Advertisement

Journal of Neurocytology

, Volume 16, Issue 1, pp 1–10 | Cite as

Elimination of distributed acetylcholine receptor clusters from developing fast-twitch fibres in an avian muscle

  • William D. Phillips
  • Max R. Bennett
Article

Summary

The development of the focal localization of large acetylcholine receptor clusters (AChR-Cs) on avian fast muscle fibres has been investigated in the triceps brachii pars humeralis (TH) muscle of the chick embryo. The mature TH muscle consists of both fast fibres, which usually receive a focal innervation at single synaptic sites, and slow fibres which receive a distributed innervation at multiple synaptic sites. Single fibre fragments dissociated from the embryonic muscle were typed using anti-myosin antibodies; fluorescently labelled α-bungarotoxin was used to identify large AChR-Cs which serve as synaptic markers. In contrast to the mature focal innervation, at embryonic day 11 (E11), many fast-type fibres in the TH muscle displayed large, distributed AChR-Cs (3.7 ± 0.7 per 1000 μm fibre length;n = 6 embryos) like neighbouring slow-type fibres. By E16 distributed AChR-Cs were rare on fast type fibres (0.9 ± 0.2 per 1000 μm fibre length). As it was possible that the frequency of fast fibres with distributed AChR-Cs declined simply as a consequence of the increase in number of secondary generation fibres, tritiated thymidine was injected at E7 in order to identify the primary generation fibres at E14. The great majority of fast fibres that were heavily labelled with thymidine at E14 appeared to possess a focal AChR-C. The results suggest that at E11 fast-type primary fibres in the TH muscle receive a distributed innervation very similar to neighbouring slow-type fibres; this subsequently evolves into the mature focal innervation following the elimination of synaptic sites between E11 and E14.

Keywords

Chick Embryo Tritiated Thymidine Slow Fibre Fast Fibre Synaptic Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ashmore, C. R., Kikuchi, T. &Doerr, L. (1978) Some observations on the innervation patterns of different fiber types of chick muscle.Experimental Neurology 58, 272–84.PubMedCrossRefGoogle Scholar
  2. Atsumi, S. (1977) Development of neuromuscular junctions of fast and slow muscles in the chick embryo: a light and electron microscopic study.Journal of Neurocytology 6, 691–709.PubMedCrossRefGoogle Scholar
  3. Barnard, E. A., Lyles, J. M. &Pizzey, J. A. (1982) Fibre types in chicken skeletal muscles and their changes in muscular dystrophy.Journal of Physiology 331, 333–54.PubMedGoogle Scholar
  4. Bennett, M. R., Fernandez, H. &Lavidis, N. A. (1985) Development of the mature distribution of synapses on fibres in the frog sartorius muscle.Journal of Neurocytology 14, 981–95.PubMedCrossRefGoogle Scholar
  5. Bennett, M. R. &Pettigrew, A. G. (1974a) The formation of synapses in striated muscle during development.Journal of Physiology 241, 515–45.PubMedGoogle Scholar
  6. Bennett, M. R. &Pettigrew, A. G. (1974b) The formation of synapses in reinnervated and cross-reinnervated striated muscle during development.Journal of Physiology 241, 547–73.PubMedGoogle Scholar
  7. Betz, H., Bourgeois, J.-P. &Chanceux, J.-P. (1980) Evolution of cholinergic proteins in developing slow and fast skeletal muscles in chick embryo.Journal of Physiology 302, 197–218.PubMedGoogle Scholar
  8. Bevan, S. &Steinbach, J. H. (1977) The distribution of α-bungarotoxin binding sites on mammalian skeletal muscle developingin vivo.Journal of Physiology 267, 195–213.PubMedGoogle Scholar
  9. Brown, M. C., Jansen, J. K. S. &Van Essen, D. (1976) Polyneuronal innervation of skeletal muscle in newborn rats and its elimination during maturation.Journal of Physiology 261, 387–422.PubMedGoogle Scholar
  10. Burden, S. (1977) Development of the neuromuscular junction in the chick embryo: the number, distribution, and stability of acetylcholine receptors.Developmental Biology 57, 317–29.PubMedCrossRefGoogle Scholar
  11. Butler, J., Cosmos, E. &Brierley, J. (1982) Differentiation of muscle fibre types in aneurogenic brachial muscles of the chick embryo.Journal of Experimental Zoology 224, 65–80.PubMedCrossRefGoogle Scholar
  12. Elizalde, A., Huerta, M. &Stefani, E. (1983) Selective reinnervation of twitch and tonic muscle fibres of the frog.Journal of Physiology 340, 513–24.PubMedGoogle Scholar
  13. Feng, T. P., Wu, W. Y. &Yang, F. Y. (1965) Selective reinnervation of a ‘slow’ or ‘fast’ muscle by its original motor supply during regeneration of a mixed nerve.Scientia Sinica 14, 1717–20.Google Scholar
  14. Hamburger, V. &Hamilton, H. L. (1951) A Series of normal stages in the development of the chick embryo.Journal of Morphology 88, 49–92.CrossRefGoogle Scholar
  15. Harris, A. J. (1981) Embryonic growth and innervation of rat skeletal muscles. III. Neural regulation of junctional and extra-junctional acetylcholine receptor clusters.Philosophical Transactions of the Royal Society of London, Series B 293, 287–314.Google Scholar
  16. Hess, A. (1961) Structural differences of fast and slow extrafusal muscle fibres and their nerve endings in chickens.Journal of Physiology 157, 221–31.PubMedGoogle Scholar
  17. Hess, A. (1970) Vertebrate slow muscle fibres.Physiological Reviews 50, 40–62.PubMedGoogle Scholar
  18. Hoh, J. F. Y. (1971) Selective reinnervation of fast-twitch and slow-graded muscle fibres in the toad.Experimental Neurology 30, 263–76.PubMedGoogle Scholar
  19. Ishikawa, Y., Masuko, S. &Shimada, Y. (1983) Acetylcholine receptors and motor nerve terminals in developing chick skeletal muscles as revealed by fluorescence microscopy.Developmental Brain Research 8, 111–18.CrossRefGoogle Scholar
  20. Jacob, M. &Lentz, T. L. (1979) Localization of acetylcholine receptors by means of horseradish peroxidase-α-bungarotoxin during formation and development of the neuromuscular junction in the chick embryo.Journal of Cell Biology 82, 195–211.PubMedCrossRefGoogle Scholar
  21. Khaskiye, A., Toutant, J. -P., Toutant, M., Renaud, D. &Le Douarin, -G. H. (1980) Effect of heterotopic innervation on the development of synaptic pattern in chick embryo muscles.Archives d'Anatomie Microscopique et de Morphologie Experimentale 69, 135–46.PubMedGoogle Scholar
  22. Kikuchi, T. (1971) Studies on development and differentiation of muscle. III. Especially on the mode of increase in the number of cells.Tohoku Journal of Agricultural Research 22, 1–15.Google Scholar
  23. Koenig, J. (1970) Contribution a l'etude de la morphologie des plaques motrices des grands dorsaux anterieur et posterieur du poulet apres innervation croisee.Archives d'Anatomie Microscopique et de Morphologie Experimentale 59, 403–26.PubMedGoogle Scholar
  24. McLennan, I. S. (1983) The development of the pattern of innervation in chicken hindlimb muscles: evidence for specification of nerve-muscle connections.Developmental Biology 97, 229–38.PubMedCrossRefGoogle Scholar
  25. Ontell, M. &Dunn, R. F. (1978) Neonatal muscle growth: a quantitative study.American Journal of Anatomy 152, 539–56.PubMedCrossRefGoogle Scholar
  26. Phillips, W. D. &Bennett, M. R. (1984) Differentiation of fiber types in wing muscles during development: effect of neural tube removal.Developmental Biology 106, 457–68.PubMedCrossRefGoogle Scholar
  27. Phillips, W. D., Everett, A. W. &Bennett, M. R. (1986) The role of innervation in the establishment of the topographical distribution of primary myotube types during development.Journal of Neurocytology 15, 397–405.PubMedCrossRefGoogle Scholar
  28. Phillips, W. D., Lai, K. &Bennett, M. R. (1985) Spatial distribution and size of acetylcholine receptor clusters determined by motor nerves in developing chick muscles.Journal of Neurocytology 14, 309–25.PubMedCrossRefGoogle Scholar
  29. Pittman, R. &Oppenheim, R. W. (1979) Cell death of motoneurons in the chick embryo spinal cord. IV. Evidence that a functional neuromuscular interaction is involved in the regulation of naturally occurring cell death and the stabilization of synapses.Journal of Comparative Neurology 187, 425–46.PubMedCrossRefGoogle Scholar
  30. Redfern, P. A. (1970) Neuromuscular transmission in newborn rats.Journal of Physiology 209, 701–9.PubMedGoogle Scholar
  31. Rouaud, T. &Toutant, J.-p. (1982) Histochemical properties and innervation pattern of fast and slow-tonic fibre types of the anterior latissimus dorsi muscle of the chick.Histochemical Journal 14, 415–28.PubMedCrossRefGoogle Scholar
  32. Smith, M. A. &Slater, C. R. (1983) Spatial distribution of acetylcholine receptors at developing chick neuromuscular junctions.Journal of Neurocytology 12, 993–1005.PubMedCrossRefGoogle Scholar
  33. Toutant, J. P., Rouaud, T. &Le Douarin, G. H. (1981) Histochemical properties of the biventer cervicis muscle of the chick: a relationship between multiple innervation and slow-tonic fibre types.Histochemical Journal 13, 481–93.PubMedCrossRefGoogle Scholar
  34. Toutant, J. P., Toutant, M. N., Renaud, D. &Le Douarin, G. H. (1979) Enzymatic differentiation of muscle fibre types in embryonic latissimus dorsi of the chick: effects of spinal cord stimulation.Cell Differentiation 8, 375–82.PubMedCrossRefGoogle Scholar
  35. Zelena, J., Vyklicky, L. &Jirmanova, I. (1967) Motor endplates in fast and slow muscles of the chick after cross union of their nerves.Nature 214, 1010–1.PubMedCrossRefGoogle Scholar

Copyright information

© Chapman and Hall Ltd 1987

Authors and Affiliations

  • William D. Phillips
    • 1
  • Max R. Bennett
    • 1
  1. 1.The Neurobiology Research CentreUniversity of SydneyNSWAustralia

Personalised recommendations