Skip to main content
Log in

Development of the myoneural junction in the rat

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

The structure of the myoneural junction in the striated muscle of rat embryos and postnatal rats was studied by electron microscopy in order to assess at ultrastructural level the roles of neuronal and muscular elements and the sequence of events resulting in the formation of a functionally mature synaptic organization.

From the observations it is concluded that the axon terminals enveloped by Schwann cells contain vesicles prior to apposition of the prospective synaptic membranes. Subsequently, subsarcolemmal thickening of the postsynaptic membrane takes place after the synaptic gap has been formed by disappearance of the teloglial cell from between the synaptic membranes but before the primary synaptic cleft in the strict sense is formed. Secondary synaptic clefts are formed later, when the primary synaptic cleft is regular in width, by local finger-like invaginations of the postsynaptic membrane, which thereafter expand basally, in a plane transverse to the axis of the axon terminal, to resemble flattened flasks. The junction is formed between multinucleated muscle cells and multiple axons, which at first lie side by side and later, when formation of adult-type secondary synaptic clefts is in progress, become separated by folds of the sarcoplasm and the teloglia. In extraocular muscles of adult rats the sarcoplasmic reticulum is closely associated with the postjunctional sarcoplasm.

In the light of earlier observations on the development of contractibility after nerve stimulation, cholinesterase histochemistry and muscle fibre physiology, these observations are interpreted to indicate that functional differentiation of the myoneural synapse results from induction by the motor axon and that the association of the sarcoplasmic reticulum with the postjunctional sarcoplasm in adult extraocular muscles is related to modified fibre physiology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson-Cedergren, E.: Ultrastructure of motor end plate and sarcoplasmic components of mouse skeletal muscle fiber as revealed by free-dimensional reconstructions from serial sections. J. Ultrastruct. Res. 2, Suppl. 1, 1–191 (1959).

    Google Scholar 

  • Angulo, y Gonzales, A. W.: The prenatal development of behaviour in the albino rat. J. comp. Neurol. 55, 395–442 (1932).

    Google Scholar 

  • —: Anat. Rec. 52, 117–138 (1932a).

    Google Scholar 

  • Bauer, W. C., J. M. Blumberg, and S. I. Zacks: Short and long term ultrastructure changes in denervated mouse motor end plates. Proc. IV. int. Congr. Neuropathology Munich 1962, p. 16–18. Stuttgart: Georg Thieme 1962.

    Google Scholar 

  • Beams, H. W., and T. C. Evans: Electron micrographs of motor end-plates. Proc. Soc. exp. Biol. (N.Y.) 82, 344–346 (1953).

    Google Scholar 

  • Bergman, R. A.: Observations on the morphogenesis of rat skeletal muscle. Bull. Johns Hopk. Hosp. 110, 187–201 (1962).

    Google Scholar 

  • Birks, R., H. E. Huxley, and B. Katz: The fine structure of the neuromuscular junction of the frog. J. Physiol. (Lond.) 150, 134–144 (1960).

    Google Scholar 

  • Blechschmidt, E., u. S. H. Daikoku: Die Entstehung der motorischen Innervation in der menschlichen Zungenmuskulatur. Elektronenmikroskopie der embryonalen Endplatte. Acta anat. (Basel) 63, No. 2, 179–198 (1966).

    Google Scholar 

  • Breemen, V. L. van, E. D. Anderson, and J. F. Reger: An attempt to determine the origin of synaptic vesicles. Exp. Cell Res., Suppl. 1, 153–167 (1958).

    Google Scholar 

  • Brown, G. L., and A. M. Harvey: Neuromuscular transmission in the extrinsic muscles of the eye. J. Physiol. (Lond.) 99, 379–399 (1941).

    Google Scholar 

  • Brzybylski, R. I., and J. M. Blumberg: Ultrastructural aspects of myogenesis in the chick. Lab. Invest. 15, 836–863 (1966).

    Google Scholar 

  • Couteaux, R.: The differentiation of synaptic areas. Proc. roy. Soc. B 158, 457–480 (1963).

    Google Scholar 

  • De Harven, E., and C. Coërs: Electron microscopic study of the human neuromuscular junction. J. biophys. biochem. Cytol. 6, 7–10 (1959).

    Google Scholar 

  • de Robertis, E.: Submicroscopic morphology and function of the synapse. Exp. Cell Res., Suppl. 5, 347–369 (1958).

    Google Scholar 

  • —: Ultrastructure and cytochemistry of the synaptic region. The macromolecular components involved in nerve transmission are being studied. Science 156, 907–914 (1967).

    Google Scholar 

  • Düring, M. v.: Über die Feinstruktur der motorischen Endplatte von höheren Wirbeltieren. Z. Zellforsch. 81, 74–90 (1967).

    Google Scholar 

  • East, E. W.: An anatomical study of the initiation of movement in rat embryos. Anat. Rec. 50, 201–219 (1931).

    Google Scholar 

  • Edwards, G. A., H. Ruska, and E. De Harven: Electron microscopy of peripheral nerves and neuromuscular junctions in the wasp leg. J. biophys. biochem. Cytol. 4, 107–114 (1958).

    Google Scholar 

  • —: Neuromuscular junctions in flight and tymbal muscles of the cicada. J. biophys. biochem. Cytol. 4, 251–256 (1958).

    Google Scholar 

  • Eränkö, O.: Histochemistry of nervous tissues: catecholamines and cholinesterases. Ann. Rev. Pharmacol. 7, 203–222 (1967).

    Google Scholar 

  • Estable, C., W. Acosta-Ferreira, and I. R. Sotelo: An electron microscopic study of the regenerating nerve fibres. Z. Zellforsch. 46, 387–399 (1957).

    Google Scholar 

  • Fawcett, D. H.: The sarcoplasmic reticulum of skeletal and cardiac muscle. Circulation 24, 336–348 (1961).

    Google Scholar 

  • Firket, H.: Ultrastructural aspects of myofibrils formation in cultured skeletal muscle. Z. Zellforsch. 78, 313–327 (1967).

    Google Scholar 

  • Fischmann, D. A.: An electron microscopic study of myofibril formation in embryonic chick skeletal muscle. J. Cell Biol. 32, 557–575 (1967).

    Google Scholar 

  • Gauthier, G. F., and H. A. Padykula: Cytological studies of fiber types in skeletal muscle. A comparative study of the mammalian diaphragm. J. Cell Biol. 28, 333–354.

  • Glees, P., and L. Sheppard: Electron microscopical studies on the synapse in developing chick spinal cord. Z. Zellforsch. 62, 356–362 (1964).

    Google Scholar 

  • Gustafsson, R., J. R. Tata, O. Lindberg, and L. Ernster: The relationship between the structure and activity of rat skeletal muscle mitochondria after thyroidectomy and thyroid hormone treatment. J. Cell Biol. 26, 555–578 (1965).

    Google Scholar 

  • Harrison, R. G.: An experimental study of the relation of the nervous system to the developing musculature in the embryo of the frog. Amer. J. Anat. 3, 197–220 (1904).

    Google Scholar 

  • Hess, A.: The sarcoplasmic reticulum, the T system, and the motor terminals of slow and twitch muscle fibers in the garter snake. J. Cell Biol. 26, 467–476 (1965).

    Google Scholar 

  • Hirano, H.: Ultrastructural study on the morphogenesis of the neuromuscular junction in the skeletal muscle of the chick. Z. Zellforsch. 79, 198–208 (1967).

    Google Scholar 

  • Hooker, D.: The development and function of voluntary and cardiac muscle in embryos without nerves. J. exp. Zool. 11, 159–186 (1911).

    Google Scholar 

  • Kelly, A. M.: The development of the motor end plate in the rat. J. Cell Biol. 31, A 114 (1966).

    Google Scholar 

  • Kokko, A., and L. Rechardt: Block staining for electron microscopy of nervous tissue. Z. Zellforsch. (1967) in press.

  • Lampert, P. W.: A comparative electron microscopic study of reactive, degenerating, regenerating and dystrophic axons. J. Neuropath. exp. Neurol. 26, 345–368 (1967).

    Google Scholar 

  • Luft, J. H.: The fine structure of electric tissue. Exp. Cell Res., Suppl. 5, 168–182 (1958).

    Google Scholar 

  • —: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Mauro, A.: Satellite cells of skeletal muscle fibres. J. biophys. biochem. Cytol. 9, 493–495 (1961).

    Google Scholar 

  • Meller, K.: Elektronenmikroskopische Befunde zur Differenzierung der Rezeptorzellen und Bipolarzellen der Retina und ihrer synaptischen Verbindungen. Z. Zellforsch. 64, 733–750 (1964).

    Google Scholar 

  • —, u. R. Haupt: Die Feinstructur der Hemo-, Glio- und Ependymoblasten von Hühnerembryonen in der Gewebekultur. Z. Zellforsch. 76, 260–277 (1967).

    Google Scholar 

  • Ochi, J.: Elektronenmikroskopische Untersuchung des Bulbus olfactorius der Ratte während der Entwicklung. Z. Zellforsch. 76, 339–348 (1967).

    Google Scholar 

  • Page, S. G.: A comparison of the fine structures of frog slow and twitch muscle fibers. J. Cell Biol. 26, 477–497 (1965).

    Google Scholar 

  • Palade, G. E., and S. L. Palay: Electron microscopic observations of interneuronal and neuromuscular synapses. Anat. Rec. 118, 335–336 (1954).

    Google Scholar 

  • Porter, K. R.: The sarcoplasmic reticulum. Its recent history and present status. J. biophys. biochem. Cytol. 10, Suppl. 4, 219–226 (1961).

    Google Scholar 

  • Reger, J. F.: Electron microscopy of the motor end-plate in the rat intercostal muscle. Anat. Rec. 122, 1–16 (1955).

    Google Scholar 

  • —: Electron micrographs of neuromuscular synapses from mammalian (albino mice) and amphibian (Rana pipens) gastrocnemii muscles. Anat. Rec. 128, 608–609 (1957).

    Google Scholar 

  • —: The fine structure of neuromuscular synapses of gastrocnemii from mouse and frog. Anat. Rec. 130, 7–24 (1958).

    Google Scholar 

  • —: Studies on the fine structure of normal and denervated neuromuscular junctions from mouse gastrocnemius. J. Ultrastruct. Res. 2, 269–282 (1959).

    Google Scholar 

  • —: A study on the fine structure of muscle and neuromuscular junctions from vertebrate skeletal muscle known to give the tonus (ACh) contracture reaction. Anat. Rec. 133, 327 (1959a).

    Google Scholar 

  • —: The fine structure of neuromuscular junctions and the sarcoplasmic reticulum of extrinsic eye muscles of Fundulus heteroclitus. J. biophys. biochem. Cytol. 10, Suppl. 4, 111–121 (1961).

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Robertson, J. D.: The ultrastructure of a reptilian myoneural junction J. biophys. biochem. Cytol. 2, 381–394 (1956).

    Google Scholar 

  • —: Electron microscopy of the motor end plate and the neuromuscular spindle. Amer. J. phys. Med. 39, 1–43 (1960).

    Google Scholar 

  • Rosenbluth, J.: Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13, 405–421 (1962).

    Google Scholar 

  • Sabatini, D. D., K. Bensch, and R. J. Barrnett: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963).

    Google Scholar 

  • Straus, W. L.: Changes in the structure of skeletal muscle at the time of its first visible contraction in living rat embryos. Anat. Rec. 73, Suppl. 2, 50–55 (1939).

    Google Scholar 

  • —, and G. Weddell: Nature of the first visible contractions of the forelimb musculature in rat foetuses. J. Neurophysiol. 3, 358–369 (1940).

    Google Scholar 

  • Takaya, H.: Series of investigations 1953–1957. Cited in: Primary embryonic induction (Saxén, L., and S. Toivonen, eds.), p. 221–227. London: Acad. Press, Inc. 1962.

    Google Scholar 

  • Teräväinen, H.: Electron microscopic localization of cholinesterases in the rat myoneural junction. Histochemie 10, 266–271 (1967).

    Google Scholar 

  • —: Carboxylic esterases in developing myoneural junctions of rat striated muscle. Histochemie 12, 307–315 (1968).

    Google Scholar 

  • Thaemert, J. C.: Ultrastructural interrelationships of nerve processes and smooth muscle cells in three dimensions of frog and snake. J. Cell Biol. 28, 37–49 (1966).

    Google Scholar 

  • Waterman, A. J.: A laboratory manual of comparative vertebrate embryology, p. 71–81. London: Constable and Company, Ltd. 1948.

    Google Scholar 

  • Watson, M. L.: Staining of tissue sections for electron microskopy with heavy metals. J. Cell Biol. 4, 475–478 (1958).

    Google Scholar 

  • Wettstein, R., and J. R. Sotelo: Electron microscopic study on the regenerative processes of peripheral nerves of mice. Z. Zellforsch. 59, 708–730 (1963).

    Google Scholar 

  • Windle, W. F., and R. E. Baxter: Development of reflex mechanisms in the spinal cord of albino rat embryos. Correlations between structure and function, and comparisons with the cat and the chick. J. comp. Neurol. 63, 189–210 (1936).

    Google Scholar 

  • —, W. L. Minear, M. F. Austin, and D. W. Orr: The origin and early development of somatic behaviour in the albino rat. Physiol. Zool. 8, 156–185 (1935).

    Google Scholar 

  • Wolff, H. H.: Über den Einfluß der Fixierung auf die elektronenmikroskopische Darstellung der Muskelfasern des Rattendiaphgragmas. Z. Zellforsch. 73, 192–204 (1966).

    Google Scholar 

  • Zacks, S. I., and I. M. Blumberg: Observations on the fine structure and cytochemistry of mouse and human intercostal neuromuscular junctions. J. Cell Biol. 10, 517–528 (1961).

    Google Scholar 

  • Zenker, W., and E. Krammer: Untersuchungen über Feinstruktur und Innervation der inneren Augenmuskulatur des Huhnes. Z. Zellforsch. 83, 147–168 (1967).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The author wishes to thank Prof. Antti Telkkä, M.D., Head of the Electron Microscope Laboratory, University of Helsinki, for placing the electron microscopic facilities at his disposal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Teräväinen, H. Development of the myoneural junction in the rat. Z. Zellforsch. 87, 249–265 (1968). https://doi.org/10.1007/BF00319723

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00319723

Keywords

Navigation