Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1973 Sep;233(3):501–517. doi: 10.1113/jphysiol.1973.sp010320

The formation of synapses in mammalian striated muscle reinnervated with autonomic preganglionic nerves

M R Bennett, Elspeth M McLachlan, R S Taylor
PMCID: PMC1350589  PMID: 4127829

Abstract

1. A study has been made of the formation of synapses during reinnervation of the hemidiaphragm of adult rabbits with preganglionic fibres of the thoracic vagus, using histological, ultrastructural and electrophysiological techniques.

2. Following reinnervation with preganglionic axons, silver-stained nerve terminals were found in association with cholinesterase-stained end-plates only in the region of the muscle corresponding to the original innervation band.

3. The fine preganglionic axons retained their normal structure in striated muscle, but were found to synapse over discrete areas of dimensions not larger than those of the original end-plates.

4. The regenerated varicose preganglionic nerve terminals were observed with the electronmicroscope in positions either overlying or in the vicinity of the old synaptic folds.

5. Spontaneous potentials and evoked synaptic potentials were recorded only in the middle of the muscle fibres after vagus reinnervation.

6. In a few cases, multiple synaptic potentials with similar time courses were recorded, suggesting that several axons had formed synapses at a single site on a muscle fibre.

7. It has been shown that, during reinnervation of adult mammalian striated muscle fibres with nerves other than those of the somatic system, synapses are formed preferentially in the region of the old end-plates.

Full text

PDF
505

Images in this article

504Text-fig. 1
on p.504
516-1Plate 1
on p.516-1
516-2Plate 2
on p.516-2
516-3a
on p.516-3
516-3b-e
on p.516-3
516-4Plate 4
on p.516-4
516-5Plate 5
on p.516-5

Selected References

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

  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. Beattie J., Duel A. B., Ballance C. The Effects of Stimulation of the Hypothalamic Pupillo-Dilator Centre after Successful Anastomoses Between the Cervical Sympathetic and Certain Motor Nerves. J Anat. 1932 Apr;66(Pt 3):283–299. [PMC free article] [PubMed] [Google Scholar]
  3. Bennett M. R., McLachlan E. M., Taylor R. S. The formation of synapses in reinnervated mammalian striated muscle. J Physiol. 1973 Sep;233(3):481–500. doi: 10.1113/jphysiol.1973.sp010319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett M. R., Pettigrew A. G., Taylor R. S. The formation of synapses in reinnervated and cross-reinnervated adult avian muscle. J Physiol. 1973 Apr;230(2):331–357. doi: 10.1113/jphysiol.1973.sp010191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blackman J. G., Crowcroft P. J., Devine C. E., Holman M. E., Yonemura K. Transmission from pregnanglionic fibres in the hypogastric nerve to peripheral ganglia of male guinea-pigs. J Physiol. 1969 May;201(3):723–743. doi: 10.1113/jphysiol.1969.sp008784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blackman J. G., Purves R. D. Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig. J Physiol. 1969 Jul;203(1):173–198. doi: 10.1113/jphysiol.1969.sp008858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. COERS C. Structural organization of the motor nerve endings in mammalian muscle spindles and other striated muscle fibers. Am J Phys Med. 1959 Aug;38:166–175. [PubMed] [Google Scholar]
  8. COUTEAUX R. THE DIFFERENTIATION OF SYNAPTIC AREAS. Proc R Soc Lond B Biol Sci. 1963 Nov 19;158:457–480. doi: 10.1098/rspb.1963.0058. [DOI] [PubMed] [Google Scholar]
  9. DEL CASTILLO J., KATZ B. Quantal components of the end-plate potential. J Physiol. 1954 Jun 28;124(3):560–573. doi: 10.1113/jphysiol.1954.sp005129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DESMEDT J. E. The physio-pathology of neuromuscular transmission and the trophic influence of motor innervation. Am J Phys Med. 1959 Dec;38:248–261. [PubMed] [Google Scholar]
  11. Dennis M. J., Harris A. J., Kuffler S. W. Synaptic transmission and its duplication by focally applied acetylcholine in parasympathetic neurons in the heart of the frog. Proc R Soc Lond B Biol Sci. 1971 Apr 27;177(1049):509–539. doi: 10.1098/rspb.1971.0045. [DOI] [PubMed] [Google Scholar]
  12. Duchen L. W. Changes in motor innervation and cholinesterase localization induced by botulinum toxin in skeletal muscle of the mouse: differences between fast and slow muscles. J Neurol Neurosurg Psychiatry. 1970 Feb;33(1):40–54. doi: 10.1136/jnnp.33.1.40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. EVANS D. H., MURRAY J. G. Regeneration of non-medullated nerve fibres. J Anat. 1954 Oct;88(4):465–480. [PMC free article] [PubMed] [Google Scholar]
  14. Elfvin L. G. Ultrastructural studies on the synaptology of the inferior mesenteric ganglion of the cat. 3. The structure and distribution of the axodendritic and dendrodendritic contacts. J Ultrastruct Res. 1971 Nov;37(3):432–448. doi: 10.1016/s0022-5320(71)80137-5. [DOI] [PubMed] [Google Scholar]
  15. Filogamo G., Gabella G. Cholinesterase behaviour in the denervated and reinnervated muscles. Acta Anat (Basel) 1966;63(2):199–214. doi: 10.1159/000142789. [DOI] [PubMed] [Google Scholar]
  16. GUTH L., FRANK K. Restoration of diaphragmatic function following vagophrenic anastomosis in the rat. Exp Neurol. 1959 Apr;1(1):1–12. doi: 10.1016/0014-4886(59)90009-3. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. GUTH L., SOUTTER L., FRANK K., CAMPBELL J. B., LLOYD J. B. Diaphragmatic function following anastomosis of recurrent laryngeal and phrenic nerves. Exp Neurol. 1960 Jun;2:251–260. doi: 10.1016/0014-4886(60)90012-1. [DOI] [PubMed] [Google Scholar]
  19. GUTH L., ZALEWSKI A. A. Disposition of cholinesterase following implantation of nerve into innervated and denervated muscle. Exp Neurol. 1963 Apr;7:316–326. doi: 10.1016/0014-4886(63)90078-5. [DOI] [PubMed] [Google Scholar]
  20. Gutmann E. The reinnervation of muscle by sensory nerve fibres. J Anat. 1945 Jan;79(Pt 1):1–8.4. [PMC free article] [PubMed] [Google Scholar]
  21. HOFFMAN H. A study of the factors influencing innervation of muscles by implanted nerves. Aust J Exp Biol Med Sci. 1951 Jul;29(4):289–308. doi: 10.1038/icb.1951.35. [DOI] [PubMed] [Google Scholar]
  22. HOFFMAN H. Fate of interrupted nerve-fibres regenerating into partially denervated muscles. Aust J Exp Biol Med Sci. 1951 May;29(3):211–219. doi: 10.1038/icb.1951.25. [DOI] [PubMed] [Google Scholar]
  23. Hoh J. F. Selective reinnervation of fast-twitch and slow-graded muscle fibers in the toad. Exp Neurol. 1971 Feb;30(2):263–276. doi: 10.1016/s0014-4886(71)80006-7. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. MILEDI R. Properties of regenerating neuromuscular synapses in the frog. J Physiol. 1960 Nov;154:190–205. doi: 10.1113/jphysiol.1960.sp006573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nakai J. The development of neuromuscular junctions in cultures of chick embryo tissues. J Exp Zool. 1969 Jan;170(1):85–106. doi: 10.1002/jez.1401700108. [DOI] [PubMed] [Google Scholar]
  29. Perri V., Sacchi O., Caella C. Electrical properties and synaptic connections of the sympathetic neurons in the rat and guinea-pig superior cervical ganglion. Pflugers Arch. 1970;314(1):40–54. doi: 10.1007/BF00587045. [DOI] [PubMed] [Google Scholar]
  30. 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]

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

RESOURCES