Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1983 Feb;335:467–479. doi: 10.1113/jphysiol.1983.sp014544

Reinnervation of skeletal muscles by vagal sensory fibres in the sheep, cat and rabbit.

M Falempin, J P Rousseau
PMCID: PMC1197363  PMID: 6875888

Abstract

Fibres of the sterno-cleido-mastoid (s.c.m.) muscle normally innervated by the accessory nerve have been reinnervated by afferent fibres of the vagus nerve after supranodose vagal-accessory nerve anastomoses or direct implantation of the vagus nerve into the s.c.m. in cats, rabbits and sheep. The afferent fibres contributing to this reinnervation were confirmed to be cholinergic as transmission was blocked by gallamine, and histochemical evidence obtained of cholinergic motor end-plates. The association of the axons of cells of the nodose ganglion and s.c.m. muscle fibres was further demonstrated when horseradish peroxidase injected into the s.c.m. was detected in somata of nodose ganglia cells. The largest number of reinnervated motor units, fifty, identified by electromyographic recording from the s.c.m. muscle, represents a small proportion of the afferent fibres in the vagus. Factors contributing to this degree of reinnervation are discussed. Conduction velocities in afferent fibres involved in the reinnervation were in the range less than 2.5 to greater than 35 m/s with 36% being 6-12 m/s. Between 40 and 98.5% of the myelinated fibres of the accessory nerve replaced by vagal afferent fibres were less than 6 microns in diameter. The afferent nerve fibres involved in the reinnervation were associated with larynx, respiratory tract, oesophagus and stomach. Afferent discharges recorded as bursts of electromyographic potentials in the s.c.m. occurred during spontaneous movements of these structures and on their mechanical stimulation.

Full text

PDF
467

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adrian E. D. Afferent impulses in the vagus and their effect on respiration. J Physiol. 1933 Oct 6;79(3):332–358. doi: 10.1113/jphysiol.1933.sp003053. [DOI] [PMC free article] [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. DE CASTRO F. Aspects anatomiques de la transmission synaptique ganglionnaire chez les mammifères. Arch Int Physiol. 1951 Dec;59(4):479–525. doi: 10.3109/13813455109150845. [DOI] [PubMed] [Google Scholar]
  4. DUSSARDIER M. Contrôle nerveux du rythme gastrique des ruminants. J Physiol (Paris) 1955;47(1):170–173. [PubMed] [Google Scholar]
  5. Fujiwara M., Kurahashi K. Cholinergic nature of the primary afferent vagus synapsed in cross anastomosed superior cervical ganglia. Life Sci. 1976 Oct 15;19(8):1175–1180. doi: 10.1016/0024-3205(76)90252-6. [DOI] [PubMed] [Google Scholar]
  6. Fujiwara M., Kurahashi K., Mizuno N., Nakamura Y. Involvement of nicotinic and muscarinic receptors in synaptic transmission in cat superior cervical ganglions reinnervated by vagal primary afferent axons. J Pharmacol Exp Ther. 1978 Apr;205(1):77–90. [PubMed] [Google Scholar]
  7. Fujiwara M., Kurahashi K. Pharmacological studies on the superior cervical ganglion reinnervated by the afferent vagus. Proc West Pharmacol Soc. 1975;18:225–228. [PubMed] [Google Scholar]
  8. GUTH L. Neuromuscular function after regeneration of interrupted nerve fibers into partially denervated muscle. Exp Neurol. 1962 Aug;6:129–141. doi: 10.1016/0014-4886(62)90083-3. [DOI] [PubMed] [Google Scholar]
  9. GWYN D. G., HEARDMAN V. A CHOLINESTERASE-BIELSCHOWSKY STAINING METHOD FOR MAMMALIAN MOTOR END PLATES. Stain Technol. 1965 Jan;40:15–18. doi: 10.3109/10520296509116367. [DOI] [PubMed] [Google Scholar]
  10. Gottschall J., Zenker W., Neuhuber W., Mysicka A., Müntener M. The sternomastoid muscle of the rat and its innervation. Muscle fiber composition, perikarya and axons of efferent and afferent neurons. Anat Embryol (Berl) 1980;160(3):285–300. doi: 10.1007/BF00305109. [DOI] [PubMed] [Google Scholar]
  11. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  12. Grinnell A. D., Rheuben M. B. The physiology, pharmacology, and trophic effectiveness of synapses formed by autonomic preganglionic nerves on frog skeletal muscle. J Physiol. 1979 Apr;289:219–240. doi: 10.1113/jphysiol.1979.sp012734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gruber H., Freilinger G., Holle H., Mayr R. Motor endplates in autologous muscle transplants. Experientia. 1974 Oct 15;30(10):1191–1192. doi: 10.1007/BF01923683. [DOI] [PubMed] [Google Scholar]
  14. Hanker J. S., Yates P. E., Metz C. B., Rustioni A. A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J. 1977 Nov;9(6):789–792. doi: 10.1007/BF01003075. [DOI] [PubMed] [Google Scholar]
  15. Helke C. J., O'Donohue T. L., Jacobowitz D. M. Substance P as a baro- and chemoreceptor afferent neurotransmitter: immunocytochemical and neurochemical evidence in the rat. Peptides. 1980 Spring;1(1):1–9. doi: 10.1016/0196-9781(80)90027-3. [DOI] [PubMed] [Google Scholar]
  16. IGGO A. Gastro-intestinal tension receptors with unmyelinated afferent fibres in the vagus of the cat. Q J Exp Physiol Cogn Med Sci. 1957 Jan;42(1):130–143. doi: 10.1113/expphysiol.1957.sp001228. [DOI] [PubMed] [Google Scholar]
  17. IGGO A. Tension receptors in the stomach and the urinary bladder. J Physiol. 1955 Jun 28;128(3):593–607. doi: 10.1113/jphysiol.1955.sp005327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iggo A., Leek B. F. An electrophysiological study of single vagal efferent units associated with gastric movements in sheep. J Physiol. 1967 Jul;191(1):177–204. doi: 10.1113/jphysiol.1967.sp008244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kobayashi R. M., Brownstein M., Saavedra J. M., Palkovits Choline acetyltransferase content in discrete regions of the rat brain stem. J Neurochem. 1975 Apr;24(4):637–640. [PubMed] [Google Scholar]
  20. Landmesser L. Pharmacological properties, cholinesterase activity and anatomy of nerve-muscle junctions in vagus-innervated frog sartorius. J Physiol. 1972 Jan;220(1):243–256. doi: 10.1113/jphysiol.1972.sp009704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Leek B. F. Reticulo-ruminal mechanoreceptors in sheep. J Physiol. 1969 Jun;202(3):585–609. doi: 10.1113/jphysiol.1969.sp008829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MATSUMURA M., KOELLE G. B. The nature of synaptic transmission in the superior cervical ganglion following reinnervation by the afferent vagus. J Pharmacol Exp Ther. 1961 Oct;134:28–46. [PubMed] [Google Scholar]
  23. Mei N. Mécanorécepteurs vagaux digestifs chez le chat. Exp Brain Res. 1970;11(5):502–514. [PubMed] [Google Scholar]
  24. PAINTAL A. S. A study of gastric stretch receptors; their role in the peripheral mechanism of satiation of hunger and thirst. J Physiol. 1954 Nov 29;126(2):255–270. doi: 10.1113/jphysiol.1954.sp005207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rapoport S. Location of sternocleidomastoid and trapezius motoneurons in the cat. Brain Res. 1978 Nov 10;156(2):339–344. doi: 10.1016/0006-8993(78)90515-2. [DOI] [PubMed] [Google Scholar]
  26. Roman C. Contrôle nerveux du péristaltisme oesophagien. J Physiol (Paris) 1966 Jan-Feb;58(1):79–108. [PubMed] [Google Scholar]
  27. Rousseau J. P., Falempin M. Activity of gut receptors in the conscious sheep. Ann Rech Vet. 1979;10(2-3):189–191. [PubMed] [Google Scholar]
  28. 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]
  29. Zalewski A. A. Effects of reinnervation on denervated skeletal muscle by axons of motor, sensory, and sympathetic neurons. Am J Physiol. 1970 Dec;219(6):1675–1679. doi: 10.1152/ajplegacy.1970.219.6.1675. [DOI] [PubMed] [Google Scholar]
  30. Zalewski A. A. Regeneration of taste buds after reinnervation by peripheral or central sensory fibers of vagal ganglia. Exp Neurol. 1969 Nov;25(3):429–437. doi: 10.1016/0014-4886(69)90137-x. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES