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. 1963 Dec 1;19(3):529–550. doi: 10.1083/jcb.19.3.529

CORRELATION OF FINE STRUCTURE AND PHYSIOLOGY OF THE INNERVATION OF SMOOTH MUSCLE IN THE GUINEA PIG VAS DEFERENS

Neil C R Merrillees 1, Geoffrey Burnstock 1, Mollie E Holman 1
PMCID: PMC2106328  PMID: 14086135

Abstract

An electron microscope study of the innervation of smooth muscle of the guinea pig vas deferens was undertaken in order to find a structural basis for recent electrophysiological observations. The external longitudinal muscle coat was examined in transverse section. Large areas of the surfaces of adjacent muscle cells were 500 to 800 A apart. Closer contacts were rare. A special type of close contact suggested cytoplasmic transfer between neighbouring cells. Groups of non-myelinated axons from ganglia at the distal end of the hypogastric nerve ramified throughout the muscle. Some small axon bundles and single axons lay in narrow fissures within closely packed muscle masses. Many axons contained "synaptic vesicles." About 25 per cent of the muscle fibres in the plane of section were within 0.25 µ of a partly naked axon; of these 15 per cent were within 500 A of the axon, and about 1 per cent made close contact (200 A) with a naked axon. It is unlikely that every muscle fibre is in close contact with an axon, and it is not possible for every fibre to have many such contacts. Muscle fibres are probably activated by both diffusion of transmitter from naked portions of axons a fraction of a micron distant, and electrotonic spread of activity from neighbouring cells.

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Selected References

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

  1. BERGMAN R. A. Intercellular bridges in ureteral smooth muscle. Bull Johns Hopkins Hosp. 1958 Apr;102(4):195–202. [PubMed] [Google Scholar]
  2. BURNSTOCK G., HOLMAN M. E. Autonomic nerve-smooth muscle transmission. Nature. 1960 Sep 10;187:951–952. doi: 10.1038/187951a0. [DOI] [PubMed] [Google Scholar]
  3. BURNSTOCK G., HOLMAN M. E. Effect of denervation and of reserpine treatment on transmission at sympathetic nerve endings. J Physiol. 1962 Mar;160:461–469. doi: 10.1113/jphysiol.1962.sp006859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BURNSTOCK G., HOLMAN M. E. Spontaneous potential at sympathetic nerve endings in smooth muscle. J Physiol. 1962 Mar;160:446–460. doi: 10.1113/jphysiol.1962.sp006858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BURNSTOCK G., HOLMAN M. E. The transmission of excitation from autonomic nerve to smooth muscle. J Physiol. 1961 Jan;155:115–133. doi: 10.1113/jphysiol.1961.sp006617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. CAESAR R., EDWARDS G. A., RUSKA H. Architecture and nerve supply of mammalian smooth muscle tissue. J Biophys Biochem Cytol. 1957 Nov 25;3(6):867–878. doi: 10.1083/jcb.3.6.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DE ROBERTIS E. D., BENNETT H. S. Some features of the submicroscopic morphology of synapses in frog and earthworm. J Biophys Biochem Cytol. 1955 Jan;1(1):47–58. doi: 10.1083/jcb.1.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DE ROBERTIS E., PELLEGRINO DE IRALDI A., RODRIGUEZ DE LORES GARNAIZ G., SALGANICOFF L. Cholinergic and non-cholinergic nerve endings in rat brain. I. Isolation and subcellular distribution of acetylcholine and acetylcholinesterase. J Neurochem. 1962 Jan-Feb;9:23–35. doi: 10.1111/j.1471-4159.1962.tb07489.x. [DOI] [PubMed] [Google Scholar]
  9. Dewey M. M., Barr L. Intercellular Connection between Smooth Muscle Cells: the Nexus. Science. 1962 Aug 31;137(3531):670–672. doi: 10.1126/science.137.3531.670-a. [DOI] [PubMed] [Google Scholar]
  10. ECCLES J. C. The mechanism of synaptic transmission. Ergeb Physiol. 1961;51:299–430. [PubMed] [Google Scholar]
  11. ELFVIN L. G. Electron-microscopic investigation of filament structures in unmyelinated fibers of cat splenic nerve. J Ultrastruct Res. 1961 Mar;5:51–64. doi: 10.1016/s0022-5320(61)80005-1. [DOI] [PubMed] [Google Scholar]
  12. ELFVIN L. G. The ultrastructure of unmyelinated fibers in the splenic nerve of the cat. J Ultrastruct Res. 1958 Aug;1(4):428–454. doi: 10.1016/s0022-5320(58)90012-1. [DOI] [PubMed] [Google Scholar]
  13. GRAY E. G., WHITTAKER V. P. The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J Anat. 1962 Jan;96:79–88. [PMC free article] [PubMed] [Google Scholar]
  14. HESS A. The fine structure and morphological organization of non-myelinated nerve fibres. Proc R Soc Lond B Biol Sci. 1956 Mar 13;144(917):496–506. doi: 10.1098/rspb.1956.0006. [DOI] [PubMed] [Google Scholar]
  15. KATZ B. Microphysiology of the neuromuscular junction; a physiological quantum of action at the myoeneural junction. Bull Johns Hopkins Hosp. 1958 Jun;102(6):275–295. [PubMed] [Google Scholar]
  16. KATZ B. Microphysiology of the neuromuscular junction; the chemo-receptor function of the motor end-plate. Bull Johns Hopkins Hosp. 1958 Jun;102(6):296–312. [PubMed] [Google Scholar]
  17. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. LUNDBERG A. Electrophysiology of salivary glands. Physiol Rev. 1958 Jan;38(1):21–40. doi: 10.1152/physrev.1958.38.1.21. [DOI] [PubMed] [Google Scholar]
  19. MARK J. S. An electron microscope study of uterine smooth muscle. Anat Rec. 1956 Jul;125(3):473–493. doi: 10.1002/ar.1091250306. [DOI] [PubMed] [Google Scholar]
  20. PALAY S. L. Synapses in the central nervous system. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):193–202. doi: 10.1083/jcb.2.4.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. PEASE D. C., MOLINARI S. Electron microscopy of muscular arteries; pial vessels of43 the cat and monkey. J Ultrastruct Res. 1960 Jun;3:447–468. doi: 10.1016/s0022-5320(60)90022-8. [DOI] [PubMed] [Google Scholar]
  22. PROSSER C. L., BURNSTOCK G., KAHN J. Conduction in smooth muscle: comparative structural properties. Am J Physiol. 1960 Sep;199:545–552. doi: 10.1152/ajplegacy.1960.199.3.545. [DOI] [PubMed] [Google Scholar]
  23. RICHARDSON K. C. Electronmicroscopic observations on Auerbach's plexus in the rabbit, with special reference to the problem of smooth muscle innervation. Am J Anat. 1958 Jul;103(1):99–135. doi: 10.1002/aja.1001030105. [DOI] [PubMed] [Google Scholar]
  24. RICHARDSON K. C. The fine structure of autonomic nerve endings in smooth muscle of the rat vas deferens. J Anat. 1962 Oct;96:427–442. [PMC free article] [PubMed] [Google Scholar]
  25. SJOSTRAND N. O. Inhibition by ganglionic blocking agents of the motor response of the isolated guinea-pig vas deferens to hypogastric nerve stimulation. Acta Physiol Scand. 1962 Mar-Apr;54:306–315. doi: 10.1111/j.1748-1716.1962.tb02354.x. [DOI] [PubMed] [Google Scholar]
  26. YAMAMOTO T. Electron microscope investigation on the relationship between the smooth muscle cell of the Proc. vermiformis and the autonomic peripheral nerves. Acta Neuroveg (Wien) 1960;21:406–425. doi: 10.1007/BF01228271. [DOI] [PubMed] [Google Scholar]

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