Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1972 Jan;220(1):211–227. doi: 10.1113/jphysiol.1972.sp009702

Adrenergic re-innervation of smooth muscle of nictitating membrane by preganglionic sympathetic fibres

B Ceccarelli, F Clementi, P Mantegazza
PMCID: PMC1331697  PMID: 4333827

Abstract

1. The preganglionic and post-ganglionic trunks of the cervical sympathetic nerve were joined in an end-to-end anastomosis after excision of the superior cervical ganglion in the cat.

2. Seventy-five days after the anastomosis the diameter of the pupil was nearly normal and there was almost complete recovery of the prolapsed palpebra and of the nictitating membrane. The contraction of the nictitating membrane, induced by electrical stimulation, caudally to the point of anastomosis, showed that the smooth muscle of the nictitating membrane had been re-innervated.

3. Neither hexamethonium nor nicotine had any marked effect on the contraction of the nictitating membrane. Severing the regenerated nerve trunk produced a degeneration contraction. These results are strong evidence that the denervated membranes were re-innervated by true cholinergic preganglionic fibres.

4. Our pharmacological studies indicated that in the re-innervated preparations neuromuscular transmission was adrenergic in the sense that it was blocked by phentolamine and not by atropine. These results were confirmed by the histochemical-fluorescence studies which showed that the endings of the regenerated axons contained high concentrations of catecholamines.

5. Electron microscopy showed that the regenerated terminals contained none of the small dense-core vesicles, considered to be typical of adrenergic nerve endings, but contained clear synaptic vesicles and an unusually great number of large granular vesicles.

6. Our results suggest that the denervated nictitating membranes were re-innervated by cholinergic presynaptic sympathetic fibres that had been modified so that they could release catecholamines in addition to, or instead of, acetylcholine.

Full text

PDF
211

Images in this article

226-3Figs. 7-9
on p.226-3
226-1Figs. 1-3
on p.226-1
226-2Figs. 4-6
on p.226-2

Selected References

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

  1. BERSELLI L., ROSSI G. Recherches sur la régénération des fibres préganglionnaires du sympathique. Acta Anat (Basel) 1953;19(2):133–148. [PubMed] [Google Scholar]
  2. BURN J. H., RAND M. J. Sympathetic postganglionic cholinergic fibres. Br J Pharmacol Chemother. 1960 Mar;15:56–66. doi: 10.1111/j.1476-5381.1960.tb01210.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BURN J. H., TRENDELENBURG U. The hypersensitivity of the denervated nictitating membrane to various substances. Br J Pharmacol Chemother. 1954 Jun;9(2):202–209. doi: 10.1111/j.1476-5381.1954.tb00842.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BUTSON A. R. C. Regeneration of the cervical sympathetic. Br J Surg. 1950 Oct;38(150):223–239. doi: 10.1002/bjs.18003815011. [DOI] [PubMed] [Google Scholar]
  5. Bisby M. A., Fillenz M. The storage of endogenous noradrenaline in sympathetic nerve terminals. J Physiol. 1971 May;215(1):163–179. doi: 10.1113/jphysiol.1971.sp009463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. CERVONI P., WEST T. C., FINK L. D. Autonomic postganglionic innervation of the nictitating membrane of the cat. J Pharmacol Exp Ther. 1956 Jan;116(1):90–97. [PubMed] [Google Scholar]
  7. Ceccarelli B., Clementi F., Mantegazza P. Synaptic transmission in the superior cervical ganglion of the cat after reinnervation by vagus fibres. J Physiol. 1971 Jul;216(1):87–98. doi: 10.1113/jphysiol.1971.sp009510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ceccarelli B., Pensa P. Acrolein fixation of the central nervous system in the rat. Sperimentale. 1968 May-Jun;118(3):197–217. [PubMed] [Google Scholar]
  9. Clementi F., Mantegazza P., Botturi M. A pharmacologic and morphologic study on the nature of the dense-core granules present in the presynaptic endings of sympathetic ganglia. Int J Neuropharmacol. 1966 Jul;5(4):281–285. doi: 10.1016/0028-3908(66)90035-9. [DOI] [PubMed] [Google Scholar]
  10. Clementi F. Modifications ultrastructurelles provoquées par quelques médicaments sur les terminaisons nerveuses adrénergiques et sur la médullaire surrénale. Experientia. 1965 Mar 15;21(3):171–176. doi: 10.1007/BF02142003. [DOI] [PubMed] [Google Scholar]
  11. DOUGLAS W. W., RITCHIE J. M. The conduction of impulses through the superior cervical and accessory cervical ganglia of the rabbit. J Physiol. 1956 Jul 27;133(1):220–231. doi: 10.1113/jphysiol.1956.sp005580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Douglas W. W., Lywood D. W., Straub R. W. On the excitant effect of acetylcholine on structures in the preganglionic trunk of the cervical sympathetic: with a note on the anatomical complexities of the region. J Physiol. 1960 Sep;153(2):250–264. doi: 10.1113/jphysiol.1960.sp006533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. EVANS D. H., EVANS E. M. THE MEMBRANE RELATIONSHIPS OF SMOOTH MUSCLES: AN ELECTRON MICROSCOPE STUDY. J Anat. 1964 Jan;98:37–46. [PMC free article] [PubMed] [Google Scholar]
  14. Esterhuizen A. C., Graham J. D., Lever J. D., Spriggs T. L. Catecholamine and acetylcholinesterase distribution in relation to noradrenaline release. An enzyme histochemical and autoradiographic study on the innervation of the cat nictitating muscle. Br J Pharmacol Chemother. 1968 Jan;32(1):46–56. doi: 10.1111/j.1476-5381.1968.tb00428.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Esterhuizen A. C., Graham J. D., Lever J. D., Spriggs T. L. The innervation of the smooth muscle of the nictitating membrane of the cat. J Physiol. 1967 Sep;192(2):41P–42P. [PubMed] [Google Scholar]
  16. GARDINER J. E., HELLMANN K., THOMPSON J. W. The nature of the innervation of the smooth muscle, Harderian gland and blood vessels of the cat's nictitating membrane. J Physiol. 1962 Oct;163:436–456. doi: 10.1113/jphysiol.1962.sp006988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Geffen L. B., Ostberg A. Distribution of granular vesicles in normal and constricted sympathetic neurones. J Physiol. 1969 Oct;204(3):583–592. doi: 10.1113/jphysiol.1969.sp008933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Giacobini E. Biochemistry of synaptic plasticity studied in single neurons. Adv Cytopharmacol. 1971 May;1:427–431. [PubMed] [Google Scholar]
  19. JACOBOWITZ D., KOELLE G. B. HISTOCHEMICAL CORRELATIONS OF ACETYLCHOLINESTERASE AND CATECHOLAMINES IN POSTGANGLIONIC AUTONOMIC NERVES OF THE CAT, RABBIT, AND GUINEA PIG. J Pharmacol Exp Ther. 1965 May;148:225–237. [PubMed] [Google Scholar]
  20. Jacobowitz D., Woodward J. K. Adrenergic neurons in the cat superior cervical ganglion and cervical sympathetic nerve trunk. A histochemical study. J Pharmacol Exp Ther. 1968 Aug;162(2):213–226. [PubMed] [Google Scholar]
  21. Jaim-Etcheverry G., Zieher L. M. Ultrastructural aspects of neurotransmitter storage in adrenergic nerves. Adv Cytopharmacol. 1971 May;1:343–361. [PubMed] [Google Scholar]
  22. Langer S. Z. The degeneration contraction of the nictitating membrane in the unanesthetized cat. J Pharmacol Exp Ther. 1966 Jan;151(1):66–72. [PubMed] [Google Scholar]
  23. Langer S. Z., Trendelenburg U. The onset of denervation supersensitivity. J Pharmacol Exp Ther. 1966 Jan;151(1):73–86. [PubMed] [Google Scholar]
  24. 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]
  25. Langley J. N. Notes on the regeneration of the pre-ganglionic fibres in the sympathetic system. J Physiol. 1900 Aug 29;25(5):417–426. doi: 10.1113/jphysiol.1900.sp000805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pellegrino de Iraldi A., De Robertis E. The neurotubular system of the axon and the origin of granulated and non-granulated vesicles in regenerating nerves. Z Zellforsch Mikrosk Anat. 1968;87(3):330–344. doi: 10.1007/BF00333684. [DOI] [PubMed] [Google Scholar]
  27. Pye-Smith P. H. Observations upon the Persistent Effects of Division of the Cervical Sympathetic: I. J Physiol. 1887 Feb;8(1):25–49. doi: 10.1113/jphysiol.1887.sp000241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Spriggs T. L., Lever J. D., Rees P. M., Graham J. D. Controlled formaldehyde-catecholamine condensation in cryostat sections to show adrenergic nerves by fluorescence. Stain Technol. 1966 Nov;41(6):323–327. doi: 10.3109/10520296609116333. [DOI] [PubMed] [Google Scholar]
  29. THOMPSON J. W. Studies on the responses of the isolated nictitating membrane of the cat. J Physiol. 1958 Apr 3;141(1):46–72. doi: 10.1113/jphysiol.1958.sp005954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. THOMPSON J. W. The nerve supply to the nictitating membrane of the cat. J Anat. 1961 Jul;95:371–385. [PMC free article] [PubMed] [Google Scholar]
  31. Tranzer J. P., Thoenen H. Various types of amine-storing vesicles in peripheral adrenergic nerve terminals. Experientia. 1968 May 15;24(5):484–486. doi: 10.1007/BF02144407. [DOI] [PubMed] [Google Scholar]
  32. VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. VERA C. L., VIAL J. D., LUCO J. V. Reinnervation of nictitating membrane of cat by cholinergic fibers. J Neurophysiol. 1957 Jul;20(4):365–373. doi: 10.1152/jn.1957.20.4.365. [DOI] [PubMed] [Google Scholar]
  34. Van Orden L. S., 3rd, Bensch K. G., Langer S. Z., Trendelenburg U. Histochemical and fine structural aspects of the onset of denervation supersensitivity in the nictitating membrane of the spinal cat. J Pharmacol Exp Ther. 1967 Aug;157(2):274–283. [PubMed] [Google Scholar]
  35. Van Orden L. S., 3rd, Bloom F. E., Barnett R. J., Giarman N. J. Histochemical and functional relationships of catecholamines in adrenergic nerve endings. I. Participation of granular vesicles. J Pharmacol Exp Ther. 1966 Nov;154(2):185–199. [PubMed] [Google Scholar]
  36. 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]
  37. Weiner N., Langer S. Z., Trendelenburg U. Demonstration by the histochemical fluorescence method of the prolonged disappearance of catecholamines from the denervated nictitating membrane of the cat. J Pharmacol Exp Ther. 1967 Aug;157(2):284–289. [PubMed] [Google Scholar]

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

RESOURCES