Summary
The M. complexus in the chick, commonly called the hatching muscle, undergoes conspicuous growth during the latter stages of embryonic development. Myogenesis of this muscle was compared to that of M. biceps femoris with regard to development of types of muscle fiber and their innervation. In both muscles β fibers are of relatively uniform size and show little growth in diameter between 12 days of development and hatching; α fibers develop continuously and display a wide range of diameters at all stages.
Initial thickenings on the sarcolemma of β fibers where axons are closely approximate were first observed at 10 days of development in both muscles. In both muscles β fibers are innervated prior to α fibers. Terminal axon networks bridge intercellular spaces and contact β fibers in different myogenic clusters, α fibers that develop on the surface membrane of β fibers exhibit focal thickenings of the membrane and some cell projections that are directed toward axon-β fiber contacts. These changes occurred only in α fibers of M. complexus.
At 14 days of embryogenesis, the processes of synaptogenesis and of myelin formation are less advanced in M. biceps femoris than in M. complexus. At this stage a fibers were observed to be innervated in M. complexus, but not yet in M. biceps femoris. Each β fiber was observed to be encircled by several preterminal axons.
It is concluded that the earlier development of M. complexus is correlated with an equally early development of nerve-muscle interactions.
Similar content being viewed by others
References
Ashmore, C.R., Addis, P.B., Doerr, L., Stokes, H.: Development of muscle fibers in the complexus muscle of normal and dystrophic chicks. J. Histochem. Cytochem. 21, 266–278 (1973)
Ashmore, C.R. Doerr, L.: Postnatal development of fiber types in normal and dystrophic chicks. Exp. Neurol. 30, 431–446 (1971a)
Ashmore, C.R., Doerr, L.: Comparative aspects of muscle fiber types in different species. Exp. Neurol. 31, 408–418 (1971 b)
Ashmore, C.R., Robinson, D.W., Rattray, P.V., Doerr, L.: Biphasic development of muscle fibers in the fetal lamb. Exp. Neurol. 37, 241–255 (1972)
Blechschmidt, E., Daikoku, S.H.: Die Entstehung der motorischen Innervation in der menschlichen Zungenmuskulatur. Elektronenmikroskopie der embryonalen Endplatte. Acta anat. (Basel) 63, 179–198 (1966)
Bock, W.J., Hikada, R.S.: An analysis of twitch and tonus fibers in the hatching muscle. Condor 70, 211–222 (1968)
Burke, R.E., Levine, D.N., Zojac, F.E., Tsaires, P., Engel, W.K.: Mammalian motor units: Physiological-histochemical correlation in three types of cat gastrocnemius. Science 174, 709–711 (1971)
Couteaux, R.: Motor endplate structure. In: The structure and function of muscle, Vol. I (G.H. Bourne, ed.), pp. 337–380. New York: Academic Press 1960
Cuajunco, F.: Development of the human motor endplate. Contr. Embryol. 195, 129–152 (1942)
Dabrós, W., Kaczmarski, F.: Motor endplates in the extraocular muscles of the tree sparrow, Passer montanus L. Z. mikr. anat. Forsch. 88, 1137–1148 (1974)
Edström, L., Kugelberg, E.: Histochemical composition, distribution of fibres and fatiguability of single motor units. J. Neurol. Neurosurg. Psychiat. 31, 424–433 (1968)
Fisher, H.I.: The “hatching muscle” in the chick. Auk. 75, 391–399 (1958)
Gerebtzoff, M.A.: Cholinesterase. A histochemical contribution to the solution of some functional problems. London: Pergamon Press 1959
Ginsborg, B.L.: Some properties of avian skeletal muscle fibers with multiple neuromuscular junctions. J. Physiol. (Lond.) 154, 581–598 (1960)
Guth, L.: Trophic influences of nerve on muscle. Physiol. Rev. 48, 645–680 (1968)
Hess, A.: Structural difference of fast and slow extrafusal muscle fibers and their nerve endings in chicken. J. Physiol. (Lond.) 157, 221–231 (1961)
Hirano, H.: Ultrastructural study on the morphogenesis of the neuromuscular junction in the skeletal muscle of the chick. Z. Zellforsch. 79, 198–208 (1967b)
Kano, M., Shimada, Y.: Innervation of skeletal muscle cells differentiated in vitro from chick embryo. Brain Res. 27, 402–405 (1971)
Kelly, A.M., Zacks, S.I.: The fine structure of motor endplate morphogenesis. J. Cell Biol. 42, 154–169 (1969)
Kikuchi, T.: Studies on development and differentiation of muscle. III. Especially on the mode of increase in the number of cells. Tohoku J. Agr. Res. 22, 1–15 (1971)
Kikuchi, T.: Ultrastructural evaluation of the myogenic cell fusion in chick embryo using the goniometer stage of electron microscopy. Tohoku J. Agr. Res. 23, 82–92 (1972a)
Kikuchi, T., Nagatani, T., Tamate, H.: Studies on development and differentiation of muscle. V. A comparative study of the growth of hatching muscle and the other muscles in chick embryo. Tohoku J. Agr. Res. 23, 149–159 (1972b)
Kikuchi, T., Nagatani, T., Tamate, H.: Studies on development and differentiation of muscle. VI. Cytokinetic analysis of cell proliferation by using 3H-thymidine autoradiography in various muscle tissues of chick embryo. Tohoku J. Agr. Res. 25, 22–36 (1974a)
Kikuchi, T., Nagatani, T., Tamate, H.: Studies on development and differentiation of muscle. VII. An expression of the myogenic cell fusion by using 3H-thymidine autoradiography in chick embryos. Tohoku J. Agr. Res. 25, 37–42 (1974b)
Krüger, P.: Untersuchungen am Vogelflügel. Zool. Anz. 145, 445–460 (1950)
Luft, J.H.:Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961)
Mumenthaler, M., Engel, W.K.: Cytological localization of cholinesterase in developing chick embryo skeletal muscle. Acta anat. (Basel) 47, 274–299 (1961)
Redfern, P.A.: Neuromuscular transmission in newborn rats. J. Physiol. (Lond.) 209, 701–709 (1970)
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)
Robbins, N., Yonezawa, T.: Developing neuromuscular junctions. First signs of chemical transmission during formation in tissue culture. Science 172, 395–398 (1971 a)
Robbins, N., Yonezawa, T.: Physiological studies during formation and development of rat neuromuscular junction in tissue culture. J. gen. Physiol. 58, 467–481 (1971 b)
Silver, S.: A histochemical investigation of cholinesterase at neuromuscular junctions in mammalian and avian muscles. J. Physiol. (Lond.) 169, 386–393 (1963)
Sisto-Daneo, L., Filogamo, G.: Ultrastructure of early neuromuscular contacts in chick embryo. J. Submicr. Cytol. 5, 219–225 (1973)
Sisto-Daneo, L., Filogamo, G.: Ultrastructure of developing myoneural junctions. Evidence for two patterns of synaptic area differentiation. J. Submicr. Cytol. 6, 219–228 (1974)
Sisto-Daneo, L., Filogamo, G.: Differentiation of synaptic area in «slow» and «fast» muscle fibres. J. Submicr. Cytol. 7, 121–131 (1975)
Tello, J.F.: Die Entstehung der motorischen und sensiblen Nervendigungen. I. In dem lokomotorischen System der höheren Wirbeltiere. Anat. Entwickl. Gesch. 64, 348–440 (1922)
Teräväinen, H.: Electron microscopic localization of cholinesterases in the rat myoneural junction. Histochemie 10, 266–271 (1967)
Teräväinen, H.: Development of the myoneural junction in the rat. Z. Zellforsch. 87, 249–265 (1968)
Visintini, F., Levi-Montalcini, R.: Relazione tra differenziazione strutturale e funzionale dei centri e delie vie nervose nell' émbrione di polio. Schweiz. Arch. Neurol. Psychiat. 43, 119–150 (1939)
Wake, K.: Motor endplates in developing chick embryo skeletal muscle, histological structure and histochemical localization of cholinesterase activity. Arch. Histol. Jap. 25, 23–41 (1964)
Zacks, S.I.: Embryogenesis of neuromuscular junction. In: The motor endplate (S.I. Zacks, ed.), pp. 32–51. New York: Robert E. Krieger Publishing Co. 1973
Author information
Authors and Affiliations
Additional information
This work was supported in part by a grant from the Muscular Dystrophy Association of America, Inc.
Postdoctoral Fellow of the Muscular Dystrophy Association I would like to thank Professor Dr. H. Tamate for his valuable advise. I am also grateful to Dr. L. Doerr, H. Stokes and Judi K. Lund for their advice and skilled technical assistance
Rights and permissions
About this article
Cite this article
Kikuchi, T., Ashmore, C.R. Developmental aspects of the innervation of skeletal muscle fibers in the chick embryo. Cell Tissue Res. 171, 233–251 (1976). https://doi.org/10.1007/BF00219408
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00219408