Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1970 Jul 1;46(1):27–41. doi: 10.1083/jcb.46.1.27

THE ULTRASTRUCTURE OF THE NEUROMUSCULAR JUNCTIONS OF MAMMALIAN RED, WHITE, AND INTERMEDIATE SKELETAL MUSCLE FIBERS

Helen A Padykula 1, Geraldine F Gauthier 1
PMCID: PMC2108070  PMID: 5459010

Abstract

Distinct ultrastructural differences exist at the neuromuscular junctions of red, white, and intermediate fibers of a mammalian twitch skeletal muscle (albino rat diaphragm). The primary criteria for recognizing the three fiber types are differences in fiber diameter, mitochondrial content, and width of the Z line. In the red fiber the neuromuscular relationship presents the least sarcoplasmic and axoplasmic surface at each contact. Points of contact are relatively discrete and separate, and axonal terminals are small and elliptical. The junctional folds are relatively shallow, sparse, and irregular in arrangement. Axoplasmic vesicles are moderate in number, and sarcoplasmic vesicles are sparse. In the white fiber long, flat axonal terminals present considerable axoplasmic surface. Vast sarcoplasmic surface area is created by long, branching, closely spaced junctional folds that may merge with folds at adjacent contacts to occupy a more continuous and widespread area. Axoplasmic and sarcoplasmic vesicles are numerous. Both axoplasmic and sarcoplasmic mitochondria of the white fiber usually contain intramitochondrial granules. The intermediate fiber has large axonal terminals that are associated with the most widely spaced and deepest junctional folds. In all three fiber types, the junctional sarcoplasm is rich in free ribosomes, cisternae of granular endoplasmic reticulum, and randomly distributed microtubules.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

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

  1. ANZENBACHER H., ZENKER W. UBER DIE GROESSENBEZIEHUNG DER MUSKELFASERN ZU IHREN MOTORISCHEN ENDPLATTEN UND NERVEN. Z Zellforsch Mikrosk Anat. 1963 Sep 18;60:860–871. [PubMed] [Google Scholar]
  2. BARRNETT R. J. The fine structural localization of acetylcholinesterase at the myoneural junction. J Cell Biol. 1962 Feb;12:247–262. doi: 10.1083/jcb.12.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BULLER A. J., ECCLES J. C., ECCLES R. M. Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol. 1960 Feb;150:417–439. doi: 10.1113/jphysiol.1960.sp006395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burke R. E. Motor unit types of cat triceps surae muscle. J Physiol. 1967 Nov;193(1):141–160. doi: 10.1113/jphysiol.1967.sp008348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. COLE W. V. Structural variations of nerve endings in the striated muscles of the rat. J Comp Neurol. 1957 Dec;108(3):445–463. doi: 10.1002/cne.901080306. [DOI] [PubMed] [Google Scholar]
  6. Csillik B., Knyihár E. On the effect of motor nerve degeneration on the fine-structural localization of esterases in the mammalian motor end-plate. J Cell Sci. 1968 Dec;3(4):529–538. doi: 10.1242/jcs.3.4.529. [DOI] [PubMed] [Google Scholar]
  7. Davis R., Koelle G. B. Electron microscopic localization of acetylcholinesterase and nonspecific cholinesterase at the neuromuscular junction by the gold-thiocholine and gold-thiolacetic acid methods. J Cell Biol. 1967 Jul;34(1):157–171. doi: 10.1083/jcb.34.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Durell J., Garland J. T., Friedel R. O. Acetylcholine action: biochemical aspects. Science. 1969 Aug 29;165(3896):862–866. doi: 10.1126/science.165.3896.862. [DOI] [PubMed] [Google Scholar]
  9. ECCLES J. C., ECCLES R. M., LUNDBERG A. The action potentials of the alpha motoneurones supplying fast and slow muscles. J Physiol. 1958 Jul 14;142(2):275–291. doi: 10.1113/jphysiol.1958.sp006015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Edström L., Kugelberg E. Histochemical composition, distribution of fibres and fatiguability of single motor units. Anterior tibial muscle of the rat. J Neurol Neurosurg Psychiatry. 1968 Oct;31(5):424–433. doi: 10.1136/jnnp.31.5.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fernand V. S., Hess A. The occurrence, structure and innervation of slow and twitch muscle fibres in the tensor tympani and stapedius of the cat. J Physiol. 1969 Feb;200(2):547–554. doi: 10.1113/jphysiol.1969.sp008707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gauthier G. F. On the relationship of ultrastructural and cytochemical features of color in mammalian skeletal muscle. Z Zellforsch Mikrosk Anat. 1969;95(3):462–482. doi: 10.1007/BF00995217. [DOI] [PubMed] [Google Scholar]
  13. Gauthier G. F., Padykula H. A. Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J Cell Biol. 1966 Feb;28(2):333–354. doi: 10.1083/jcb.28.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gruber H. Die Grössenbeziehung von Muskelfaservolumen und Fläche der motorischen Endplatte bei verschiedenen Skeletmuskeln der Ratte. Acta Anat (Basel) 1966;64(4):628–633. [PubMed] [Google Scholar]
  15. HENNEMAN E., SOMJEN G., CARPENTER D. O. FUNCTIONAL SIGNIFICANCE OF CELL SIZE IN SPINAL MOTONEURONS. J Neurophysiol. 1965 May;28:560–580. doi: 10.1152/jn.1965.28.3.560. [DOI] [PubMed] [Google Scholar]
  16. KARNOVSKY M. J. Simple methods for "staining with lead" at high pH in electron microscopy. J Biophys Biochem Cytol. 1961 Dec;11:729–732. doi: 10.1083/jcb.11.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. KATZ B., THESLEFF S. On the factors which determine the amplitude of the miniature end-plate potential. J Physiol. 1957 Jul 11;137(2):267–278. doi: 10.1113/jphysiol.1957.sp005811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. KUFFLER S. W. The two skeletal nerve-muscle systems in frog. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol. 1953;220(1-2):116–135. doi: 10.1007/BF00246099. [DOI] [PubMed] [Google Scholar]
  19. Mayr R., Stockinger L., Zenker W. Elektronenmikroskopische Untersuchungen an unterschiedlich innervierten Muskelfasern der äusseren Augenmuskulatur des Rhesusaffen. Z Zellforsch Mikrosk Anat. 1966;75(2):434–452. [PubMed] [Google Scholar]
  20. Miledi R., Slater C. R. Electrophysiology and electron-microscopy of rat neuromuscular junctions after nerve degeneration. Proc R Soc Lond B Biol Sci. 1968 Feb 27;169(1016):289–306. doi: 10.1098/rspb.1968.0012. [DOI] [PubMed] [Google Scholar]
  21. NACHMANSOHN D. Metabolism and function of the nerve cell. Harvey Lect. 1953;49:57–99. [PubMed] [Google Scholar]
  22. Nickel E., Vogel A., Waser P. G. Coated Vesicles in der Umgebung der neuro-muskulären Synapsen. Z Zellforsch Mikrosk Anat. 1967;78(2):261–266. [PubMed] [Google Scholar]
  23. Nickel E., Waser P. G. Elektronenmikroskopische Untersuchungen am Diaphragma der Maus nach einseitiger Phrenikotomie. I. Die degenerierende motorische Endplatte. Z Zellforsch Mikrosk Anat. 1968;88(2):278–296. [PubMed] [Google Scholar]
  24. PALADE G. E. A study of fixation for electron microscopy. J Exp Med. 1952 Mar;95(3):285–298. doi: 10.1084/jem.95.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. PEACHEY L. D. ELECTRON MICROSCOPIC OBSERVATIONS ON THE ACCUMULATION OF DIVALENT CATIONS IN INTRAMITOCHONDRIAL GRANULES. J Cell Biol. 1964 Jan;20:95–111. doi: 10.1083/jcb.20.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. PEACHEY L. D., HUXLEY A. F. Structural identification of twitch and slow striated muscle fibers of the frog. J Cell Biol. 1962 Apr;13:177–180. doi: 10.1083/jcb.13.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Page S. G. A comparison of the fine structures of frog slow and twitch muscle fibers. J Cell Biol. 1965 Aug;26(2):477–497. doi: 10.1083/jcb.26.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Page S. G. Fine structure of tortoise skeletal muscle. J Physiol. 1968 Aug;197(3):709–715. doi: 10.1113/jphysiol.1968.sp008583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. RITCHIE J. M. The relation between force and velocity of shortening in rat muscle. J Physiol. 1954 Mar 29;123(3):633–639. doi: 10.1113/jphysiol.1954.sp005075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. ROBERTSON J. D. The ultrastructure of a reptilian myoneural junction. J Biophys Biochem Cytol. 1956 Jul 25;2(4):381–394. doi: 10.1083/jcb.2.4.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Romanul F. C., Van der Meulen J. P. Slow and fast muscles after cross innervation. Enzymatic and physiological changes. Arch Neurol. 1967 Oct;17(4):387–402. doi: 10.1001/archneur.1967.00470280053006. [DOI] [PubMed] [Google Scholar]
  33. SABATINI D. D., BENSCH K., BARRNETT R. J. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. doi: 10.1083/jcb.17.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. STEIN J. M., PADYKULA H. A. Histochemical classification of individual skeletal muscle fibers of the rat. Am J Anat. 1962 Mar;110:103–123. doi: 10.1002/aja.1001100203. [DOI] [PubMed] [Google Scholar]
  35. Salpeter M. M. Electron microscope radioautography as a quantitative tool in enzyme cytochemistry. I. The distribution of acetylcholinesterase at motor end plates of a vertebrate twitch muscle. J Cell Biol. 1967 Feb;32(2):379–389. doi: 10.1083/jcb.32.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Salpeter M. M. Electron microscope radioautography as a quantitative tool in enzyme cytochemistry. II. The distribution of DFP-reactive sties at motor endplates of a vertebrate twitch muscle. J Cell Biol. 1969 Jul;42(1):122–134. doi: 10.1083/jcb.42.1.122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Teräväinen H. Electron microscopic and histochemical observations on different types of nerve endings in the extraocular muscles of the rat. Z Zellforsch Mikrosk Anat. 1968;90(3):372–388. doi: 10.1007/BF00341993. [DOI] [PubMed] [Google Scholar]
  38. Teräväinen H. Localization of acetylcholinesterase in the rat myoneural junction. Histochemie. 1969;17(2):162–169. doi: 10.1007/BF00277782. [DOI] [PubMed] [Google Scholar]
  39. Thomas R. S., Greenawalt J. W. Microincineration, electron microscopy, and electron diffraction of calcium phosphate-loaded mitochondria. J Cell Biol. 1968 Oct;39(1):55–76. doi: 10.1083/jcb.39.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yellin H. Neural regulation of enzymes in muscle fibers of red and white muscle. Exp Neurol. 1967 Sep;19(1):92–103. doi: 10.1016/0014-4886(67)90009-x. [DOI] [PubMed] [Google Scholar]
  41. ZENKER W., ANZENBACHER H. ON THE DIFFERENT FORMS OF MYO-NEURAL JUNCTION IN TWO TYPES OF MUSCLE FIBER FROM THE EXTERNAL OCULAR MUSCLES OF THE RHESUS MONKEY. J Cell Physiol. 1964 Jun;63:273–285. doi: 10.1002/jcp.1030630303. [DOI] [PubMed] [Google Scholar]
  42. Zacks S. I., Saito A. Uptake of exogenous horseradish peroxidase by coated vesicles in mouse neuromuscular junctions. J Histochem Cytochem. 1969 Mar;17(3):161–170. doi: 10.1177/17.3.161. [DOI] [PubMed] [Google Scholar]
  43. von Düring M. Uber die Feinstruktur der motorischen Endplatte von höheren Wirbeltieren. Z Zellforsch Mikrosk Anat. 1967;81(1):74–90. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES