Specificity of Nerve-Muscle Interactions

  • Douglas M. Fambrough
Part of the Current Topics in Neurobiology book series (CTNB)


Developmental neurobiology today can be described as the field of scientific research in which investigators are attempting to explain the organization of extremely complex adult nervous systems in terms of a minimum number of “simple” mechanisms of cellular interaction and the timing of these interactions during development. Even the briefest description of a nervous system will acknowledge the proper connectivity of functional elements. Within a species the organization of the nervous system is extremely similar and not very different from that of any closely related species. This uniformity of organization is ensured by cellular mechanisms that determine the establishment and maintenance of proper connections. In this chapter, I will examine the evidence related to mechanisms of interaction between motoneurons and skeletal muscle fibers in the vertebrates and will discuss what inferences and deductions might be made from the evidence concerning the specifity of such interactions.


Skeletal Muscle Acetylcholine Receptor Neuromuscular Junction Skeletal Muscle Fiber Muscle Fiber Type 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Aitkin, J. T., 1965, Problems of reinnervation of muscle, in: Degeneration Pattern in the Nervous System (M. Singer and J. P. Schade, eds.), Progr. Brain Res. 14: 232.Google Scholar
  2. Albuquerque, E. X., Barnard, E. A., Porter, C. W. and Warnick, J. E., 1974, The density of acetylcholine receptors and their sensitivity in the post-synaptic membrane of muscle endplates, Proc. Natl. Acad. Sci. LISA 71: 2818.Google Scholar
  3. Anderson, M. J., and Cohen, M. S., 1974, Fluorescent staining of acetylcholine receptors in vertebrate skeletal muscle, J. Physiol. (London) 237: 385.Google Scholar
  4. Andersson-Cedergren, E., 1959, Ultrastructure of motor endplate and sarcoplasmic components of mouse skeletal muscle fiber as revealed by three-dimensional reconstruction from serial section, J. Ultrastruct. Res. (Suppl. 1 ).Google Scholar
  5. Atsumi, S., 1971a, The histogenesis of motor neurons with special reference to the correlation of their endplate formation. I. The development of endplates in the intercostal muscle in the chick embryo, Acta Anat. 80: 161.Google Scholar
  6. Atsumi, S., 1971b, The histogensis of motor neurons with special reference to the correlation of their endplate formation. III. The development of motor neurons innervating the intercostal muscle in the chick embryo, Acta Anat. 80: 504.Google Scholar
  7. Axelsson, J., and Thesleff, S., 1959, A study of supersensitivity in denervated mammalian skeletal muscle, J. Physiol. (London) 147: 158.Google Scholar
  8. Bagust, J., Lewis, D. M., and Westerman, R. A., 1973, Polyneuronal innervation of kitten skeletal musde, J. Physiol. (London) 229: 241.Google Scholar
  9. Barker, D., and Ip, M. C., 1966, Sprouting and degeneration of mammalian motor axons in normal and deafferented skeletal muscle, Proc. Roy Soc. London Ser. B 163: 538.Google Scholar
  10. Bauer, W. C., Blumberg, J. M., and Zacks, S. I., 1962, Short and long-term unitrastructural changes in denervated mouse endplates, in: Proceedings of the IV International Congress of Neuropathology ( Bauer, W. C., Blumberg, J. M., and Zacks, S. I., ed.), pp. 16–18, Stuttgart.Google Scholar
  11. Bennett, M. R., and Pettigrew, A. G., 1974a, The formation of synapses in striated muscle during development, J. Physiol. (London) 241: 515.Google Scholar
  12. Bennett, M. R., and Pettigrew, A. G., 1974b, The formation of synapses in reinnervated and cross-reinnervated striated muscle during development, J. Physiol. (London) 241: 547.Google Scholar
  13. Bennett, M. R., McLachlan, E. M., and Taylor, R. S., 1973a, The formation of synapses in reinnervated mammalian striated muscle, J. Physiol. (London) 233: 481.Google Scholar
  14. Bennett, M. R., McLachlan, E. M., and Taylor, R. S., 1973b, The formation of synapses in mammalian striated muscle reinnervated with autonomic pregangliomic nerves, J. Physiol. (London) 233: 501.Google Scholar
  15. Bennett, M. R., Pettigrew, A. G., and Taylor, R. S., 1973c, The formation of synapses in reinnervated and cross-reinnervated adult avian muscle, J. Physiol. (London) 230: 331.Google Scholar
  16. Bernstein, J. J., and Guth, L., 1961, Nonselectivity in establishment of neuromuscular connections following nerve regeneration in the rat, Exp. Neurol. 4: 262.Google Scholar
  17. Betz, W., and Sakmann, B., 1971, “Disjunction” of frog neuromuscular synapses by treatment with proteolytic enzymes, Nature (London) New Biol. 232:94.Google Scholar
  18. Betz, W., and Sakmann, B., 1973, Effects of proteolytic enzymes on function and structure of frog neuromuscular junctions, J. Physiol. (London). 230: 673.Google Scholar
  19. Birks, R., Huxley, H. E., and Katz, B., 1960, The fine structure of the neuromuscular junction of the frog, J. Physiol. (London) 150: 134.Google Scholar
  20. Bone, Q., 1964, Patterns of muscular innervation in the lower chordates, Int. Rev. Neurobiol. 6: 99.Google Scholar
  21. Bourgeois, J.-P., Ryter, A., Menez, A., Fromageot, P., Bouquet, P., and Changeux, J.-P., 1972, Localization of the cholinergic receptor protein in Electrophorus electroplax by high resolution autoradiography, FEBS Lett. 25: 127.Google Scholar
  22. Brown, M. C., and Matthews, P. B. C., 1960, An investigation into the possible existence of polyneuronal innervation of individual skeletal muscle fibers in certain hind-limb muscles of the cat, J. Physiol. (London) 151: 436.Google Scholar
  23. Burke, R. E., and Tsairis, P., 1973, Anatomy and innervation ratios in motor units of cat gastrocnemius, J. Physiol. (London) 234: 749.Google Scholar
  24. Burke, R. E., Levine, D. N., Tsairis, P., and Zajac, F. E., 1973, Physiological types and histochemical profiles in motor units of the cat gastrocnemius, J. Physiol. (London) 234: 723.Google Scholar
  25. Cass, D. T., Sutton, T. J., and Mark, R. F., 1973, Competition between nerves for functional connections with axolotl muscles, Nature (London) 243: 201.Google Scholar
  26. Close, R. I., 1972, Dynamic properties of mammalian skeletal muscles, 1972, Physiol. Rev. 52: 129.Google Scholar
  27. Close, R. I., and Hoh, J. F. Y., 1968, Effects of nerve cross-union on fast-twitch and slow-graded muscle fibers in the toad, J. Physiol. (London) 198: 103.Google Scholar
  28. Cöers, C., 1969, Structure and organization of the myoneural junction, Int. Rev. Cytol. 22: 239.Google Scholar
  29. Cohen, M. W., 1973, The development of neuromuscular connexions in the presence of Dtubocurarine, Brain Res. 41: 457.Google Scholar
  30. Couteaux, R., 1960, Motor endplate structure, in: Structure and Function of Muscle, Vol. 1 ( G. H. Boume, ed.), pp. 337–380, Academic Press, New York.Google Scholar
  31. Couteaux, R., 1963, The differentiation of synaptic areas, Proc. R. Soc. London Ser. B 158: 457.Google Scholar
  32. Couteaux, R., and Pécot-Dechavassine, M., 1970, Vesicules synaptiques et poches au niveau des “zones actives” de la junction neuromusculaire, C. R. Acad. Sci. 271: 2346.Google Scholar
  33. Cowan, W. M., and Wenger, E., 1968, The development of the nucleus of origin of centrifugal fibers to the retina in the chick, J. Comp. Neurol. 133: 207.Google Scholar
  34. Crain, S. M., and Peterson, E. R., 1971, Development of paired explants of fetal spinal cord and adult skeletal muscle during chronic exposure to curare and hemicholinium, In Vitro 6: 373.Google Scholar
  35. Crossland, W. J., Cowan, W. M., Rodgers, L. A., and Kelley, J. P., 1974, The specification of the retina—tectal projection in the chick, J. Comp. Neurol. 155: 127.Google Scholar
  36. Csillik, B., 1965, Functional Structure of the Post-synaptic Membrane in the Myoneural Junction, Akademiai Kiado, Budapest.Google Scholar
  37. Daniels, M. P., and Vogel, Z., 1975, Immunoperoxidase staining of a-bungarotoxin binding sites in muscle endplates shows distribution of acetylcholine receptors, Nature (London) 254: 339.Google Scholar
  38. Dennis, M., 1975, Physiological properties of junctions between nerve and muscle during salamander limb regeneration, J. Physiol. (London) 244: 683.Google Scholar
  39. Dennis, M. J., and Miledi, R., 1974, Non-transmitting neuromuscular junctions during an early stage of end-plate reinnervation, J. Physiol. (London) 239: 553.Google Scholar
  40. Diamond, J., and Miledi, R., 1962, A study of foetal and new-born rat muscle fibers, J. Physiol. (London) 162: 393.Google Scholar
  41. Dreyer, F., Peper, K., Akert, K., Sandri, C., and Moor, H., 1973, Ultrastructure of the “active zone” in the frog neuromuscular junction, Brain Res. 62: 373.Google Scholar
  42. Dunlap, D. G., 1966, The development of the musculature of the hindlimb in the frog, Rana pipiens, J. Morphol. 119: 241.Google Scholar
  43. Edds, M. V., 1955, Collateral regeneration in partially reinnervated muscles of the rat, J. Exp. Zool. 129: 225.Google Scholar
  44. Elsberg, C. A., 1917, Experiments on motor nerve regeneration and the direct neurotization of paralyzed muscles by their own and foreign nerves, Science 45: 318.Google Scholar
  45. Elul, R., Miledi, R., and Stefani, E., 1968, Neurotrophic control of contracture in slow muscle fibers, Nature (London) 217: 1274.Google Scholar
  46. Eränkö, O., and Teräväinen, H., 1967, Cholinesterases and eserine-resistant carboxylic esterases in degenerating and regenerating motor endplates of the rat, J. Neurochem. 14: 947.Google Scholar
  47. Evans, R. H., 1974, The entry of calcium into the innervated region of the mouse diaphragm muscle, J. Physiol. (London) 240: 517.Google Scholar
  48. Fambrough, D., and Rash, J. E., 1971, Development of acetylcholine sensitivity during myogenesis, Deb. Biol. 26: 55.Google Scholar
  49. Feng, T. P., Wu, W. Y., and Yang, F. Y., 1965, Selective reinnervation of a “slow” or “fast” muscle by its original motor supply during regeneration of a mixed nerve, Sci. Sinica 14: 1717.Google Scholar
  50. Fertuck, H. C., and Salpeter, M. M., 1974, Localization of acetylcholine receptor by 125Ilabeled a-bungarotoxin binding at mouse motor end-plates, Proc. Natl. Acad. Sci. USA 71: 1376.Google Scholar
  51. Filogamo, G., and Gabella, G., 1967, Cholinsterase behavior in the denervated and reinnervated muscles, Acta Anat. 63: 199.Google Scholar
  52. Fischbach, G. D., 1972, Synapse formation between dissociated nerve and muscle cells in low density cell cultures, Dev. Biol. 28: 407.Google Scholar
  53. Fischman, D. A., 1970, The synthesis and assembly of myofibrils in embryonic muscle, Curr. Top. Dev. Biol. 5: 235.Google Scholar
  54. Fluck, R. A., and Strohman, R. C., 1973, Acetylcholinesterase activity in developing skeletal muscle cells in vitro, Dev. Biol. 33: 417.Google Scholar
  55. Frank, E., Jansen, J. K. S., Lomo, T., and Westgaard, R. H., 1974, Effect of foreign innervation on the reinnervation of muscle by its original nerve, J. Physiol. (London) 240: 24 P.Google Scholar
  56. Fukuda, J., 1974, Chloride spike: A third type of action potential in tissue-cultured skeletal muscle cells from chick, Science 185: 76.Google Scholar
  57. Giller, E. L., Schrier, B. K., Shainberg, A., Fisk, H. R., and Nelson, P. G., 1973, Choline acetyltransferase activity is increased in combined cultures of spinal cord and muscle cells from mice, Science 182: 588.Google Scholar
  58. Gonzenbach, H. R., and Waser, P. G., 1973, Electron microscopic studies of degeneration and regeneration of rat neuromuscular junctions, Brain Res. 63: 167.Google Scholar
  59. Goodwin, B. C., and Sizer, I. W., 1965, Effects of spinal cord and substrate on acetylcholinesterase in chick embryonic skeletal muscle, Dev. Biol. 11: 136.Google Scholar
  60. Gordon, T., and Vrbova, G., 1974, Synapse formation during development (abst), XXVI International Congress of Physiological Sciences, Jerusalem Satellite Symposium “Mechanisms of Synaptic Action,” p. 21.Google Scholar
  61. Grimm, L., 1971, An evaluation of myotopic respecification in axolotls, J. Exp. Zool. 178: 479.Google Scholar
  62. Guth, L., 1956, Regeneration in the mammalian peripheral nervous system, Physiol. Rev. 36: 441.Google Scholar
  63. Guth, L., 1968, “Trophic” influences of nerve on muscle, Physiol. Rev. 48:645.Google Scholar
  64. Guth, L., and Brown, W. C., 1965a, The sequence of changes in cholinesterase activity during reinnervation of muscle, Exp. Neurol. 12: 329.Google Scholar
  65. Guth, L., and Brown, W. C., 1965b, Changes in cholinesterase activity following partial denervation, collateral reinnervation, and hyperneurotization of muscle, Exp. Neurol. 13: 198.Google Scholar
  66. Guth, L., and Frank, K., 1959, Restoration of diaphragmatic function following vagophrenic anastomosis in the rat, Exp. Neurol. 1: 1.Google Scholar
  67. Guth, L., and Samaha, F. J., 1969, Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle, Exp. Neurol. 25: 138.Google Scholar
  68. Guth, L., Zalewski, A. A., and Brown, W. C., 1966, Quantitative changes in cholinesterase activity of denervated sole plate following implantation of nerve into muscle, Exp. Neurol. 16: 136.Google Scholar
  69. Gutmann, E., and Young, J. Z., 1944, The reinnervation of muscle after various periods of atrophy, J. Anat. 78: 15.Google Scholar
  70. Gutmann, E., Hanzlikova, V., and Holeckova, E., 1969, Development of fast and slow muscles of the chicken in vivo and their latent period in tissue culture, Exp. Cell Res. 56: 33.Google Scholar
  71. Hall, Z. W., and Kelly, R. B., 1971, Enzymatic detachment of endplate acetylcholinesterase from muscle, Nature (London) New Biol. 232: 62.Google Scholar
  72. Hamburger, V., 1946, Isolation of the brachial segments of the spinal cord of the chick embryo by means of tantalum foil blocks, J. Exp. Zool. 103: 113.Google Scholar
  73. Hamburger, V., 1952, Development of the nervous system, Ann. N.Y. Acad. Sci. 55: 117.Google Scholar
  74. Harris, A. J., Heinemann, S., Schubert, D., and Tarakis, H., 1971, Trophic interaction between cloned tissue culture lines of nerve and muscle, Nature (London) 231: 296.Google Scholar
  75. Harris, J. B., and Marshall, M. W., 1973, Tetrodotoxin-resistant action potentials in newborn rat muscle, Nature (London) New Biol. 243: 191Google Scholar
  76. Harris, J. B., Marshall, M. W., and Wilson, P., 1973, A physiological study of chick myotubes grown in tissue culture, J. Physiol. (London) 229: 751.Google Scholar
  77. Harrisôn, R. G., 1904, An experimental study of the relation of the nervous system to the development of musculature in the embryo of the frog, Am. J. Anat. 3: 197.Google Scholar
  78. Harrison, R. G., 1910, The outgrowth of the nerve fibers as a mode of protoplasmic movement, J. Exp. Zool. 9: 787.Google Scholar
  79. Hartzell, H. C., and Fambrough, D. M., 1972, Acetylcholine receptors: Distribution and extrajunctional density in rat diaphragm after denervation correlated with acetylcholine sensitivity, J. Gen. Physiol. 60: 248.Google Scholar
  80. Hess, A., 1970, Vertebrate slow muscle fibers, Physiol. Rev. 50: 40.Google Scholar
  81. Heuser, J. E., and Reese, T. S., 1973, Evidence for recycling of synaptic vesicle membrane during transmitter release at frog neuromuscular junction, J. Cell Biol. 47: 315.Google Scholar
  82. Heuser, J. E., Reese, T. S., and Landis, D. M. D., 1974, Functional changes in frog neuromuscular junction studied with freeze-fracture J. Neurocytol. 3: 108.Google Scholar
  83. Hirano, H., 1967, Ultrastructural study on the morphogenesis of the neuromuscular junction in the skeletal muscle of the chick, Z. Zellforsch. 79: 198.Google Scholar
  84. Hnik, P., Jirmanova, I., Vyklicky, L., and Zelena, J., 1967, Fast and slow muscles of the chick after nerve cross-union, J. Physiol. (London) 193: 309.Google Scholar
  85. Hoh, J. F. Y., 1971, Selective reinnervation of fast-twitch and slow-graded muscle fibers in the toad, Exp. Neurol. 30: 263.Google Scholar
  86. Hubbard, J. I., 1973, Microphysiology of vertebrate neuromuscular transmission, Physiol. Rev. 53: 674.Google Scholar
  87. Hughes, A. F. W., 1965, A quantitative study of the development of the nerves in the hindlimb of Eleutherodactylus martinicensis, J. Embryol. Exp. Morphol. 13: 9.Google Scholar
  88. Hughes, A., 1968, Aspects of Neural Ontogeny, Academic Press, New York.Google Scholar
  89. Hughes, A. F. W., and Prestige, M. C., 1967, Development of behavior in the hindlimb of Xenopus laevis, J. Zool. 152: 347.Google Scholar
  90. Hunt, C. C., and Kuffler, S. W., 1954, Motor innervation of skeletal muscle: Multiple innervation of individual muscle fibers and motor unit function, J. Physiol. (London) 126: 293.Google Scholar
  91. Iwayama, T., 1969, Relation of regenerating nerve terminals to original end-plates, Nature (London) 229: 81.Google Scholar
  92. Jansen, J. K. S., Lomo, T., Nicolaysen, K., and Westgaard, R., 1973, Hyperinnervation of skeletal muscle fibers: Dependence of muscle activity, Science 181: 559.Google Scholar
  93. Jirmanova, I., and Thesleff, S., 1972, Ultrastructural study of experimental muscle degeneration and regeneration in the adult rat, Z. Zellforsch. Microsk. Anat. 131: 77.Google Scholar
  94. Jirmanova, I., Hnik, P., and Zelena, J., 1971, Implantation of “fast” nerve into slow muscle in young chiçkens, Physiol. Bohemoslov. 20: 199.Google Scholar
  95. Katz, B., and Miledi, R., 1964, The development of acetylcholine sensitivity in nerve-free segments of skeletal muscle, J. Physiol. (London) 170: 389.Google Scholar
  96. Kelly, A. M., and Zacks, S. I., 1969, The fine structure of motor endplate morphogenesis, J. Cell Biol. 42: 154.Google Scholar
  97. Kidokoro, Y., 1973, Development of action potentials in a clonal rat skeletal muscle cell line, Nature (London) New Biol. 241: 158.Google Scholar
  98. Koenig, J., 1963, Innervation motrice experimentale d’une portion de muscle strié nor- malement depouvrée de plaques motrices chez le rat, C. R. Acad. Sci. 256: 2918.Google Scholar
  99. Koening, J., and Pecot-Dechavassine, M., 1971, Relation between appearance of miniature endplate potentials and ultrastructure of reinnervating or newly formed endplates in rats, Brain Res. 27: 43.Google Scholar
  100. Kuno, M., Miyata, Y., and Munoz-martinez, E. J., 1974, Properties of fast and slow alpha motoneurons following motor reinnervation, J. Physiol. (London) 242: 273.Google Scholar
  101. Landmesser, L., 1971, Contractile and electrical responses of vagus-innervated frog sartorius muscles, J. Physiol. (London) 213: 707.Google Scholar
  102. Landmesser, L., 1972, Pharmacological properties, cholinesterase activity and anatomy of nerve-muscle junctions in vagus-innervated frog sartorius, J. Physiol. (London) 220: 243.Google Scholar
  103. Langley, J. N., and Anderson, H. K., 1904, The union of different kinds of nerve fibers, J. Physiol. (London) 31: 365.Google Scholar
  104. Lentz, T. L., 1969, Development of the neuromuscular junction. I. Cytological and cytochemical studies on the neuromuscular junction of differentiating muscle in the regenerating limb of the newt Triturus, J. Cell Biol. 42: 431.Google Scholar
  105. Letinsky, M. S., 1974, The development of nerve-muscle junctions in Rana catesbeiana tadpoles, Dev. Biol. 40: 129.Google Scholar
  106. Levi-Montalcini, R., 1950, The origin and development of the visceral system in the spinal cord of the chick embryo, J. Morphol. 86: 253.Google Scholar
  107. Lewis, P. R., and Hughes, A. F. W., 1960, Patterns of myoneural junctions and cholinesterase activity in the muscles of tadpoles of Xenopus laevis, Q. J. Microsc. Sci. 101: 55.Google Scholar
  108. Liu, H.-C., and Maneely, R. B., 1968, The development of motor endplates in the embryonic and regenerative tail of Hemidactylus bowringi (Gray), Acta Anat. 71: 249.Google Scholar
  109. Luco, C. F., and Luco, J. V., 1971, Sympathetic effects on fibrillary activity of denervated striated muscles, J. Neurophysiol. 34: 1066.Google Scholar
  110. Lüllmann-Rauch, R., 1971, The regeneration of neuromuscular junctions during spontaneous reinnervation of the rat diaphragm, Z. Zellforsch. 121: 593.Google Scholar
  111. Mackay, B., and Harrop, T. J., 1969, An experimental study of the longitudinal growth of skeletal muscle in the rat, Acta anat. 72: 38.Google Scholar
  112. Mark, R. B., 1969, Matching muscles and motoneurons: A review of some experiments on motor nerve regeneration, Brain Res. 14: 245.Google Scholar
  113. Mark, R. F., 1970, Chemospecific synaptic repression as a possible memory store, Nature (London) 225: 178.Google Scholar
  114. Mark, R., 1974, Memory and Nerve Cell Connections, Clarendon Press, Oxford.Google Scholar
  115. Mark, R. F., and Marotte, L. R., 1972, The mechanism of selective reinnervation of fish eye muscles. III. Functional electrophysiological and anatomical analysis of recovery from section of the IIIrd and IVth nerves, Brain Res. 46: 131.Google Scholar
  116. Mark, R., Marotte, L., and Johnstone, J., 1970, Reinnervated eye muscles do not respond to impulses in foreign nerves, Science 170: 193.Google Scholar
  117. Mark, R. F., Marotte, L. R., and Mart, P. E., 1972, The mechanism of selective reinnervation of fish eye muscles. IV. Identification of repressed synapses, Brain Res. 46: 149.Google Scholar
  118. Marotte, L. R., and Mark, F. F., 1970a, The mechanisms of selective reinnervation of fish eye muscle. I. Evidence from muscle function during recovery, Brain Res. 19: 41.Google Scholar
  119. Marotte, L. R., and Mark, R. F., 1970b, The mechanism of selective reinnervation of fish eye muscle. II. Evidence from electron microscopy of nerve endings, Brain Res. 19: 53.Google Scholar
  120. McLachlan, E. M., 1974, The formation of synapses in mammalian sympathetic ganglia reinnervated with pre-ganglionic or somatic nerves, J. Physiol. (London) 237: 217.Google Scholar
  121. Mendez, J., Aranda, L. C., and Luco, J. V., 1970, Antifibrillary effect of adrenergic fibers on denervated striated muscles, J. Neurophysiol. 33: 882.Google Scholar
  122. Miledi, R., 1960, Properties of regenerating neuromuscular synapses in the frog, J. Physiol. (London) 154: 190.Google Scholar
  123. Miledi, R., 1962, Induced innervation of endplate free muscle segments, Nature (London) 193: 281.Google Scholar
  124. Miledi, R., 1963, Formation of extra nerve-muscle junctions in innervated muscle, Nature (London) 199: 1191.Google Scholar
  125. Miledi, R., and Slater, C. R., 1968, Electrophysiology and electron microscopy of rat neuromuscular junctions after nerve degeneration, Proc. R. Soc. London Ser. B 169: 289.Google Scholar
  126. Miledi, R., and Slater, C. R., 1970, On the degeneration of rat neuromuscular junctions after nerve section, J. Physiol. (London) 207: 507.Google Scholar
  127. Miledi, R., and Stefani, E., 1969, Non-selective reinnervation of slow and fast muscle fibers in the rat, Nature (London) 222: 569.Google Scholar
  128. Mumenthaler, M., and Engel, W. K., 1961, Cytological localization of cholinesterase in developing chick embryo skeletal muscle, Acta Anat. 47: 274.Google Scholar
  129. Nelson, P. G., 1975, Nerve and muscle cells in culture, Physiol. Rev. 55: 1.Google Scholar
  130. Nickel, E., and Waser, P. G., 1968, Electronenmikroskopische Untersuchungen am Diaphragma der Maus nach einseitiger Phrenikotomie, Z. Zellforsch. 88: 278.Google Scholar
  131. Obata, K., 1974, Transmitter sensitivities of some nerves and muscle cells in culture, Brain Res. 73: 71.Google Scholar
  132. Oh, T. H., Johnson, D. D., and Kim, S. U., 1972, Neurotrophic effect on isolated chick embryo muscle in culture, Science 178: 1298.Google Scholar
  133. Patterson, B., and Prives, J., 1973, Appearance of acetylcholine receptor in differentiating cultures of embryonic chick breast muscle, J. Cell Biol. 59: 241.Google Scholar
  134. Pecot-Dechavassine, M., 1968, Course of the activity of cholinesterases and their functional capacity at the neuromuscular and musculotendinous junctions in the frog after motor nerve section, Arch. Int. Pharmacodyn. 176: 118.Google Scholar
  135. Peper, K., Dreyer, F., Sandri, C., Akert, K., and Moor, H., 1974, Structure and ultrastructure of the frog motor endplate, Cell Tissue Res. 149: 437.Google Scholar
  136. Peterson, E. R., and Crain, S. M., 1972, Regeneration and innervation in cultures of mammalian skeletal muscle coupled with fetal rodent spinal cord, Exp. Neural. 36: 136.Google Scholar
  137. Piatt, J., 1940, Nerve-muscle specificity in Amblystoma, studied by means of heterotopic cord grafts, J. Exp. Zool. 85: 211.Google Scholar
  138. Prestige, M. C., 1967, The control of cell number in the lumbar spinal ganglion during the development of Xenopus laevis tadpole, J. Embryol. Exp. Morphol. 17: 453.Google Scholar
  139. Prestige, M.C., and Wilson, M. A., 1972, Loss of ventral roots during development, Brain Res. 41: 467.Google Scholar
  140. Prives, J. M., and Patterson, B. M., 1974, Differentiation of cell membranes in cultures of embryonic chick breast muscle, Proc. Natl. Acad. Sci. 71: 3208.Google Scholar
  141. Rash, J. E., and Ellisman, M. H., 1974, Studies on excitable membranes. I. Macromolecular specializations at the neuromuscular junction and the nonjunctional sarcoplasm, J. Cell Biol. 63: 567.Google Scholar
  142. Rash, J. E., Ellisman, M. H., Staehelin, L. A., and Porter, K. R., 1975, Molecular specializations of excitable membranes in normal, chronically denervated and dystrophic muscle fibers, in: Exploratory Concepts in Muscular Dystrophy II: Proceedings of an International Conference, Carefree, Arizona, October 15–19, 1973, Exerpta Medica, Amsterdam.Google Scholar
  143. Redfern, P. A., 1970, Neuromuscular transmission in new-born rats, J. Physiol. (London) 209: 701.Google Scholar
  144. Redfern, P., and Thesleff, S., 1971, Action potential generation in denervated rat skeletal muscle. II. The action of tetrodotoxin, Acta Physiol. Scand. 82: 70.Google Scholar
  145. Reger, J. F., 1959, Studies on the fine structure of normal and denervated neuromuscular junctions from mouse gastrocnemius, J. Ultrastruct. Res. 2: 269.Google Scholar
  146. Reier, P. J., and Hughes, A., 1972, Evidence for spontaneous axon degeneration during peripheral nerve maturation, Am. J. Anat. 135: 147.Google Scholar
  147. Robbins, N., and Yonezawa, T., 1971, Physiological studies during formation and development of rat neuromuscular junctions in tissue culture, J. Gen. Physiol. 58: 467.Google Scholar
  148. Romanul, C. A., and Van der Meulen, J. P., 1967, Slow and fast muscles after crossinnervation: Enzymatic and physiological changes, Neurology 17: 387.Google Scholar
  149. Rosenbluth, J., 1974, Structure of amphibian motor endplate: Evidence for a granular component projecting from the outer surface of the receptive membrane, J. Cell Biol. 62: 755.Google Scholar
  150. Saito, A., and Zacks, S. I., 1969, Fine structure observations of denervation and reinnervation of neuromuscular junctions in mouse foot muscle, J. Bone Jt. Surg. 51A: 1163.Google Scholar
  151. Salpeter, M. M., 1967, Electron microscope autoradiography as a quantitative tool in enzyme cytochemistry. I. The distribution of acetylcholinesterase at motor endplates of a vertebrate twitch muscle, J. Cell Biol. 32: 379.Google Scholar
  152. Sandbank, U., and Bubis, J. J., 1974, The Morphology of Motor Endplates, Brain Information Service, University of California, Los Angeles.Google Scholar
  153. Scott, S. A., 1975, Persistence of foreign innervation on reinnervated goldfish extraocular muscles, Science 189: 644.Google Scholar
  154. Sonesson, B., and Thesleff, S., 1968, Cholinesterase activity after DFP application in botulinum poisoned, surgically denervated or normally innervated rat skeletal muscles, Life Sci. 7: 411.Google Scholar
  155. Sperry, R. W., 1945, The problem of central nervous reorganization after nerve regeneration and muscle transposition, Q. Rev. Biol. 20: 311.Google Scholar
  156. Steinbach, J. H., Harris, A. J., Patrick, J., Schubert, D., and Heinemann, S., 1973, Nerve-muscle interaction in vitro: Role of acetylcholine, J. Gen. Physiol. 62: 255.Google Scholar
  157. Stefani, E., and Schmidt, H., 1972, Early stage of reinnervation of frog slow muscle fibers, Pfluegers Arch. 336: 271.Google Scholar
  158. Sytkowski, A. J., Vogel, Z., and Nirenberg, M. W., 1973, Development of acetylcholine receptor clusters on cultured musde cells, Proc. Natl. Acad. Sci. USA 70: 270.Google Scholar
  159. Taylor, A. C., 1943, Development of the innervation pattern in the limb bud of the frog, Anat. Rec. 87: 379.Google Scholar
  160. Tennyson, V. M., Brzin, M., and Kremzner, L. T., 1973, Acetylcholinesterase activity in the myotube and muscle satellite cell of the fetal rabbit: An electron microscopiccytochemical and biochemical study, J. Histochem. Cytochem. 21: 634.Google Scholar
  161. Teräväinen, H., 1968, Development of the myoneural junction in the rat, Z. Zellforsch. 87: 249.Google Scholar
  162. Thesleff, S., 1960, Supersensitivity of skeletal muscle produced by botulinum toxin, J. Physiol. (London) 151: 598.Google Scholar
  163. Tiegs, D. N., 1953, Innervation of voluntary muscle, Physiol. Rev. 33: 90.Google Scholar
  164. Tonge, D. A., 1974a, Synaptic function in experimental innervated muscle in the mouse, J. Physiol. (London) 239: 96 P.Google Scholar
  165. Tonge, D. A., 1974b, Reinnervation of skeletal muscle in the mouse, J. Physiol. (London) 236: 22 P.Google Scholar
  166. Tuffery, A. R., 1971, Growth and degeneration of motor endplates in normal cat hind limb muscles, J. Anat. 110: 221.Google Scholar
  167. Vera, C. L., and Luco, J. V., 1967, Reinnervation of smooth and striated muscle by sensory nerve fibers, J. Neurophysiol. 30: 620.Google Scholar
  168. Vogel, Z., Sytkowski, A. J., and Nirenberg, M. W., 1972, Acetylcholine receptors of muscle grown in vitro, Proc. Natl. Acad. Sci. USA 69: 3180.Google Scholar
  169. Wenger, B. S., 1951, Determination of structural patterns in the spinal cord of the chick embryo studied by transplantations between brachial and adjacent levels, J. Exp. Zool. 116: 123.Google Scholar
  170. Weiss, P., and Edds, M. V., 1945, Sensory-motor nerve cross in the rat, J. Neurophysiol. 8: 173.Google Scholar
  171. Weiss, P., and Hoag, A., 1946, Competitive reinnervation of rat muscles by their own and foreign nerves, J. Neurophysiol. 9: 413.Google Scholar
  172. Weiss, P., and Taylor, A. C., 1944, Further experimental evidence against “neurotropism” in nerve regeneration, J. Exp. Zool. 95: 233.Google Scholar
  173. Williams, P. E., and Goldspink, G., 1971, Longitudinal growth of striated muscle fibers, J. Cell Sci. 9: 751.Google Scholar
  174. Wilson, B. W., Nieberg, P. S., Walker, C. R., Linkhart, T. A., and Fry, D. M., 1973, Production and release of acetylcholinesterase by cultured chick embryo muscle, Dev. Biol. 33: 285.Google Scholar
  175. Yaffe, D., 1969, Cellular aspects of muscle differentiation in vitro, Curr. Top. Dev. Biol. 4: 37.Google Scholar
  176. Yaffe, D. and Feldman, M., 1965, The formation of hybrid multinucleated muscle fibers from myoblasts of different genetic origin, Dev. Biol. 11: 300.Google Scholar
  177. Yellin, H., 1967, Neural regulation of enzymes in muscle fibers of red and white muscle, Exp. Neurol. 19: 92.Google Scholar
  178. Yonezawa, T., Saida, T., Robbins, N., and Ibata, Y., 1973, Electron microscopic studies on the neuromuscular junctions developed in vitro: Cholinesterase activity. (Japanese) Advan. Neurol. Sci. 17: 170.Google Scholar
  179. Zacks, S. I., 1964, The Motor Endplate, Saunders, Philadelphia.Google Scholar
  180. Zalewski, A. A., 1970, Reinnervation of denervated skeletal muscle by axons of motor, sensory and sympathetic neurons, Physiologist 12: 354.Google Scholar
  181. Zelena, J., and Jirmanova, I., 1973, Ultrastructure of chicken slow muscle after nerve cross union, Exp. Neurol. 38: 272.Google Scholar
  182. Zelena, J., and Szentagothai, J., 1957, Verlagerung der Lokalisation specifischer Cholinesterase Während der Entwicklung der Muskelinnervation, Acta Histochem. 3: 284.Google Scholar
  183. Zelena, J., Vyklicky, L., and Jirmanova, I., 1967, Motor enplates in fast and slow muscles of the chick after cross-union of their nerves, Nature (London) 214: 1010.Google Scholar

Copyright information

© Plenum Press, New York 1976

Authors and Affiliations

  • Douglas M. Fambrough
    • 1
  1. 1.Department of EmbryologyCarnegie Institution of WashingtonBaltimoreUSA

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