Summary
Muscle spindles of limb muscles were deefferented in neonatal rats by sectioning ventral roots or by removal of the lumbosacral spinal cord.
Ten to 56 days after the operation, muscle spindles were examined in the medial gastrocnemius, extensor digitorum longus and soleus muscles. The differentiation of muscle spindles was not affected by deefferentation. The number of spindles in the investigated muscles was not reduced. Intrafusal fibres increased in number from two at birth to four per spindle on the average, as in normal muscles. The characteristic ultrastructural distinctions of nuclear bag and nuclear chain fibres developed as under normal conditions. However, intrafusal fibres atrophied slowly after fusimotor denervation, their polar zones becoming reduced in diameter by about 25% in comparison with control fibre diameters. Spindle capsules, on the other hand, increased in size and attained diameters comparable with normal spindles, appearing even somewhat distended.
As intrafusal fibres degenerate after complete denervation at birth (Zelená, 1957), but differentiate in the absence of fusimotor innervation, it can be concluded that sensory nerve terminals induce and support their development. It is assumed that the morphogenetic influence of sensory terminals is mediated by release and uptake of a trophic substance at the synaptic junction. The occurrence of light and dense core vesicles in the sensory terminals and of coated invaginations and vesicles at both the axonal and plasma membrane speak in favour of such a possibility.
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References
Adal, M.N.: The fine structure of the sensory region of cat muscle spindles. J. Ultrastruct. Res. 26, 332–354 (1969)
Banker, B.Q., Girvin, J.P.: The ultrastructural features of the mammalian muscle spindle. J. Neuropath. exp. Neurol. 30, 155–195 (1971)
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
Banker, B.Q., Przybylski, R.J., Van der Meulen, J.P., Victor, M., eds.: Research in muscle development and the muscle spindle. International Congress Series No. 240, p. 1–474. Amsterdam: Excerpta Medica 1972
Barker, D.: The innervation of the muscle spindle. Quart. J. micr. Sci. 89, 143–186 (1948)
Barker, D.: The structure and distribution of muscle receptors. In: Symposium on muscle receptors (D. Barker, ed.), p. 227–240. Hong Kong: Hong Kong University Press 1962
Barker, D., ed.: Symposium on Muscle Receptors, p. 1–292. Hong Kong: Hong Kong University Press 1962
Barker, D., Harker, D., Stacey, M.J., Smith, C.R.: Fusimotor innervation. 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. 227–250. Amsterdam: Excerpta Medica 1972
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)
Barker, D., Stacey, M.J.: Rabbit intrafusal muscle fibres. J. Physiol. (Lond.) 210, 70–72P (1970)
Boyd, I.A.: The diameter and distribution of the nuclear bag and nuclear chain muscle fibres in the muscle spindles of the cat. J. Physiol. (Lond.) 153, 23–24P (1960)
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)
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)
Bunge, R.P., Bunge, M.B., Peterson, E.R.: An electron microscope study of cultured rat spinal cord. J. Cell Biol. 24, 163–191 (1965)
Chin, N.K., Cope, M., Pang, M.: Number and distribution of spindle capsules in seven hindlimb muscles of the cat. In: Symposium on Muscle Receptors (D. Barker, ed.), p. 241–248. Hong Kong: Hong Kong University Press 1962
Clérot, J.C.: Mise en évidence par cytochimie ultrastructurale de l'émission de protéines par le noyau d'auxocytes de batraciens. J. Microscopie 7, 973–992 (1968)
Cooper, S.: Muscle spindles and other muscle receptors. In: Structure and function of muscle (G.H. Bourne, ed.), vol. 1, p. 381–420. New York: Academic Press 1960
Cooper, S., Daniel, P.M.: Muscle spindles in man; their morphology in the lumbricals and the deep muscles of the neck. Brain 86, 563–586 (1963)
Corvaja, N., Marinozzi, V., Pompeiano, O.: Muscle spindles in the lumbrical muscle of the adult cat. Electron microscopic observation and functional considerations. Arch. ital. Biol. 107, 365–543 (1969)
Dhainaut, A.: Etude en microscopie électronique et par autoradiographie à haute résolution des extrusions nucléaires au cours de l'ovogénèse de Nereis pelagica (Annélide polychète). J. Microscopie 9, 99–118 (1970)
Düring, M. v., Andres, K.H.: Zur Feinstruktur der Muskelspindel von Mammalia. Anat. Anz. 124, 566–573 (1969)
Engel, W.K.: The essentiality of histo- and cytochemical studies of skeletal muscle in the investigation of neuromuscular disease. Neurology (Minneap.) 12, 778–794 (1962)
Fukami, Y.: Tonic and phasic muscle spindles in snake. J. Neurophysiol. 33, 28–45 (1970)
Fukami, Y., Hunt, C.C.: Structure of snake muscle spindles. J. Neurophysiol. 33, 9–27 (1970)
Gruner, J.E.: La structure fine du fuseau neuromusculaire humain. Rev. neurol. 104, 490–507 (1961)
Hennig, G.: Die Nervenendigungen der Rattenmuskelspindel im elektronen- und phasenkontrastmikroskopischen Bild. Z. Zellforsch. 96, 275–294 (1969)
Hník, P.: Increased sensory outflow from the de-efferented muscles. Physiol. bohemoslov. 13, 405–410 (1964)
Hník, P.: The increased response of chronically de-efferented rat muscle spindles to stretch. Brain Res. 21, 448–451 (1970)
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)
Hník, P., Zelená, J.: Atypical spindles in reinnervated rat muscles. J. Embryol. exp. Morph. 9, 456–467 (1961)
Landon, D.N.: Electron microscopy of muscle spindles. In: Control and innervation of skeletal muscle (B.L. Andrew, ed.), p. 96–111. Dundee, Scotland: D.C. Thomson and Co., Ltd. 1966
Landon, D.N.: The fine structure of the equatorial regions of developing muscle spindles in the rat. J. Neurocytol. 1, 189–210 (1972)
Le Beux, Y.J.: An ultrastructural study of the neurosecretory cells of the medial vascular prechiasmatic gland, the preoptic recess and the anterior part of the suprachiasmatic area. I. Cytoplasmic inclusions resembling nucleoli. Z. Zellforsch. 114, 404–440 (1971)
MacDonald, R.D., Engel, A.G.: The cytoplasmic body: another structural anomaly of the Z disk. Arch. Neurol. 14, 99–107 (1969)
Marchand, E.R., Eldred, E.: Postnatal increase of intrafusal fibres in the rat muscle spindle. Exp. Neurol. 25, 655–676 (1969)
Matthews, P.B.C.: Muscle spindles and their motor control. Physiol. Rev. 44, 219–288 (1964)
Matthews, P.B.C.: Mammalian muscle receptors and their central actions, p. 1–630. London: Eduard Arnold, Ltd. 1972
Mayr, R.: Zwei elektronenmikroskopisch unterscheidbare Formen sekundärer sensorischer Endigungen in einer Muskelspindel der Ratte. Z. Zellforsch. 110, 97–107 (1970)
Merrillees, N.C.R.: The fine structure of muscle spindles in the lumbrical muscles of the rat. J. biophys. biochem. Cytol. 7, 725–742 (1960)
Milburn, A.: The early development of muscle spindles in the rat. J. Cell Sci. 12, 175–195 (1973)
Nakashima, N., Tamura, Z., Okamoto, S., Goto, H.: Inclusion bodies in a human neuromuscular disorder. Arch. Neurol. 22, 270–278 (1970)
Odor, D. L., Patel, A. N., Pearce, L. A.: Familiar hypokalemic periodic paralysis with permanent myopathy. J. Neuropath. exp. Neurol. 26, 98–114 (1967)
Olmstead, J.M.D.: The results of cutting the seventh cranial nerve in Ameiurus nebulosus. J. exp. Zool. 31, 369–401 (1920)
Ovalle, W.K.: Fine structure of rat intrafusal muscle fibres. The equatorial region. J. Cell Biol. 52, 382–396 (1972)
Parker, G.H.: On the trophic impulse, so-called, its rate and nature. Amer. Naturalist. 66, 147–158 (1932)
Rumpelt, H.-J., Schmalbruch, H.: Zur Morphologie der Bauelemente von Muskelspindeln bei Mensch und Ratte. Z. Zellforsch. 102, 601–630 (1969)
Scalzi, M.A., Price, H.M.: The arrangement and sensory innervation of the intrafusal fibres in the feline muscle spindle. J. Ultrastruct. Res. 36, 375–390 (1971)
Shimizu, N., Ishii, S.: Electron-microscopic observations on nucleolar extrusion in nerve cells of the rat hypothalamus. Z. Zellforsch. 67, 367–372 (1965)
Smith, A. D.: Summing up: Some implications of the neuron as a secreting cell. Phil. Trans. B 261, 423–437 (1971)
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
Swett, J.E., Eldred, E.: Comparison in structure of stretch receptors in medial gastrocnemius and soleus muscles of the cat. Anat. Rec. 137, 461–473 (1960)
Thomson, J. D.: Mechanical characteristics of skeletal muscle undergoing atrophy of denervation. Amer. J. Phys. Med. 34, 606–511 (1955)
Tower, S.: Atrophy and degeneration in the muscle spindle. Brain 55, 77–89 (1932)
Uehara, Y.: Unique sensory endings in rat muscle spindles. Z. Zellforsch. 136, 511–520 (1973)
Zelená, J.: Morphogenetic influence of innervation on the ontogenetic development of muscle spindles. J. Embryol. exp. Morph. 5, 283–292 (1957)
Zelená, J.: Effect of innervation on the development of skeletal muscle. (In Czech, with English and Russian summary), p. 1–102. Prague: Státní zdravotnické nakladatelství, 1959
Zelená, J.: The effects of denervation on muscle development. In: The denervated muscle (E. Gutmann, ed.), p. 103–126, Prague: Publishing House of the Czechoslovak Academy of Sciences 1962
Zelená, J.: Development of muscle receptors after tenotomy. Physiol. bohemoslov. 12, 30–36 (1963)
Zelená, J.: Development, degeneration and regeneration of receptor organs. In: Mechanisms of neural regeneration (M. Singer and J.P. Schadé, eds.), Progress in brain research, vol. 13, p. 175–213. Amsterdam: Elsevier 1964
Zelená, J.: The influence of fusimotor innervation upon the development of muscle spindles. Čs. Fysiol. 14, 377–378 (1965)
Zelená, J., Hník, P.: Muscle atrophy in young rats. Physiol. bohemoslov. 6, 193–199 (1957)
Zelená, J., Hník, P.: Effect of innervation on the development of muscle receptors. In: The effect of use and disuse on neuromuscular functions (E. Gutmann and P. Hník, eds.), p. 95–105. Prague: Publishing House of the Czechoslovak Academy of Sciences 1963
Zelená, J., Sobotková, M.: Absence of muscle spindles in regenerated muscles of the rat. Physiol. bohemoslov. 20, 433–439 (1971)
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The authors wish to thank Mrs. M. Sobotková, Dr. Z. Lišková, Mr. H. Kunz and Ing. M. Doubek for their skillful technical assistance.
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Zelená, J., Soukup, T. Development of muscle spindles deprived of fusimotor innervation. Z.Zellforsch 144, 435–452 (1973). https://doi.org/10.1007/BF00307586
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DOI: https://doi.org/10.1007/BF00307586