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. 1966 Jan 1;28(1):37–49. doi: 10.1083/jcb.28.1.37

ULTRASTRUCTURAL INTERRELATIONSHIPS OF NERVE PROCESSES AND SMOOTH MUSCLE CELLS IN THREE DIMENSIONS

J C Thaemert 1
PMCID: PMC2106893  PMID: 5322460

Abstract

The muscularis externa of the intestinal wall of frogs was fixed in osmium tetroxide, embedded in Vestopal-W, serially sectioned for electron microscopy, and stained with uranyl acetate. A method to obtain individually mounted and properly positioned serial sections is described. The three-dimensional techniques used during the course of this investigation demonstrate that it is possible to examine carefully relatively large areas of tissue on individual serial sections with the electron microscope and subsequently to construct montages of electron micrographs of pertinent areas from each section. Several carefully rendered interrelationships of nerve processes and smooth muscle cells in three dimensions are exhibited and described. Recent studies of other neuro-effector relationships are discussed in relation to the present status of the nature and organization of the autonomic nervous system in visceral organs.

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Selected References

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  1. AKIO Y. (ELECTRON MICROSCOPIC STUDIES ON THE AUTONOMIC NEURO-MUSCULAR JUNCTION IN THE TENIA COLI OF THE GUINEA PIG.) Kaibogaku Zasshi. 1964 Feb 1;39:22–38. [PubMed] [Google Scholar]
  2. BEAMS H. W., EVANS T. C. Electron micrographs of motor end-plates. Proc Soc Exp Biol Med. 1953 Feb;82(2):344–346. doi: 10.3181/00379727-82-20112. [DOI] [PubMed] [Google Scholar]
  3. BENCOSME S. A. Studies on the terminal autonomic nervous system with special reference to the pancreatic islets. Lab Invest. 1959 May-Jun;8(3):629–646. [PubMed] [Google Scholar]
  4. BULBRING E., LIN R. C., SCHOFIELD G. An investigation of the peristaltic reflex in relation to anatomical observations. Q J Exp Physiol Cogn Med Sci. 1958 Jan;43(1):26–37. doi: 10.1113/expphysiol.1958.sp001305. [DOI] [PubMed] [Google Scholar]
  5. BURNSTOCK G., HOLMAN M. E., PROSSER C. L. Electrophysiology of smooth muscle. Physiol Rev. 1963 Jul;43:482–527. doi: 10.1152/physrev.1963.43.3.482. [DOI] [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. COUTEAUX R., LAURENT P. Etude au microscope électronique du coeur de l'anguille: observations sur la structure du tissu musculaire de l'oreillette et son innervation. C R Hebd Seances Acad Sci. 1957 Dec 4;245(23):2097–2100. [PubMed] [Google Scholar]
  8. COUTEAUX R. Morphological and cytochemical observations on the post-synaptic membrane at motor end-plates and ganglionic synapses. Exp Cell Res. 1958;14(Suppl 5):294–322. [PubMed] [Google Scholar]
  9. DE HARVEN E., COERS C. Electron microscope study of the human neuromuscular junction. J Biophys Biochem Cytol. 1959 Aug;6(1):7–10. doi: 10.1083/jcb.6.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. GANSLER H. [Phase contrast and electron microscopic studies on the innervation of smooth muscles]. Acta Neuroveg (Wien) 1961;22:192–211. doi: 10.1007/BF01226812. [DOI] [PubMed] [Google Scholar]
  12. GRIMLEY P. M., EDWARDS G. A. The ultrastructure of cardiac desnosomes in the toad and their relationship to the intercalated disc. J Biophys Biochem Cytol. 1960 Oct;8:305–318. doi: 10.1083/jcb.8.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HAMBERGER B., NORBERG K. A. ADRENERGIC SYNAPTIC TERMINALS AND NERVE CELLS IN BLADDER GANGLIA OF THE CAT. Int J Neuropharmacol. 1965 Feb;4:41–45. doi: 10.1016/0028-3908(65)90045-6. [DOI] [PubMed] [Google Scholar]
  14. ISHIKAWA T. Fine structure of the human cillary muscle. Invest Ophthalmol. 1962 Oct;1:587–608. [PubMed] [Google Scholar]
  15. KAPPERS J. A. A SURVEY OF DIFFERENT OPINIONS RELATING TO THE STRUCTURE OF THE PERIPHERAL AUTONOMIC NERVOUS SYSTEM. Acta Neuroveg (Wien) 1964 Jan 27;26:145–171. doi: 10.1007/BF01234589. [DOI] [PubMed] [Google Scholar]
  16. KISCH B. Electronmicroscopy of the frog's heart. Exp Med Surg. 1961;19:104–142. [PubMed] [Google Scholar]
  17. KOSTERLITZ H. W., LEES G. M. PHARMACOLOGICAL ANALYSIS OF INTRINSIC INTESTINAL REFLEXES. Pharmacol Rev. 1964 Sep;16:301–339. [PubMed] [Google Scholar]
  18. LATIES A., JACOBOWITZ D. A HISTOCHEMICAL STUDY OF THE ADRENERGIC AND CHOLINERGIC INNERVATION OF THE ANTERIOR SEGMENT OF THE RABBIT EYE. Invest Ophthalmol. 1964 Dec;3:592–600. [PubMed] [Google Scholar]
  19. LEVER J. D., ESTERHUIZEN A. C. Fine structure of the arteriolar nerves in the guinea pig pancreas. Nature. 1961 Nov 11;192:566–567. doi: 10.1038/192566a0. [DOI] [PubMed] [Google Scholar]
  20. LEVER J. D., GRAHAM J. D., IRVINE G., CHICK W. J. THE VESICULATED AXONS IN RELATION TO ARTERIOLAR SMOOTH MUSCLE IN THE PANCREAS. A FINE STUCTURAL AND QUANTITATIVE STUDY. J Anat. 1965 Apr;99:299–313. [PMC free article] [PubMed] [Google Scholar]
  21. MERRILLEES N. C., BURNSTOCK G., HOLMAN M. E. CORRELATION OF FINE STRUCTURE AND PHYSIOLOGY OF THE INNERVATION OF SMOOTH MUSCLE IN THE GUINEA PIG VAS DEFERENS. J Cell Biol. 1963 Dec;19:529–550. doi: 10.1083/jcb.19.3.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MICHAELSON I. A., RICHARDSON K. C., SNYDER S. N., TITUS E. O. THE SEPARATION OF CATECHOLAMINE STORAGE VESICLES FROM RAT HEART. Life Sci. 1964 Sep;3:971–978. doi: 10.1016/0024-3205(64)90107-9. [DOI] [PubMed] [Google Scholar]
  23. Mitchell H. C., Thaemert J. C. Three Dimensions in Fine Structure. Science. 1965 Jun 11;148(3676):1480–1482. doi: 10.1126/science.148.3676.1480. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. NAPOLITANO L. M., WILLMAN V. L., HANLON C. R., COOPER T. INTRINSIC INNERVATION OF THE HEART. Am J Physiol. 1965 Mar;208:455–458. doi: 10.1152/ajplegacy.1965.208.3.455. [DOI] [PubMed] [Google Scholar]
  26. ORFANOS C. [On micromorphology of the neuromuscular junction of the afibrillar-tonic skeletal muscle fiber in the frog (Rana temporaria L.)]. Z Zellforsch Mikrosk Anat. 1962;56:387–403. [PubMed] [Google Scholar]
  27. POTTER L. T., AXELROD J. SUBCELLULAR LOCALIZATION OF CATECHOLAMINES IN TISSUES OF THE RAT. J Pharmacol Exp Ther. 1963 Dec;142:291–298. [PubMed] [Google Scholar]
  28. PRICE Z., EIDE B., PRINTZMETAL M., CARPENTER C. Ultrastructure of the dog cardiac muscle cell. Circ Res. 1959 Nov;7:858–865. doi: 10.1161/01.res.7.6.858. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. REGER J. F. Electron microscopy of the motor end-plate in rat intercostal muscle. Anat Rec. 1955 May;122(1):1–15. doi: 10.1002/ar.1091220102. [DOI] [PubMed] [Google Scholar]
  31. REGER J. F. Studies on the fine structure of normal and denervated neuromuscular junctions from mouse gastrocnemius. J Ultrastruct Res. 1959 Mar;2(3):269–282. doi: 10.1016/s0022-5320(59)80001-0. [DOI] [PubMed] [Google Scholar]
  32. REGER J. F. The ultrastructure of normal and denervated neuromuscular synapses in mouse gastrocnemius muscle. Exp Cell Res. 1957 Jun;12(3):662–665. doi: 10.1016/0014-4827(57)90184-2. [DOI] [PubMed] [Google Scholar]
  33. REVEL J. P. The sarcoplasmic reticulum of the bat cricothroid muscle. J Cell Biol. 1962 Mar;12:571–588. doi: 10.1083/jcb.12.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. RICHARDSON K. C. Studies on the structure of autonomic nerves in the small intestine, correlating the silver-impregnated image in light microscopy with the permanganate-fixed ultrastructure in electronmicrscopy. J Anat. 1960 Oct;94:457–472. [PMC free article] [PubMed] [Google Scholar]
  36. RICHARDSON K. C. THE FINE STRUCTURE OF THE ALBINO RABBIT IRIS WITH SPECIAL REFERENCE TO THE IDENTIFICATION OF ADRENERGIC AND CHOLINERGIC NERVES AND NERVE ENDINGS IN ITS INTRINSIC MUSCLES. Am J Anat. 1964 Mar;114:173–205. doi: 10.1002/aja.1001140202. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. SCOTT B. L., PEASE D. C. Electron microscopy of the salivary and lacrimal glands of the rat. Am J Anat. 1959 Jan;104:115–161. doi: 10.1002/aja.1001040106. [DOI] [PubMed] [Google Scholar]
  39. SJOSTRAND F. S. Ultrastructure of retinal rod synapses of the guinea pig eye as revealed by three-dimensional reconstructions from serial sections. J Ultrastruct Res. 1958 Nov;2(1):122–170. doi: 10.1016/s0022-5320(58)90050-9. [DOI] [PubMed] [Google Scholar]
  40. SMITH C. A., SJOSTRAND F. S. Structure of the nerve endings on the external hair cells of the guinea pig cochlea as studied by serial sections. J Ultrastruct Res. 1961 Dec;5:523–556. doi: 10.1016/s0022-5320(61)80025-7. [DOI] [PubMed] [Google Scholar]
  41. SPERELAKIS N., TARR M. WEAK ELECTRONIC INTERACTION BETWEEN NEIGHBORING VISCERAL SMOOTH MUSCLE CELLS. Am J Physiol. 1965 Apr;208:737–747. doi: 10.1152/ajplegacy.1965.208.4.737. [DOI] [PubMed] [Google Scholar]
  42. TAXI J. ETUDE, AU MICROSCOPE 'ELECTRONIQUE, DE L'INNERVATION DU MUSCLE LISSE INTESTINAL, COMPAR'EE 'A CELLE DE QUELQUES AUTRES MUSCLES LISSES DE MAMMIF'ERES. Arch Biol (Liege) 1964;75:301–328. [PubMed] [Google Scholar]
  43. TAXI J. [On the innervation of the smooth muscle fibers of the mouse intestine]. C R Hebd Seances Acad Sci. 1961 Jan 9;252:331–333. [PubMed] [Google Scholar]
  44. THAEMERT J. C. The ultrastructure and disposition of vesiculated nerve processes in smooth muscle. J Cell Biol. 1963 Feb;16:361–377. doi: 10.1083/jcb.16.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. TRAUTWEIN W., UCHIZONO K. ELECTRON MICROSCOPIC AND ELECTROPHYSIOLOGIC STUDY OF THE PACEMAKER IN THE SINO-ATRIAL NODE OF THE RABBIT HEART. Z Zellforsch Mikrosk Anat. 1963 Oct 8;61:96–109. doi: 10.1007/BF00341523. [DOI] [PubMed] [Google Scholar]
  46. VAN HARN G. L. Responses of muscles of cat small intestine to autonomic nerve stimulation. Am J Physiol. 1963 Feb;204:352–358. doi: 10.1152/ajplegacy.1963.204.2.352. [DOI] [PubMed] [Google Scholar]
  47. VIRAGH S., PORTE A. [Intracardiac nervous elements and innervation of the myocardium. Electron microscopic study of the rat heart]. Z Zellforsch Mikrosk Anat. 1961;55:282–296. [PubMed] [Google Scholar]
  48. WESTRUM L. E., BLACKSTAD T. W. An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA 1) with particular emphasis on synaptology. J Comp Neurol. 1962 Dec;119:281–309. doi: 10.1002/cne.901190303. [DOI] [PubMed] [Google Scholar]
  49. WOLFE D. E., POTTER L. T., RICHARDSON K. C., AXELROD J. Localizing tritiated norepinephrine in sympathetic axons by electron microscopic autoradiography. Science. 1962 Oct 19;138(3538):440–442. doi: 10.1126/science.138.3538.440. [DOI] [PubMed] [Google Scholar]
  50. YAMADA E. SOME OBSERVATIONS ON THE NERVE TERMINAL ON THE LIVER PARENCHYMAL CELL OF THE MOUSE AS REVEALED BY ELECTRON MICROSCOPY. Okajimas Folia Anat Jpn. 1965 Jan;40:663–677. doi: 10.2535/ofaj1936.40.4-6_663. [DOI] [PubMed] [Google Scholar]
  51. YATES R. D. A LIGHT AND ELECTRON MICROSCOPIC STUDY CORRELATING THE CHROMAFFIN REACTION AND GRANULE ULTRASTRUCTURE IN THE ADRENAL MEDULLA OF THE SYRIAN HAMSTER. Anat Rec. 1964 Jun;149:237–249. doi: 10.1002/ar.1091490207. [DOI] [PubMed] [Google Scholar]

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