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Ultrastructural identification of the primitive muscle spindle in the Xenopus laevis larvae

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Summary

The initial formation of muscle spindles was studied with electron microscopy using the toe muscle of Xenopus laevis. At the larval stage 57 (Nieuwkoop and Faber 1967), muscle spindles were first identified primarily by the presence of sensory endings associated with a thin bundle of myotubes, e.g. intrafusal (IF) myotubes which were partly invested by a single cellular layer. The number of IF myotubes per spindle was 5 to 6; the adult complement. IF-and extrafusal (EF) myotubes were almost identical in their size and structure. A few thinner IF myotubes with scaree myofibrils were also present. The reticular zone had been undeveloped. Sensory endings were smaller in size and in number per spindle than those in the adult, forming irregular beaded chains with occasional tubular expansions. The endings and IF myotubes were rarely in direct contact, being frequently interposed by a satellite cell and its process. Incipient fusimotor endings were widely distributed from the juxta-equatorial to the polar region. Large cored vesicles resembling the neurosecretory vesicles occurred in sensory and motor endings as well as in intramuscular nerve fibers. The vesicles may be involved in the neuronal influence upon the spindle differentiation.

The results were compared with the formative process of mammalian spindles.

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References

  • Barker D (1974) The morphology of muscle receptors. In: Hunt CC (ed) Handbook of Sensory Physiology. Vol. III/2 Muscle Receptors. Springer, Berlin, pp 1–190

    Google Scholar 

  • Barker D, Milburn A (1984) Development and regeneration of mammalian muscle spindles. Sci Prog Oxf 69: 45–64

    Google Scholar 

  • Campion DR (1984) The muscle satellite cell. Int Rev Cytol 87:225–251

    Google Scholar 

  • Cuajunco F (1927) Embryology of the neuromuscular spindle. Contrib Embryol 19: 45–72

    Google Scholar 

  • Cuajunco F (1940) Development of the neuromuscular spindle in human fetuses. Contrib Embryol 28: 97–128

    Google Scholar 

  • Gray EG (1957) The spindle and extrafusal innervation of a frog muscle. Proc R Soc B 146: 416–430

    Google Scholar 

  • Grillo MA, Paley SL (1962) Granule containing vesicles in the autonomic nervous system. In: Fifth Int Cong Electron Microscopy. Academic Press, New York, vol I.2, U-1

    Google Scholar 

  • Ishikawa H (1983) Fine structure of skeletal muscle. In: Dowben M, Shay JW (eds) Cell and Muscle Motility. Plenum Press, New York, vol 4, pp 1–84

    Google Scholar 

  • Karlsson UL (1972) The frog muscle spindle: Ultrastructure and intrafusal stretch characteristics. In: Banker BQ, Prizybylski RJ, Van Der Meulen JP, Victor M (eds) Research in Muscle Development and the Muscle Spindle. Excerpta Medica, Amsterdam, pp 299–332

    Google Scholar 

  • Karlsson UL, Andersson-Cedergren E, Ottoson D (1966) Cellular organization of the frog muscle spindle as revealed by serial sections for electron microscopy. J Ultrastruct Res 14: 1–35

    Google Scholar 

  • Karlsson UL, Andersson-Cedergren E (1966) Motor myoneural junctions on frog intrafusal muscle fibres. J Ultrastruct Res 14: 191–211

    Google Scholar 

  • Katz B (1961) The terminations of the afferent nerve fibre in the muscle spindle of the frog. Phil Trans R Soc B 243: 221–240

    Google Scholar 

  • Kozeka K, Ontell M (1981) The three-dimensional cytoarchitecture of developing murine muscle spindles. Dev Biol 87:133–147

    Google Scholar 

  • Kullberg RW, Lentz TL, Cohen MW (1977) Development of the myotomal neuromuscular junction in Xenopus laevis: an electrophysiological and fine-structural study. Dev Biol 60: 101–120

    Google Scholar 

  • Landon DN (1966) Electron microscopy of muscle spindles. In: Andrew BL (ed) Control and Innervation of Skeletal Muscle. D.C. Thomson & Co., Ltd, Dundee Scotland, pp 96–107

    Google Scholar 

  • Landon DN (1972a) The fine structure of developing muscle spindles in the rat. J Anat 111: 512–513

    Google Scholar 

  • Landon DN (1972b) The fine structure of the equatorial regions of developing muscle spindles in the rat. J Neurocytol 1: 189–210

    Google Scholar 

  • Marchand ER, Eldred E (1969) Post-natal increase in intrafusal fibres in the rat muscle spindle. Exp Neurol 25: 655–676

    Google Scholar 

  • Milburn A (1973) The early development of muscle spindles in the rat. J Cell Sci 12: 175–195

    Google Scholar 

  • Milburn A (1984) Stages in the development of cat muscle spindles. J Embryol Exp Morphol 82: 177–216

    Google Scholar 

  • Nieuwkoop PD, Faber J (1967) Normal Table of Xenopus Laevis (Daudin). North Holland Amsterdam

    Google Scholar 

  • Page SG (1966) Intrafusal muscle fibres in the frog. J Microscopic 5: 101–104

    Google Scholar 

  • Robertson JD (1960) Electron microscopy of the motor end-plate and the neuromuscular spindle. Amer J Phys Med 39: 1–43

    Google Scholar 

  • Schiaffino S, Bormioli SP (1976) Morphogenesis of rat muscle formation after nerve lesion during early postnatal development. J neurocytol 5: 319–336

    Google Scholar 

  • Shantha TR, Golarz MN, Bourne GH (1968) Histological and histochemical observations on the capsule of the muscle spindle in normal and denervated muscle. Acta Anat (Basel) 69: 632–646

    Google Scholar 

  • Sutton AC (1915) On the development of the neuromuscular spindle in the extrinsic eye muscles of the pig. Am J Anat 18: 117–144

    Google Scholar 

  • Tello JF (1917) Genesis de las terminaciones nerviosas motrices y sensitivas. Trab Lab Invest Biol Univ Madr 15: 101–109

    Google Scholar 

  • Tello JF (1922) Die Entstehung der motorischen und sensiblen Nervendingungen. Z Ges Anat 64: 348–440

    Google Scholar 

  • Uehara Y (1973) Unique sensory endings in rat muscle spindles. Z Zellforsch 136: 511–520

    Google Scholar 

  • Uehara Y, Hama K (1965) Some observations on the fine structure of the frog muscle spindle. (1). On the sensory terminals and motor endings of the muscle spindle. J Electron Microsc 14: 34–42

    Google Scholar 

  • Werner J (1972) Development of the neuromuscular spindle. Amer J Phys Med 51: 192–207

    Google Scholar 

  • Werner J (1973) Mixed intra-and extrafusal muscle fibres produced by temporary denervation in newborn rats. J Comp Neurol 150: 279–302

    Google Scholar 

  • Zelena J (1957) Morphogenetic influence of innervation on the ontogenetic development of muscle spindles. J Embryol Exp Morphol 5: 283–292

    Google Scholar 

  • Zelena J (1964) Development, degeneration and regeneration of receptor organs. In: Singer M, Schade JP (eds) Mechanisms of Neural Regeneration of Receptor Organs. Progress in Brain Research 13. Elsevier Publishing Company, Amsterdam London New York, pp 175–211

    Google Scholar 

  • Zelena J, Hnik P (1960a) Absence of spindles in muscles of rats reinnervated during development. Physiol Bohemoslov 9: 373–381

    Google Scholar 

  • Zelena J, Hnik P (1960b) Irreversible elimination of muscle receptors. Nature (Lond) 188: 946–947

    Google Scholar 

  • Zelena J, Soukup T (1973) Development of muscle spindles deprived of fusimotor innervation. Z Zellforsch 144: 435–452

    Google Scholar 

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Shinmori, H., Desaki, J. & Uehara, Y. Ultrastructural identification of the primitive muscle spindle in the Xenopus laevis larvae. Anat Embryol 177, 381–387 (1988). https://doi.org/10.1007/BF00304734

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