gottlieb D. I., Hendrickson A. E., Price J. L., Woolsey T. A. The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res. 1972 Feb 11;37(1):21–51. doi: 10.1016/0006-8993(72)90344-7. [DOI] [PubMed] [Google Scholar]
  6. Davis H. L., Kiernan J. A. Effect of nerve extract of atrophy of denervated or immobilized muscles. Exp Neurol. 1981 Jun;72(3):582–591. doi: 10.1016/0014-4886(81)90007-8. [DOI] [PubMed] [Google Scholar]
  7. Gruber H. Motor innervation of striated oesophageal muscle. Part 2. Characteristics of the oesophagomotor fibres in the rat studied by implanting the vagus nerve into a skeletal muscle. J Neurol Sci. 1978 Apr;36(2):171–186. doi: 10.1016/0022-510x(78)90081-3. [DOI] [PubMed] [Google Scholar]
  8. Guth L. "Trophic" influences of nerve on muscle. Physiol Rev. 1968 Oct;48(4):645–687. doi: 10.1152/physrev.1968.48.4.645. [DOI] [PubMed] [Google Scholar]
  9. HOLT S. J., WITHERS R. F. J. Cytochemical localization of esterases using indoxyl derivatives. Nature. 1952 Dec 13;170(4337):1012–1014. doi: 10.1038/1701012a0. [DOI] [PubMed] [Google Scholar]
  10. Landmesser L. Contractile and electrical responses of vagus-innervated frog sartorius muscles. J Physiol. 1971 Mar;213(3):707–725. doi: 10.1113/jphysiol.1971.sp009410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Langley J. N., Anderson H. K. The union of different kinds of nerve fibres. J Physiol. 1904 Aug 22;31(5):365–391. doi: 10.1113/jphysiol.1904.sp001042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Markelonis G., Tae Hwan O. H. A sciatic nerve protein has a trophic effect on development and maintenance of skeletal muscle cells in culture. Proc Natl Acad Sci U S A. 1979 May;76(5):2470–2474. doi: 10.1073/pnas.76.5.2470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McIsaac G., Kiernan J. A. Complete staining of neuromuscular innervation with bromoindigo and silver. Stain Technol. 1974 Jul;49(4):211–214. doi: 10.3109/10520297409116980. [DOI] [PubMed] [Google Scholar]
  14. Mesulam M. M. The blue reaction product in horseradish peroxidase neurohistochemistry: incubation parameters and visibility. J Histochem Cytochem. 1976 Dec;24(12):1273–1280. doi: 10.1177/24.12.63512. [DOI] [PubMed] [Google Scholar]
  15. Shapiro R. E., Miselis R. R. The central organization of the vagus nerve innervating the stomach of the rat. J Comp Neurol. 1985 Aug 22;238(4):473–488. doi: 10.1002/cne.902380411. [DOI] [PubMed] [Google Scholar]
  16. Vera C. L., Luco J. V. Reinnervation of smooth and striated muscle by sensory nerve fibers. J Neurophysiol. 1967 May;30(3):620–627. doi: 10.1152/jn.1967.30.3.620. [DOI] [PubMed] [Google Scholar]
  17. Wilson A. S., Krcek J. P. Restoration of function in the paralyzed diaphragm. Exp Neurol. 1975 Jun;47(3):490–502. doi: 10.1016/0014-4886(75)90081-3. [DOI] [PubMed] [Google Scholar]

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