Skip to main content
Log in

The innervation pattern of crustacean skeletal muscle

Morphometry and ultrastructure of terminals and synapses

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The innervation pattern of distal muscle fibers of the opener muscle of walking legs of crayfish (Astacus leptodactylus) was investigated using methylene-blue staining, cobalt infiltration, and electron microscopy. A quantitative analysis of the entire innervation of single muscle fibers was attempted.

It was found that instead of the generally assumed parallel array of numerous excitatory and inhibitory terminals, innervation consists of only a few branched terminals. The branches of excitatory and inhibitory terminals lie side-by-side. Both types are characterized by numerous varicosities (see Fig. 9B). The aggregate length of excitatory as well as inhibitory terminals on one muscle fiber is, on the average, about 1,500 μm with a total of 152 varicosities spaced about 10 μm apart. The average diameter of the varicosities is 4.26 μm, that of the connecting thin segments about 0.5 μm. Total terminal surface of motor or inhibitory terminals amounts to about 10,000 μm2 per muscle fiber. There are approximately 2,000 motor synapses on each muscle fiber, but their average total area is only about 6% of the terminal membrane area, or 0.06% of the (idealized) muscle fiber surface.

There are conspicuous differences in the postsynaptic specializations associated with excitatory and inhibitory terminals; these are described in detail.

The results are discussed in a functional context and with regard to design and results of electrophysiological experiments.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Atwood HL (1972) Crustacean muscle. In: Bourne GH (ed) The structure and function of muscle. Plenum Press, New York London, pp 421–489

    Google Scholar 

  • Atwood HL (1973) An attempt to account for the diversity of crustacean muscle. Am Zool 13:357–378

    Google Scholar 

  • Atwood HL (1976) Organization and synaptic physiology of crustacean neuromuscular systems. Prog Neurobiol 7:291–391

    Google Scholar 

  • Atwood HL (1977) Crustacean neuromuscular systems: past, present, and future. In: Hoyle G (ed) Identified neurons and behavior of arthropods. Plenum Press, New York London, pp 9–30

    Google Scholar 

  • Atwood HL (1978) Fine structure of crustacean neuromuscular synapses. MSC-SMC Bull:18–21

  • Atwood HL, Jahromi SS (1978) Fast-axon synapses of a crab leg muscle. J Neurobiol 9:1–15

    Google Scholar 

  • Atwood HL, Johnston H (1968) Neuromuscular synapses of a crab motor axon. J Exp Zool 167:457–470

    Google Scholar 

  • Atwood HL, Jones A (1967) Presynaptic inhibition in crustacean muscle: axo-axonal synapse. Experientia 23:1036–1038

    Google Scholar 

  • Atwood HL, Kwan I (1976) Synaptic development in the crayfish opener muscle. J Neurobiol 7:289–312

    Google Scholar 

  • Atwood HL, Morin WA (1970) Neuromuscular and axoaxonal synapses of the crayfish opener muscle. J Ultrastruct Res 32:351–369

    Google Scholar 

  • Atwood HL, Lang F, Morin WA (1972) Synaptic vesicles: selective depletion in crayfish excitatory and inhibitory axons. Science 176:1353–1355

    Google Scholar 

  • Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in'wholemount preparations. Brain Res 138:359–363

    Google Scholar 

  • Bittner GD, Kennedy D (1970) Quantitative aspects of transmitter release. J Cell Biol 47:586–592

    Google Scholar 

  • Bullock TH, Orkand R, Grinnell A (1977) Introduction to the Nervous System. WH Freeman and Co, San Francisco

    Google Scholar 

  • Dudel J, Kuffler SW (1961a) The quantal nature of transmission and spontaneous miniature potentials at the crayfish neuromuscular junction. J Physiol 155:514–529

    Google Scholar 

  • Dudel J, Kuffler SW (1961b) Mechanism of facilitation at the crayfish neuromuscular junction. J Physiol (Lond) 155:530–542

    Google Scholar 

  • Florey E (1966) An Introduction to General and Comparative Physiology. WB Saunders Co, Philadelphia

    Google Scholar 

  • Florey E, Rathmayer M (1979) Is glutamate the transmitter of crustacean motoneurons? J Physiol, Paris 75:629–634

    Google Scholar 

  • Florey E, Rathmayer M (1981) Glutamate actions on crustacean muscle. In: DeFeudis FV, Mandel P (eds) Amino acid neurotransmitters. Raven Press, New York, pp 351–358

    Google Scholar 

  • Hustert R (1974) Morphologie und Atmungsbewegungen des 5. Abdominalsegmentes von Locusta migratoria migratorioides. Zool Jb Physiol 78:157–174

    Google Scholar 

  • Iles JF, Mulloney B (1971) Procion yellow staining of cockroach motoneurons without the use of microelectrodes. Brain Res 30:397–400

    Google Scholar 

  • Jahromi SS, Atwood HL (1967) Ultrastructural features of crayfish phasic and tonic muscle fibers. Can J Zool 45:601–606

    Google Scholar 

  • Jahromi SS, Atwood HL (1974) Three-dimensional ultrastructure of the crayfish neuromuscular apparatus. J Cell Biol 63:599–613

    Google Scholar 

  • Johnson EW, Wernig A (1971) The binomial nature of transmitter release at the crayfish neuromuscular junction. J Physiol (Lond) 218:757–767

    Google Scholar 

  • Kosaka K (1969) Electrophysiological and electron microscopic studies on the neuromuscular junction of the crayfish stretch receptors. Jpn J Physiol 19:160–175

    Google Scholar 

  • Lang F, Atwood HL (1973) Crustacean neuromuscular systems: functional morphology of nerve terminals and the mechanism of facilitation. Am Zool 13:337–355

    Google Scholar 

  • Linder TM (1973) Calcium and facilitation at two classes of crustacean neuromuscular synapses. J Gen Physiol 61:56–73

    Google Scholar 

  • Linder TM (1974) The accumulative properties of facilitation at crayfish neuromuscular synapses. J Physiol (Lond) 238:223–234

    Google Scholar 

  • McMahan UJ, Spitzer NC, Peper K (1972) Visual identification of nerve terminals in living isolated skeletal muscle. Proc R Soc Lond (Biol) 181:421–430

    Google Scholar 

  • Onodera K, Takeuchi A (1980) Distribution and pharmacological properties of synaptic and extrasynaptic glutamate receptors on crayfish muscle. J Physiol 306:233–250

    Google Scholar 

  • Pitman RM, Tweedle CD, Cohen MJ (1972) Branching of central neurons: intracellular cobalt injection for light and electron microscopy. Science 176:412–414

    Google Scholar 

  • Schmidt-Nielsen K (1975) Animal physiology. Cambridge University Press, London New York

    Google Scholar 

  • Siewing R (1980) Lehrbuch der Zoologie, Vol I, Allgemeine Zoologie. Gustav Fischer Verlag, Stuttgart New York

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    CAS  PubMed  Google Scholar 

  • Tilsdale AD, Nakajima Y (1976) Fine structure of synaptic vesicles in two types of nerve terminals in crayfish stretch receptor organs: influence of fixation methods. J Comp Neurol 165:369–386

    Google Scholar 

  • Uchizono K (1967) Inhibitory synapses on the stretch receptor neurone of the crayfish. Nature (Lond) 214:833–834

    Google Scholar 

  • Van Harreveld A (1939) The nerve supply of doubly and triply innervated crayfish muscles related to their function. J Comp Neurol 70:267–284

    Google Scholar 

  • Van Harreveld A (1939) Doubly-, triply-, quadruply- and quintuply-innervated crustacean muscles. J Comp Neurol 70:285–296

    Google Scholar 

  • Walther C (1981) Synaptic terminals from an identified motoneuron in locust muscle: comparison between first instar larva and adult. Neuroscience Lett 27:237–242

    Google Scholar 

  • Wernig A (1972) Changes in statistical parameters during facilitation at the crayfish neuromuscular junction. J Physiol (Lond) 226:751–759

    Google Scholar 

  • Zucker RS (1973) Changes in the statistics of transmitter release during facilitation. J Physiol (Lond) 229:787

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by Sonderforschungsbereich 138 of the Deutsche Forschungsgemeinschaft

Rights and permissions

Reprints and permissions

About this article

Cite this article

Florey, E., Cahill, M.A. The innervation pattern of crustacean skeletal muscle. Cell Tissue Res. 224, 527–541 (1982). https://doi.org/10.1007/BF00213750

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00213750

Key words

Navigation