Transducer Properties and Integrative Mechanisms in the Frog’s Muscle Spindle

  • D. Ottoson
  • G. M. Shepherd
Part of the Handbook of Sensory Physiology book series (SENSORY, volume 1)

Abstract

Since the classical studies by Adrian and Zotterman in 1926, the function of the muscle spindle has attracted a continuously increasing interest. Research in this field has been focused mainly on the reflex functions and the motor regulation of the spindle; comparatively little has been done on the action of the spindle as a mechano-electrical transducer.

Keywords

Permeability Depression Lithium Acetylcholine Stein 

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References

  1. Adrian, E. D., Zotterman, Y.: The impulse produced by sensory nerve endings. Part 2. The response of a single end-organ. J. Physiol. (Lond.) 61, 151–171 (1926).Google Scholar
  2. Albuquerque, E., Chung, S. H., Ottoson, D.: Impulse generation in the isolated muscle spindle under the action of tetrodotoxin. Acta Physiol. Scand. 75, 301–312 (1969)PubMedCrossRefGoogle Scholar
  3. Arvanitaki, A.: Les variations graduées de la polarisation des systèmes excitables. Paris: Hermann 1938.Google Scholar
  4. Barker, D.: The innervation of mammalian skeletal muscle. In: Ciba: Foundation Symp. on Myotatic and Vestibular Mechanisms, pp. 3–15. London: J. & A. Churchill, Ltd. 1967.Google Scholar
  5. Bernhard, C. G., Granit, R., Skoglund, C. R.: The breakdown of accommodation — nerve as model sense-organ. J. Neurophysiol. 5, 55–66 (1942).Google Scholar
  6. Boyd, I. A.: The structure and innervation of the nuclear bag muscle fibre system and the nuclear chain muscle fibre system in mammalian muscle spindle. Phil. Trans. R. Soc. (B) 245, 81–136 (1962).CrossRefGoogle Scholar
  7. Bridgman, C. F., Eldred, E.: Hypothesis for a pressure sensitive mechanism in muscle spindles. Science 143, 481–482 (1964).PubMedCrossRefGoogle Scholar
  8. Brown, M. C., Stein, R. B.: Quantitative studies on the slowly adapting strech receptor of the crayfish. Kybernetik 3, 175–185 (1966).PubMedCrossRefGoogle Scholar
  9. Brzezinski, D. K. Von: Untersuchungen zur Histochemie der Muskelspindeln. II. Mitteilung. Zur Topochemie und Funktion des Spindelraumes und der Spindelkapsel. Acta Histochem. 12, 277–288 (1961).Google Scholar
  10. Burkhardt, D.: Die Erregungsvorgänge sensibler Gangliezellen in Abhängigkeit von der Temperatur. Biol. Zbl. 78, 22–62 (1959).Google Scholar
  11. Cajal, S. R.: Terminaciones en los husos musculares de la rana. Rev. trim. Histol. norm. Patol. no. 1 (1888).Google Scholar
  12. Chapman, R. A.: The repetitive responses of isolated axons from the crab, Carduus maenas. J. exp. Biol. 45, 475–488 (1966).Google Scholar
  13. Davis, H.: Some principles of sensory receptor action. Physiol. Rev. 41, 391–416 (1961).PubMedGoogle Scholar
  14. Diamond, J., Gray, J. A. B., Inman, D. R.: The relation between receptor potentials and the concentration of sodium ions. J. Physiol. (Lond.) 142, 382–394 (1958).Google Scholar
  15. Dowling, J. A.: Discrete potentials in the dark-adapted eye of the crab Limulus. Nature (Lond.) 217, 28–31 (1968).CrossRefGoogle Scholar
  16. Eccles, J. C.: The Physiology of Synapses. Berlin-Heidelberg-New York: Springer 1964.CrossRefGoogle Scholar
  17. Edwards, C.: Changes in the discharge from a muscle spindle produced by electrotonus in the sensory nerve. J. Physiol., (Lond.) 127, 636–640 (1955).Google Scholar
  18. Eldred, E., Granit, R., Merton, P. A.: Supraspinal control of the muscle spindles and its significance. J. Physiol., (Lond.) 122, 498–523 (1953).Google Scholar
  19. Eyzaguirre, C., Kuffler, S. W.: Processes of excitation in the dendrites and in the soma of single isolated sensory nerve cells of the lobster and crayfish. J. Gen. Physiol. 39, 87–119 (1955).PubMedCrossRefGoogle Scholar
  20. Fatt, P., Katz, B.: An analysis of the end-plate potential recorded with an intracellular electrode. J. Physiol., (Lond.) 115, 320–370 (1951).Google Scholar
  21. Fehr, H. U.: Activation by suxamethonium of primary and secondary endings of the same de-efferented muscle spindle during static stretch. J. Physiol., (Lond.) 178, 98–110 (1965).Google Scholar
  22. Goldman, L.: The effects of strech on cable and spike parameters of single nerve fibres; some implications for the theory of impulse propagation. J. Physiol., (Lond.) 175, 425–444 (1964).Google Scholar
  23. Granit, R.: Receptors and sensory perception. New Haven: Yale Univ. Press (1955).Google Scholar
  24. Skoglund, S., Thesleef, S.: Activation of muscle spindles by succinylcholine and decamethonium. The effects of curare. Acta physiol. scand. 28, 134–151 (1953).PubMedCrossRefGoogle Scholar
  25. Gray, J. A. B.: The spindle and extrafusal innervation of a frog muscle. Proc. Roy. Soc. (B) 146, 416–430 (1957).CrossRefGoogle Scholar
  26. — Mechanical into electrical energy in certain mechanoreceptors. Progr. Biophys. Biophys. Chem. 9, 285–324 (1959).Google Scholar
  27. Diamond, J.: Pharmacological properties of sensory receptors and their relation to those of the autonomic nervous system. Br. med. Bull. 13, 185–188 (1957).PubMedGoogle Scholar
  28. Malcolm, J. L.: The excitation of touch receptors in frog’s skin. J. Physiol., (Lond.) 115, 1–15 (1951).Google Scholar
  29. Matthews, P. B. C.: A comparison of the adaption of the Pacinian corpuscle with the accommodation of its own axon. J. Physiol., (Lond.) 114, 454–464 (1951).Google Scholar
  30. Gray, J. A. B., Sato, M.: Properties of the receptor potential in Pacinian corpuscles. J. Physiol., (Lond.) 122, 610–636 (1953).Google Scholar
  31. Haapanen, L. E.: A high-sensitivity capacitance-meter. Electron. Engng. 34, 183–185 (1962).Google Scholar
  32. Henatsch, H. D., Schulte, J. J.: Wirkungsmechanismus von Acetylcholin und Succinyl-cholin auf die Muskelspindeln des Frosches. Pflügers Arch. Ges. Physiol. 265, 440–456 (1959).Google Scholar
  33. Hodgkin, A. L.: The local electric changes associated with repetitive action in a non-medul-lated axon. J. Physiol., (Lond.) 107, 165–181 (1948).Google Scholar
  34. Höglund, G., Lindblom, U.: The discharge in single touch receptors elicited by defined mechanical stimuli. Acta physiol. scand. 52, 108–119 (1961).PubMedCrossRefGoogle Scholar
  35. Husmark, I., Ottoson, D.: Relation between tension and sensory response of the isolated frog muscle spindle during stretch. Acta physiol. scand. In press (1970a).Google Scholar
  36. — — The contribution of mechanical factors to the early adaptation of the spindle response. Acta physiol. scand. In press (1970b).Google Scholar
  37. — — The effect of potassium on adaptation of the muscle spindle. In course of publication (1970c).Google Scholar
  38. Jansen, J. K., Matthews, P. B. C.: The central control of the dynamic response of muscle spindle receptors. J. Physiol. (Lond.) 161, 375–378 (1962).Google Scholar
  39. Rudjord, T.: The silent period during twitch contraction of the soleus of the decerebrate cat. Acta physiol. scand. 59, Suppl. 213, 69–70 (1963).Google Scholar
  40. Karlsson, U., Anderson-Cedergren, E., Ottoson, D.: Cellular organization of the frog muscle spindle as revealed by serial sections for electronmicroscopy. J. Ultrastruct. Res. 14, 1–35 (1966).CrossRefGoogle Scholar
  41. Ottoson, D.: Electronmicroscopical studies on the effect of anisotonic solutions on the muscle spindle. In course of publication (1970).Google Scholar
  42. Katz, B.: Action potentials from a sensory nerve ending. J. Physiol., (Lond.) 111, 248–260 (1950a).Google Scholar
  43. — Depolarization of sensory terminals and the initiation of impulses in the muscle spindle. J. Physiol., (Lond.) 111, 261–282 (1950b).Google Scholar
  44. — The termination of the afferent nerve fibre in the muscle spindle of the frog. Phil. Trans. R. Soc. 243, 221–240 (1961).CrossRefGoogle Scholar
  45. Krnjevic, K., Gelder, N. M. Vav: Tension changes in crayfish stretch receptors. J. Physiol. (Lond.) 159, 310–325 (1961).Google Scholar
  46. Lindblom, U.: The relation between stimulus and discharge in a rapidly adapting touch receptor. Acta physiol. scand. 56, 349–361 (1962).CrossRefGoogle Scholar
  47. — Phasic and static excitability of touch receptors in toad skin. Acta physiol. scand. 59, 410–423 (1963).PubMedCrossRefGoogle Scholar
  48. — Properties of touch receptors in distal glabrous skin of the monkey. J. Neurophysiol. 28, 966–985 (1965).PubMedGoogle Scholar
  49. Lippold, O. C. J., Nicholls, J. G., Redfearn, J. W. T.: Electrical and mechanical factors in the adaption of a mammalian muscle spindle. J. Physiol., (Lond.) 153, 209–217 (1960).Google Scholar
  50. Loewenstein, W. R.: Excitation and changes in adaptation by stretch of mechanoreceptors. J. Physiol., (Lond.) 133, 588–602 (1956).Google Scholar
  51. — Generator processes of repetitive activity in a Pacinian corpuscle. J. gen. Physiol. 41, 825–845 (1958).PubMedCrossRefGoogle Scholar
  52. — On the “specificity” of a sensory receptor. J. Neurophysiol. 24, 150–158 (1961).PubMedGoogle Scholar
  53. Altamirano-Orrego, R.: The refractory state of the generator and propagated potentials in a Pacinian corpuscle. J. gen. Physiol. 41, 805–824 (1958).PubMedCrossRefGoogle Scholar
  54. Mendelson, M.: Components of receptor adaptation in a Pacinian corpuscle. J. Physiol. (Lond.) 177, 377–397 (1965).Google Scholar
  55. Terzuolo, C. A., Washizu, Y.: Separation of transducer and impulse-generating processes in sensory receptors. Science 142, 1180–1181 (1963).PubMedCrossRefGoogle Scholar
  56. Matthews, B. H. C.: The response of a single end organ. J. Physiol., (Lond.) 71, 64–109 (1931).Google Scholar
  57. Matthews, P. B. C.: The response of de-efferented muscle spindle receptors to stretching at different velocities. J. Physiol., (Lond.) 168, 660–678 (1963).Google Scholar
  58. — Muscle spindles and their motor control. Physiol. Rev. 44, 219–288 (1964).PubMedGoogle Scholar
  59. 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
  60. Nishi, K., Sato, M.: Blocking of the impulse and depression of the receptor potential by tetrodotoxin in non-myelinated nerve terminals in Pacinian corpuscles. J. Physiol., (Lond.) 184, 376–386 (1966).Google Scholar
  61. Ottoson, D.: The effect of acetylcholine and related substances on the isolated muscle spindle. Acta physiol. scand. 53, 276–287 (1961).PubMedCrossRefGoogle Scholar
  62. — The effect of sodium deficiency on the response of the isolated muscle spindle. J. Physiol., (Lond.) 171, 109–118 (1964).Google Scholar
  63. — The action of calcium on the frog’s isolated muscle spindle. J. Physiol. (Lond.) 178, 68–79 (1965).Google Scholar
  64. — The effect of osmotic pressure changes on the isolated muscle spindle. Acta physiol. scand. 64, 93–105 (1965).PubMedCrossRefGoogle Scholar
  65. McReykolds, J. S., Shepherd, G. M.: Sensitivity of isolated frog muscle spindle during and after stretching. J. Neurophysiol. 32, 24–34 (1969).PubMedGoogle Scholar
  66. Shepherd, G. M.: Receptor potentials and impulse generation in the isolated spindle during controlled extension. Cold Spr. Harb. Symp. quant. Biol. 30, 105–114 (1965).Google Scholar
  67. — — Changes of length within the frog muscle spindle during stretch as shown by stroboscopic photomicroscopy. Nature (Lond). 220, 912–914 (1968).CrossRefGoogle Scholar
  68. — — Relation of afferent nerve excitability to impulse generation in the frog muscle spindle. Acta physiol. scand. 75, 49–63 (1969).PubMedCrossRefGoogle Scholar
  69. — — Length changes within isolated frog muscle spindle during and after stretch. J. Physiol. (Lond.) 207, 747–759 (1970a).Google Scholar
  70. — — Steps in impulse generation in the isolated muscle spindle. Acta physiol. scand. In press (1970b).Google Scholar
  71. — — Synchronization of activity in afferent nerve branches within the frog’s muscle spindle. In course of publication (1970 c).Google Scholar
  72. — — Transducer characteristics of the muscle spindle as revealed by its receptor potential. In course of publication (1970d).Google Scholar
  73. Overton, E.: Beiträge zur allgemeinen Muskel- und Nervenphysiologie. II. Über die Unent-behrlichkeit von Natrium-(oder Lithium-) Ionen für den Kontraktionsakt des Muskels. Pflügers Arch. ges. Physiol. 92, 346–386 (1902).CrossRefGoogle Scholar
  74. Ozeki, M., Sato, M.: Changes in the membrane potential and the membrane conductance associated with a sustained compression of the nonmyelinated nerve terminal in Pacinian corpuscles. J. Physiol., (Lond.) 180, 186–208 (1965).Google Scholar
  75. Regaud, C., Favre, M.: Les terminaisons nerveuses et les organes nerveux sensitifs de l’appareil locomoteur. Rev. gen. Histol. 1, (1904–05).Google Scholar
  76. Shepherd, G. M., Ottoson, D.: Responses of the isolated muscle spindle to different rates of stretching. Cold Spring Harbor Symp. quant. Biol. 30, 95–103 (1965).PubMedGoogle Scholar
  77. Sherrington, C. S.: On the anatomical constitution of nerves of skeletal muscles, with remarks on recurrent fibres in the ventral spinal nerve-root. J. Physiol. (Lond.) 17, 211–258 (1894).Google Scholar
  78. Smith, C. M., Eldred, E.: Mode of action of succinylcholine on sensory endings of mammalian muscle spindles. J. Pharmacol. 131, 237–242 (1961).Google Scholar
  79. Smith, R. S.: Properties of intrafusal muscle fibres. Nobel Symp. I. Muscular Afferents and Motor Control, pp. 69–80. Stockholm: Almqvist & Wiksell 1966.Google Scholar
  80. Teorell, T.: Excitability phenomena in artificial membranes. Biophys. J. 2, 27–52 (1962).PubMedCrossRefGoogle Scholar
  81. — Electrokinetic considerations of mechanoelectrical transduction. Ann. N. Y. Acad. Sci. 137, 950–966 (1966).PubMedCrossRefGoogle Scholar
  82. Terzuolo, C. A., Washizu, Y.: Relation between stimulus strength, generator potential and impulse frequency in stretch receptor of Crustacea. J. Neurophysiol. 25, 56–66 (1962).PubMedGoogle Scholar
  83. Thurm, U.: Das Receptorpotential einzelner mechano-receptorischer Zellen von Bienen. Z. vergl. Physiol. 48, 131–156 (1964).CrossRefGoogle Scholar
  84. — An insect mechanoreceptor. I. Fine structure and adequate stimulus. Cold Spring. Harbor Symp. quant. Biol. 30, 75–82 (1965).PubMedGoogle Scholar
  85. — An insect mechanooreceptr. II. Receptor potentials. Cold Spring Harbor Symp. quant. Biol. 30, 83–94 (1965).PubMedGoogle Scholar
  86. Tigerstedt, R.: Studien über die mechanische Nervenreizung. Finneschen Litteratur Gesell. Helsingfors 574–659 (1880).Google Scholar
  87. Wendler, L., Burkhardt, D.: Zeitlich abklingende Vorgänge in der Wirkungskette zwischen Reiz und Erregung. Versuche an abdominalen Streckreceptoren dekapoder Krebse. Z. Naturf. 16, 464–469 (1961).Google Scholar
  88. — Über die Wirkungskette zwischen Reiz und Erregung. Versuche an den abdominalen Streckreceptoren des Flußkrebses. Z. vergl. Physiol. 47, 279–315 (1963).CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1971

Authors and Affiliations

  • D. Ottoson
    • 1
  • G. M. Shepherd
    • 2
  1. 1.StockholmSweden
  2. 2.New HavenUSA

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