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The differentiation of intrafusal fibre types in rat muscle spindles after motor denervation

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Hind limb muscles were de-efferented in 19 new-born rats by removal of the lumbosacral spinal cord, with preservation of spinal ganglia and their peripheral branches. The juxtaequatorial and polar zones of muscle spindles were studied in different leg muscles 3 to 9 weeks after the operation in order to establish whether intrafusal fibre types would become differentiated after permanent motor denervation.

De-efferented intrafusal fibres developed into distinct ultrastructural fibre types similar to those found in control muscles. The nuclear bag type had confluent myofibrils with ill-defined M lines and relatively few mitochondria. The nuclear chain type had discrete myofibrils with prominent M lines, numerous large mitochondria and a more developed sarcotubular system. The fibre type characteristics were sometimes blurred by disarranged cross striation, but they were clearly discernible in 59 out of 69 de-efferented fibres of 31 spindles investigated in the electron microscope.

A sample of 220 de-efferented spindles from leg muscles of 6 rats was examined in the light microscope on transverse sections stained for ATPase activity. The difference in the ATPase activity among intrafusal fibre types was marked in about 70% spindles; in contrast to this, no distinct fibre types could be discerned in the population of extrafusal fibres which were stained rather uniformly. In de—efferented spindles-as in normal control spindlesnuclear chain fibres always exhibited high ATPase activity, whereas one of the nuclear bag fibres had low ATPase and the other either low or medium to high ATPase activity. However, the ATPase activity of de-efferented muscles was generally lower than that of normal muscles.

It can be concluded that intrafusal fibres do acquire their fibre type characteristics after fusimotor denervation despite complete deprivation of nerve impulse activity during the postnatal period when intrafusal fibre types differentiate in normal spindles.

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References

  • Andrew, B. L., Part, N. J.: The distribution of fusimotor fibres to distal caudal muscles in the rat (in preparation; quoted from Barker, 1974)

  • Andrew, B. L., Part, N. J., Wait, F.: Muscle spindles without γ-efferents. J. Physiol. (Lond.) 219, 28–29 (1971)

    Google Scholar 

  • Arutyunyan, R. S.: Influence of acetylcholin on normal and denervated muscle receptors. (In Russian). Byull. eksp. Biol. Med. 12, 14–17 (1969)

    Google Scholar 

  • Axelsson, J., Thesleff, S.: A study of supersensitivity in denervated mammalian skeletal muscle. J. Physiol. (Lond.) 147, 178–193 (1959)

    Google Scholar 

  • Banker, B. Q., Girvin, J. P.: The ultrastructural features of the normal and de-efferented mammalian muscle spindles. In: Research in muscle development and the muscle spindle (B. Q. Banker, R. J. Przybylski, J. P. Van der Meulen and M. Victor, eds.). International Congress Series No 240, p. 257–296. Amsterdam: Excerpta Medica 1972

    Google Scholar 

  • Barker, D.: Morphology of muscle receptors. In: Muscle receptors (C. C. Hunt ed.), vol. III, pt. 2. Handbook of sensory physiology. Berlin-Heidelberg-New York: Springer 1974 (in press)

    Google Scholar 

  • Barker, D., Bessou, P., Jankowska, E., Pagès, B., Stacey, M.: Distribution des axones fusimoteurs statiques et dynamiques aux fibres musculaires intrafusales, chez le chat. C. R. Acad. Sci. (Paris) 275, 2527–2529 (1972)

    Google Scholar 

  • Barker, D., Emonet-Dénand, P., Laporte, Y., Proske, U., Stacey, M.: Identification des terminaisons motrices des fibres fusimotrices statiques chez la chat. C. R. Acad. Sci. (Paris) 271, 1203–1206 (1970)

    Google Scholar 

  • Barker, D., Emonet-Dénand, F., Laporte, Y., Proske, U., Stacey, M.: Identification of the endings and function of cat fusimotor fibres. J. Physiol. (Lond.) 216, 51–52 (1971)

    Google Scholar 

  • Barker, D., Emonet-Dénand, F., Laporte, Y., Proske, U., Stacey, M.: Morphological identification and intrafusal distribution of the endings of static fusimotor axons in the cat. J. Physiol. (Lond.) 230, 405–427 (1973)

    Google Scholar 

  • Barker, D., Harker, D. W., Stacey, M. J., Smith, C. R.: Fusimotor innervation. In: Research concepts in muscle development and the muscle spindle (Banker, B.Q. et al., eds.), p. 227–250. Amsterdam: Excerpta Medica 1972

    Google Scholar 

  • Barker, D., Milburn, A.: Increase in number of intrafusal muscle fibres during the development of muscle spindles in the rat. J. Physiol. (Lond.) 222, 159–160P (1972)

    Google Scholar 

  • Boyd, I. A.: The structure and innervation of the nuclear bag muscle fibre system and the nuclear chain muscle fibre system in mammalian muscle spindles. Phil. Trans. B 245, 81–136 (1962)

    Google Scholar 

  • Boyd, I. A., Gladden, M. H, McWilliam, P. N.: Static and dynamic fusimotor action in isolated cat muscle spindles with intact nerve and blood supply. J. Physiol. (Lond.) 230, 29–30 (1973)

    Google Scholar 

  • Bueker, E. D., Meyers, Ch. E.: The maturity of peripheral nerves at the time of injury as a factor in nerve regeneration. Anat. Rec. 109, 723–744 (1951)

    Google Scholar 

  • Buller, A. J., Eccles, J. C., Eccles, R. M.: Interactions between motoneurones and muscles in respect to the characteristic speeds of their responses. J. Physiol. (Lond.) 150, 417–439 (1960)

    Google Scholar 

  • Burke, R. E., Levine, D. N., Tsairis, P., Zajac, F. E.: Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J. Physiol. (Lond.) 234, 723–748 (1973)

    Google Scholar 

  • Burke, R. E., Tsairis, P.: Anatomy and innervation ratios in motor units of cat gastrocnemius. J. Physiol. (Lond.) 234, 749–765 (1973)

    Google Scholar 

  • Close, R. I.: Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52, 129–197 (1972)

    Google Scholar 

  • Close, R. I., Hoh, J.F.Y.: Effects of nerve cross-union on fast-twitch and slow-graded muscle fibres in the toad. J. Physiol. (Lond.) 198, 103–125 (1968)

    Google Scholar 

  • Diamond, J., Miledi, R.: A study of foetal and new-born rat muscle fibres. J. Physiol. (Lond.) 162, 393–408 (1962)

    Google Scholar 

  • Düring, M.v., Andres, K. H.: Zur Feinstruktur der Muskelspindel von Mammalia. Anat. Anz. 124, 566–573 (1969)

    Google Scholar 

  • Edström, L., Kugelberg, E.: Properties of motor units in the rat anterior tibial muscle. Acta physiol. scand. 73, 543–544 (1968)

    Google Scholar 

  • Engel, W. K., Karpati, G.: Impaired skeletal muscle maturation following neonatal neurectomy. Develop. Biol. 17, 713–723 (1968)

    Google Scholar 

  • Eyzaguirre, C.: Modulation of sensory discharges by efferent spindle excitation. J. Neurophysiol. 21, 465–480 (1958)

    Google Scholar 

  • Eyzaguirre, C.: The electrical activity of mammalian intrafusal fibres. J. Physiol. (Lond.) 150, 169–185 (1960)

    Google Scholar 

  • Gauthier, G. F., Dunn, R. A.: Ultrastructural and cytochemical features of mammalian skeletal muscle fibres following denervation. J. Cell Sci. 12, 525–547 (1973)

    Google Scholar 

  • Gauthier, G. F., Schaeffer, S. F.: Ultrastructural and cytochemical manifestations of protein synthesis in the peripheral sarcoplasm of denervated and newborn skeletal muscle fibres. J. Cell Sci. 14, 113–137 (1974)

    Google Scholar 

  • Ginetsinskii, A. G., Shamarina, N. M.: The tonomotor phenomenon in denervated muscle. Translation number RTS 1710, Department of Scientific and Industrial Research, Lending Library Unit, London. Usp. sovrem. Biol. 15, 283–294 (1942)

    Google Scholar 

  • Gladden, M. H.: Muscle spindle innervation in the intertransverse caudal muscles of the rat. Experientia (Basel) 25, 604–606 (1969)

    Google Scholar 

  • Gray, E. G.: The spindle and extrafusal innervation of a frog muscle. Proc. roy. Soc. B 146, 416–430 (1957)

    Google Scholar 

  • Guth, L.: “Trophic” influences of nerve on muscle. Physiol. Rev. 48, 645–687 (1968)

    Google Scholar 

  • Guth, L.: Fact and artifact in the histochemical procedure for myofibrillar ATPase. Exp. Neurol. 41, 440–450 (1973)

    Google Scholar 

  • Guth, L., Samaha, F. J.: Procedure for the histochemical demonstration of actomyosin ATPase. Exp. Neurol. 28, 365–367 (1970)

    Google Scholar 

  • Gutmann, E.: Development and maintenance of neurotrophic relations between nerve and muscle. In: Growth, of nervous system (G.E.W. Wolstenholme, M. O'Connor, eds.), p. 233–243. London: Churchill 1968

    Google Scholar 

  • Gutmann, E.: Open questions in the study of the “trophic” function of the nerve cell. In: Top. Probl. Psychiat. Neurol. Current Research in Neurosciences (H. T. Wycis, ed.), vol. 10, p. 54–61. Basel: Karger 1970

    Google Scholar 

  • Gutmann, E., Hník, P. (eds.): The effect of use and disuse on neuromuscular functions, p. 1–576. Prague: Publishing House of the Czechoslovak Academy of Sciences 1963

    Google Scholar 

  • Gutmann, E., Melichna, J., Syrový, I.: Developmental changes in contraction time, myosin properties and fibre pattern of fast and slow skeletal muscles. Physiol. bohemoslov. 23, 19–27 (1974)

    Google Scholar 

  • Hanzlíková, V., Schiaffino, S.: Studies on the effect of denervation in developing muscle. III. Diversification of myofibrillar structure and origin of the heterogeneity of muscle fiber types. Z. Zellforsch. 147, 75–85 (1973)

    Google Scholar 

  • Harker, D. W.: The structure and innervation of sheep superior rectus and levator palpebrae extraocular muscles. II. Muscle spindles. Invest. Ophtal. 11, 970–979 (1972)

    Google Scholar 

  • Hennig, G.: Die Nervenendigungen der Rattenmuskelspindel im elektronen- und phasenkontrastmikroskopischen Bild. Z. Zellforsch. 96, 275–294 (1969)

    Google Scholar 

  • Hess A.: Vertebrate slow muscle fibres. Physiol. Rev. 50 40–62 (1970)

    Google Scholar 

  • Hník P.: The increased response of chronically de-efferented rat muscle spindles to stretch. Brain Res. 21 448–451 (1970)

    Google Scholar 

  • Hník P. Jirmanová L., Vyklický, L., Zelená J.: Fast and slow muscles of the chick after nerve cross-union. J. Physiol. (Lond.) 193, 309–325 (1967)

    Google Scholar 

  • Hník, P., Lessler, M. J.: Changes in muscle spindle activity of the chronically de-efferented gastrocnemius of the rat. Pflügers Arch. 341, 155–170 (1973)

    Google Scholar 

  • James, N. T.: The histochemical demonstration of three types of intrafusal fibre in rat muscle spindles. Histochem. J. 3, 457–462 (1971)

    Google Scholar 

  • Jirmanová I., Hník, P., Zelená J.: Implantation of “fast” nerve into slow muscle in young chickens. Physiol. bohemoslov. 20, 199–204 (1971)

    Google Scholar 

  • Jirmanová I., Zelená J.: Ultrastructural transformation of fast chicken muscle fibres induced by nerve cross-union. Z. Zellforsch. 146, 103–121 (1973)

    Google Scholar 

  • Karlsen, K.: The location of motor end plates and the distribution and histological structure of muscle spindles in jaw muscles of the rat. Acta odont. scand. 23, 521–547 (1965)

    Google Scholar 

  • Katz, B.: The efferent regulation of the muscle spindle in the frog. J. exp. Biol. 26, 201–217 (1949)

    Google Scholar 

  • Kidd, G. L.: Excitation of primary muscle spindle endings by β-axon stimulation. Nature (Lond.) 203, 1248–1251 (1964)

    Google Scholar 

  • Kugelberg, E., Edström, L.: Differential histochemical effects of muscle contractions on phosphorylase and glycogen in various types of fibres: Relation to fatigue. J. Neurol. Neurosurg. Psychiat. 31, 415–423 (1968)

    Google Scholar 

  • Landen, D. N.: Electron microscopy of muscle spindles. In: Control and innervation of skeletal muscle (B. L. Andrew, ed.), p. 96–111. Edinburgh-London: Livingstone 1966

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Lentz, T. L.: Development of the neuromuscular junction. III. Degeneration of motor end plate after denervation and maintenance in vitro by nerve explants. J. Cell Biol. 55, 93–103 (1972)

    Google Scholar 

  • Lewis, D. M.: Effect of denervation on the differentiation of twitch muscles in the kitten hind limb. Nature (Lond.) New Biol. 241, 285–286 (1973)

    Google Scholar 

  • Matthews, P.B.C.: The static and dynamic fusimotor fibers. Bull. Swiss Acad. Med. Sci. 27, 235–254 (1971)

    Google Scholar 

  • Matthews, P.B.C.: Mammalian muscle receptors and their central actions, p. 1–630. London: Edward Arnold 1972

    Google Scholar 

  • Matthews, P.B.C., Westbury, D. R.: Some effects of fast and slow motor fibres on muscle spindles of the frog. J. Physiol. (Lond.) 178, 178–192 (1965)

    Google Scholar 

  • Mayr, R.: Untersuchungen an isolierten Muskelspindeln der Ratte nach Cholinesterasedarstellung und Sudanschwarz-Pärbung. Z. Zellforsch. 93, 594–606 (1969)

    Google Scholar 

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

    Google Scholar 

  • Milburn, A.: The development of the muscle spindle in the rat. Ph. D. Thesis, Durham 1973b

  • Miledi, R., Orkand, P.: Effect of a “fast” nerve on “slow” muscle fibres in the frog. Nature (Lond.) 209, 717–718 (1966)

    Google Scholar 

  • Ovalle, W. K.: Pine structure of rat intrafusal muscle fibres. The polar region. J. Cell Biol. 51, 83–103 (1971)

    Google Scholar 

  • Ovalle, W. K.: Motor nerve terminals on rat intrafusal muscle fibres; a correlated light and electron microscopic study. J. Anat. (Lond.) 111, 239–253 (1972)

    Google Scholar 

  • Padykula, H. A., Herman, E.: The specificity of the histochemical method for adenosine triphosphate. J. Histochem. Cytochem. 3, 170–195 (1955)

    Google Scholar 

  • Page, S. G.: Intrafusal muscle fibres in the frog. J. Microscopie 5, 101–104 (1966)

    Google Scholar 

  • Pellegrino, C., Franzini-Armstrong, C.: Recent contributions of electron microscopy to the study of normal and pathological muscle. Int. Rev. exp. Path. 7, 139–226 (1969)

    Google Scholar 

  • Schiaffino, S., Hanzlíková V.: Autophagic degradation of glycogen in skeletal muscles of newborn rat. J. Cell Biol. 52, 41–51 (1972a)

    Google Scholar 

  • Schiaffino, S., Hauzlíková, V.: Studies on the effect of denervation in developing muscle. II. The lysosomal system. J. Ultrastruct. Res. 39, 1–14 (1972b)

    Google Scholar 

  • Schiaffino, S., Settembrini, P.: Studies on the effect of denervation in developing muscle. I. Differentiation of the sarcotubular system. Virchows Arch. Abt. B 4, 345–356 (1970)

    Google Scholar 

  • Shafiq, S. A., Asiedu, S. A., Milhorat, A. T.: Effect of neonatal neurectomy on differentiation of fiber types in rat skeletal muscle. Exp. Neurol. 35, 529–540 (1972)

    Google Scholar 

  • Smith, R. S.: Activity of intrafusal muscle fibres in muscle spindles of Xenopus laevis. Acta physiol. scand. 60, 223–239 (1964a)

    Google Scholar 

  • Smith, R. S.: Contraction in intrafusal muscle fibres of Xenopus laevis following stimulation of their motor nerves. Acta physiol. scand. 62, 195–208 (1964b)

    Google Scholar 

  • Smith, R. S., Ovalle, W. K.: Structure and function of intrafusal muscle fibres. In: Muscle biology (R. G. Cassens, ed.) vol. 1, p. 147–227. New York: Marcel Dekker, Inc. 1972

    Google Scholar 

  • Sterling, R. J.: Extrafusal and intrafusal end-plate morphology in frog muscle (in preparation); quoted from Barker, 1974

  • Tolar, M.: The development of the neuromuscular system in vitro. (In Czech), p. 1–111. Prague: Avicenum 1973

    Google Scholar 

  • Tolar, M., Hanzlíková V., Gutmann, E.: The effect of external factors on development of the chick skeletal muscle tissue in vitro. Physiol. bohemoslov. 23, 182–183 (1974)

    Google Scholar 

  • Tower, S. S.: Atrophy and degeneration in the muscle spindle. Brain 55, 77–89 (1932)

    Google Scholar 

  • Yellin, H.: A histochemical study of muscle spindles and their relationship to extrafusal fibre types in the rat. Amer. J. Anat. 125, 31–46 (1969)

    Google Scholar 

  • Zelená J.: The morphogenetic influence of innervation on the ontogenetic development of muscle spindles. J. Embryol. exp. Morph. 5, 283–292 (1957)

    Google Scholar 

  • Zelená J.: Development, degeneration and regeneration of receptor organs. In: Progress in brain research, vol.13. Amsterdam: Elsevier 1964

    Google Scholar 

  • Zelená J.: The influence of fusimotor innervation upon the development of muscle spindles. Čs. fysiol. 14, 377–378 (1965)

    Google Scholar 

  • Zelená J., Hník, P.: Muscle atrophy in young rats. Physiol. bohemoslov. 6, 193–199 (1957)

    Google Scholar 

  • Zelená J., Jirmanová, I.: Ultrastructure of chicken slow muscle after nerve cross union. Exp. Neurol. 38, 272–285 (1973)

    Google Scholar 

  • Zelená J., Sobotková M.: Absence of muscle spindles in regenerated muscles of the rat. Physiol. bohemoslov. 20, 433–439 (1971)

    Google Scholar 

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

    Google Scholar 

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The authors wish to thank Mrs. M. Sobotková Ing. M. Doubek and Mr. H. Kunz for their skillful technical assistance.

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Zelená, J., Soukup, T. The differentiation of intrafusal fibre types in rat muscle spindles after motor denervation. Cell Tissue Res. 153, 115–136 (1974). https://doi.org/10.1007/BF00225450

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