Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1966 Aug;185(3):520–535. doi: 10.1113/jphysiol.1966.sp008000

An analysis of the transmission of excitation from autonomic nerves to smooth muscle

M R Bennett, N C R Merrillees
PMCID: PMC1395836  PMID: 5950554

Abstract

1. An analysis has been made of the transmission of excitation from the hypogastric nerve to the smooth muscle cells of the guinea-pig vas deferens.

2. Depolarization of single muscle cells with current pulses from an intracellular electrode gave local depolarizations of the cell membrane which were not propagated. The total membrane resistance after 100 msec of depolarization was 15 MΩ for depolarizations between 10 and 40 mV.

3. Depolarization of some cell membranes with a current pulse during the excitatory junction potential (E.J.P.) decreased the amplitude of the E.J.P. from about 10 mV at 20 mV depolarization, to nearly zero at 60 mV depolarization. In some cells the E.J.P. was unchanged during depolarizations of 50 mV.

4. The action of transmitter on the smooth muscle cell membrane continued for the duration of the E.J.P. Action potentials which occurred at various times during the E.J.P. failed to remove the remaining phases of the E.J.P.

5. It was shown that the slow time course of the E.J.P. could not be due to the instantaneous and simultaneous release of transmitter from a number of relatively distant sources.

6. It was shown that each smooth muscle cell was innervated by several axons. The serial sections examined with the electron microscope showed that a smooth muscle had either a single axon terminating within 200 Å of the muscle or no axons terminating on it at all. Therefore transmitter must be released along the length of the axons as well as at the terminations of the axons.

Full text

PDF
520

Images in this article

534-1Fig. 1
on p.534-1
534-1Fig. 2
on p.534-1
534-2Fig. 1
on p.534-2
534-2Fig. 2
on p.534-2

Selected References

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

  1. ARAKI T., OTANI T. Response of single motoneurons to direct stimulation in toad's spinal cord. J Neurophysiol. 1955 Sep;18(5):472–485. doi: 10.1152/jn.1955.18.5.472. [DOI] [PubMed] [Google Scholar]
  2. BULBRING E., KURIYAMA H. Effects of changes in ionic environment on the action of acetylcholine and adrenaline on the smooth muscle cells of guinea-pig taenia coli. J Physiol. 1963 Apr;166:59–74. doi: 10.1113/jphysiol.1963.sp007090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BURKE W., GINSBORG B. L. The action of the neuromuscular transmitter on the slow fibre membrane. J Physiol. 1956 Jun 28;132(3):599–610. doi: 10.1113/jphysiol.1956.sp005552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BURNSTOCK G., HOLMAN M. E., KURIYAMA H. FACILITATION OF TRANSMISSION FROM AUTONOMIC NERVE TO SMOOTH MUSCLE OF GUINEA-PIG VAS DEFERENS. J Physiol. 1964 Jul;172:31–49. doi: 10.1113/jphysiol.1964.sp007401. [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. BURNSTOCK G., PROSSER C. L. Conduction in smooth muscles: comparative electrical properties. Am J Physiol. 1960 Sep;199:553–559. doi: 10.1152/ajplegacy.1960.199.3.553. [DOI] [PubMed] [Google Scholar]
  7. BURNSTOCK G. The action of adrenaline on excitability and membrane potential in the taenia coli of the guinea-pig and the effect of DNP on this action and on the action of acetylcholine. J Physiol. 1958 Aug 29;143(1):183–194. doi: 10.1113/jphysiol.1958.sp006052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bennett M. R., Burnstock G., Holman M. E. Transmission from perivascular inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J Physiol. 1966 Feb;182(3):527–540. doi: 10.1113/jphysiol.1966.sp007835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bennett M. R., Burnstock G., Holman M. Transmission from intramural inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J Physiol. 1966 Feb;182(3):541–558. doi: 10.1113/jphysiol.1966.sp007836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. COOMBS J. S., ECCLES J. C., FATT P. Excitatory synaptic action in motoneurones. J Physiol. 1955 Nov 28;130(2):374–395. doi: 10.1113/jphysiol.1955.sp005413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DEL CASTILLO J., KATZ B. On the localization of acetylcholine receptors. J Physiol. 1955 Apr 28;128(1):157–181. doi: 10.1113/jphysiol.1955.sp005297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. ECCLES J. C., JAEGER J. C. The relationship between the mode of operation and the dimensions of the junctional regions at synapses and motor end-organs. Proc R Soc Lond B Biol Sci. 1958 Jan 1;148(930):38–56. doi: 10.1098/rspb.1958.0003. [DOI] [PubMed] [Google Scholar]
  13. ECCLES J. C. Membrane time constants of cat motoneurons and time courses of synptic action. Exp Neurol. 1961 Jul;4:1–22. doi: 10.1016/0014-4886(61)90074-7. [DOI] [PubMed] [Google Scholar]
  14. FATT P., KATZ B. An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol. 1951 Nov 28;115(3):320–370. doi: 10.1113/jphysiol.1951.sp004675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GILLESPIE J. S. Spontaneous mechanical and electrical activity of stretched and unstretched intestinal smooth muscle cells and their response to sympathetic-nerve stimulation. J Physiol. 1962 Jun;162:54–75. doi: 10.1113/jphysiol.1962.sp006914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. GILLESPIE J. S. The electrical and mechanical responses of intestinal smooth muscle cells to stimulation of their extrinsic parasympathetic nerves. J Physiol. 1962 Jun;162:76–92. doi: 10.1113/jphysiol.1962.sp006915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HUKOVIC S. Responses of the isolated sympathetic nerveductus deferens preparation of the guinea-pig. Br J Pharmacol Chemother. 1961 Apr;16:188–194. doi: 10.1111/j.1476-5381.1961.tb00312.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. KATZ B., MILEDI R. THE MEASUREMENT OF SYNAPTIC DELAY, AND THE TIME COURSE OF ACETYLCHOLINE RELEASE AT THE NEUROMUSCULAR JUNCTION. Proc R Soc Lond B Biol Sci. 1965 Feb 16;161:483–495. doi: 10.1098/rspb.1965.0016. [DOI] [PubMed] [Google Scholar]
  19. KOPIN I. J. STORAGE AND METABOLISM OF CATECHOLAMINES: THE ROLE OF MONOAMINE OXIDASE. Pharmacol Rev. 1964 Jun;16:179–191. [PubMed] [Google Scholar]
  20. KURIYAMA H. ELECTROPHYSIOLOGICAL OBSERVATIONS ON THE MOTOR INNERVATION OF THE SMOOTH MUSCLE CELLS IN THE GUINEA-PIG VAS DEFERENS. J Physiol. 1963 Nov;169:213–228. doi: 10.1113/jphysiol.1963.sp007251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. KURIYAMA H., TOMITA T. THE RESPONSES OF SINGLE SMOOTH MUSCLE CELLS OF GUINEA-PIG TAENIA COLI TO INTRACELLULARLY APPLIED CURRENTS, AND THEIR EFFECT ON THE SPONTANEOUS ELECTRICAL ACTIVITY. J Physiol. 1965 May;178:270–289. doi: 10.1113/jphysiol.1965.sp007627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. NAGAI T., PROSSER C. L. Patterns of conduction in smooth muscle. Am J Physiol. 1963 May;204:910–914. doi: 10.1152/ajplegacy.1963.204.5.910. [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. SPEDEN R. N. ELECTRICAL ACTIVITY OF SINGLE SMOOTH MUSCLE CELLS OF THE MESENTERIC ARTERY PRODUCED BY SPLANCHNIC NERVE STIMULATION IN THE GUINEA PIG. Nature. 1964 Apr 11;202:193–194. doi: 10.1038/202193a0. [DOI] [PubMed] [Google Scholar]
  26. TAKEUCHI A., TAKEUCHI N. Active phase of frog's end-plate potential. J Neurophysiol. 1959 Jul;22(4):395–411. doi: 10.1152/jn.1959.22.4.395. [DOI] [PubMed] [Google Scholar]
  27. TAKEUCHI N. Some properties of conductance changes at the end-plate membrane during the action of acetylcholine. J Physiol. 1963 Jun;167:128–140. doi: 10.1113/jphysiol.1963.sp007136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. URSILLO R. C. Electrical activity of the isolated nerve-urinary bladder strip preparation of the rabbit. Am J Physiol. 1961 Sep;201:408–412. doi: 10.1152/ajplegacy.1961.201.3.408. [DOI] [PubMed] [Google Scholar]

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

RESOURCES