Structural determinants of the reliability of synaptic transmission at the vertebrate neuromuscular junction

Journal of Neurocytology

Volumn 32, Issue 5-8, 2003, Pages 505-522

  Slater, Clarke R ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN; CHOLINERGIC RECEPTOR; ION CHANNEL; MESSENGER RNA; VOLTAGE GATED SODIUM CHANNEL;

CEREBRAL PALSY; DENSITY; HUMAN; MODEL; MUSCLE FUNCTION; MYASTHENIA GRAVIS; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; PLASTICITY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RELIABILITY; REVIEW; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; VERTEBRATE; ANIMAL; PHYSIOLOGY; SKELETAL MUSCLE; ULTRASTRUCTURE;

VERTEBRATA;

ANIMALS; HUMANS; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; SYNAPTIC TRANSMISSION;

EID: 3042624687     PISSN: 03004864     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:NEUR.0000020607.17881.9b     Document Type: Review

References (134)

1. ALDERSON, K., HOLDS, J. B. & ANDERSON, R. L. (1991) Botulinum-induced alteration of nerve-muscle interactions in the human orbicularis oculi following treatment for blepharospasm. Neurology 41, 1800-1805.
2. ANDERSON, M. J. & COHEN, M. W. (1977) Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J. Physiol. 268, 757-773.
3. AWAD, S. S., BUCKEL, A., LIGHTOWLERS, R. N., LØMO, T., STOCKSLEY, M. A., WOOD, S. J., YOUNG, C. & SLATER, C. R. (1999) Accumulation of voltage-gated sodium channels at rat neuromuscular junctions. Society for Neuroscience Abstracts 25, 1021.
4. AWAD, S. S., BUCKEL, A., YOUNG, C., BRENNER, H. R. & SLATER, C. R. (2003) Accumulation of sodium channels at postsynaptic sites in rat muscles regenerating in the absence of the nerve is associated with a local increase in abundance of their mRNAs. British Neuroscience Association Abstracts 17, P101.
5. AWAD, S. S., LIGHTOWLERS, R. N., YOUNG, C., CHRZANOWSKA-LIGHTOWLERS, Z. M., LØMO, T. & SLATER, C. R. (2001) Sodium channel mRNAs at the neuromuscular junction: Distinct patterns of accumulation and effects of muscle activity. J. Neurosci. 21, 8456-8463.
6. 1 channels and ankyrinG occupy a different postsynaptic domain from AChRs from an early stage of neuromuscular junction maturation in rats. J. Neurosci. 23, 2102-2111.
7. BALICE-GORDON, R. J., BREEDLOVE, S. M., BERNSTEIN, S. & LICHTMAN, J. W. (1990) Neuromuscular junctions shrink and expand as muscle fiber size is manipulated: In vivo observations in the androgen-sensitive bulbocavernosus muscle of mice. J. Neurosci. 10, 2660-2671.
8. BALICE-GORDON, R. J. & LICHTMAN, J. W. (1993) In vivo observations of pre-and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J. Neurosci. 13, 834-855.
9. BANNER, L. R. & HERRERA, A. A. (1986) Differences in synaptic efficacy at neuromuscular junctions in frog twitch muscles. J. Physiol. 379, 205-215.
10. BEAM, K. G., CALDWELL, J. H. & CAMPBELL, D. T. (1985) Na channels in skeletal muscle concentrated near the neuromuscular junction. Nature 313, 588-590.
11. BETZ, W. J., CALDWELL, J. H. & KINNAMON, S. C. (1984) Increased sodium conductance in the synaptic region of rat skeletal muscle fibres. J. Physiol. 352, 189-202.
12. BEVAN, S. & STEINBACH, J. H. (1977) The distribution of alpha-bungarotoxin binding sites of mammalian skeletal muscle developing in vivo. J. Physiol. 267, 195-213.
13. BEWICK, G. S., YOUNG, C. & SLATER, C. R. (1996) Spatial relationships of utrophin, dystrophin, beta-dystroglycan and beta-spectrin to acetylcholine receptor clusters during postnatal maturation of the rat neuromuscular junction. J. Neurocytol. 25, 367-379.
14. BEZAKOVA, G. & LØMO, T. (2001) Muscle activity and muscle agrin regulate the organization of cytoskeletal proteins and attached acetylcholine receptor (AchR) aggregates in skeletal muscle fibers. J. Cell Biol. 153, 1453-1463.
15. BIGLAND-RITCHIE, B., KUKULKA, C. G., LIPPOLD, O. C. & WOODS, J. J. (1982) The absence of neuromuscular transmission failure in sustained maximal voluntary contractions. J. Physiol. (Lond.) 330, 265-278.
16. BIGNAMI, F., CAMUS, G., MARCHAND, S., BAILLY, L., STETZKOWSKI-MARDEN, F. & CARTAUD, J. (1998) Targeting of acetylcholine receptor and 43 kDa rapsyn to the postsynaptic membrane in Torpedo marmorata electrocyte. J. Physiol. Paris 92, 177-181.
17. BOYD, I. A. & MARTIN, A. R. (1956) The end-plate potential in mammalian muscle. J. Physiol. (Lond.) 132, 74-91.
18. BRAITHWAITE, A. W. & HARRIS, A. J. (1979) Neural influence on acetylcholine receptor clusters in embryonic development of skeletal muscles. Nature 279, 549-551.
19. BRENNER, H. R., WITZEMANN, V. & SAKMANN, B. (1990) Imprinting of acetylcholine receptor messenger RNA accumulation in mammalian neuromuscular synapses. Nature 344, 544-547.
20. BROWN, M. C., GOODWIN, S. & IRONTON, R. (1977) Prevention of motor nerve sprouting in botulinum toxin poisoned mouse soleus muscles by direct stimulation of the muscle. J. Physiol. (Lond.) 248, 44P-45P.
21. BROWN, M. C., HOLLAND, R. L. & HOPKINS, W. G. (1981) Motor nerve sprouting. Annu. Rev. Neurosci. 4, 17-42.
22. CALDWELL, J. H., CAMPBELL, D. T. & BEAM, K. G. (1986) Na channel distribution in vertebrate skeletal muscle. J. Gen. Physiol. 87, 907-932.
23. CARONI, P., SCHNEIDER, C., KIEFER, M. C. & ZAPF, J. (1994) Role of muscle insulin-like growth factors in nerve sprouting: Suppression of terminal sprouting in paralyzed muscle by IGF-binding protein 4. J. Cell Biol. 125, 893-902.
24. CASTONGUAY, A., LEVESQUE, S. & ROBITAILLE, R. (2001) Glial cells as active partners in synaptic functions. Prog. Brain Res. 132, 227-240.
25. CATTERALL, W. A. (1992) Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 72, S15-S48.
26. COHEN, I., RIMER, M., LØMO, T. & MCMAHAN, U. J. (1997) Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol. Cell Neurosci. 9, 237-253.
27. COOPER, S. (1966) Muscle spindles and motor units. In Control and innervation of skeletal muscle (edited by Andrew) pp. 9-16. Dundee: University of St. Andrews.
28. COURTNEY, J. & STEINBACH, J. H. (1981) Age changes in neuromuscular junction morphology and acetylcholine receptor distribution on rat skeletal muscle fibres. J. Physiol. 320, 435-447.
29. COUTEAUX, R. & PECOT-DECHAVASSINE, M. (1970) Vesicules synaptiques et poches au niveau des 'zones actives' de la jonction neuromusculaire. Comptes rendus des seances de l'Academie des Sciences 271, 2346-2349.
30. DE PAIVA, A., MEUNIER, F. A., MOLGO, J., AOKI, K. R. & DOLLY, J. O. (1999) Functional repair of motor endplates after botulinum neurotoxin type A poisoning: Biphasic switch of synaptic activity between nerve sprouts and their parent terminals. Proc. Natl. Acad. Sci. USA 96, 3200-3205.
31. DECONINCK, A. E., POTTER, A. C., TINSLEY, J. M., WOOD, S. J., VATER, R., YOUNG, C., METZINGER, L., VINCENT, A., SLATER, C. R. & DAVIES, K. E. (1997) Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J. Cell Biol. 136, 883-894.
32. DODGE, F. A., JR. & RAHAMIMOFF, R. (1967) Cooperative action a calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193, 419-432.
33. DUCHEN, L. W. (1970) Changes in motor innervation and cholinesterase localization induced by botulinum toxin in skeletal muscle of the mouse: Differences between fast and slow muscles. J. Neurol. Neurosurg. Psychiatry 33, 40-54.
34. ELMQVIST, D. & QUASTEL, D. M. (1965) A quantitative study of end-plate potentials in isolated human muscle. J. Physiol. (Lond.) 178, 505-529.
35. ENGEL, A. G., OHNO, K. & SINE, S. M. (2003) Congenital myasthenic syndromes: Progress over the past decade. Muscle Nerve 27, 4-25.
36. ENGEL, A. G., WALLS, T. J., NAGEL, A. & UCHITEL, O. (1990) Newly recognized congenital myasthenic syndromes: I. congenital paucity of synaptic vesicles and reduced quantal release. ii. high-conductance fast-channel syndrome, iii. abnormal acetylcholine receptor (achr) interaction with acetylcholine. iv. achr deficiency and short channel-open time. Prog. Brain Res. 84, 125-137.
37. FAWCETT, P. R., SLATER, C. R., WALLS, T. J., LYONS, P. R. & YOUNG, C. (1995) Congenital myasthenia: A clinical and in vitro study of 11 cases. Electroencephalog. Clin. Neurophysiol. 97, S45.
38. FERTUCK, H. C. & SALPETER, M. M. (1974) Localization of acetylcholine receptor by 1251-labeled alpha-bungarotoxin binding at mouse motor endplates. Proc. Natl. Acad. Sci. U.S.A. 71, 1376-1378.
39. FLUCHER, B. E. & DANIELS, M. P. (1989) Distribution of Na+ channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kd protein. Neuron 3, 163-175.
40. FONTAINE, B., SASSOON, D., BUCKINGHAM, M. & CHANGEUX, J. P. (1988) Detection of the nicotinic acetylcholine receptor alpha-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. EMBO J. 7, 603-609.
41. FUKUNAGA, H., ENGEL, A. G., LANG, B., NEWSOM-DAVIS, J. & VINCENT, A. (1983) Passive transfer of Lambert-Eaton myasthenic syndrome with IgG from man to mouse depletes the presynaptic membrane active zones. Proc. Natl. Acad. Sci. U.S.A. 80, 7636-7640.
42. FUKUOKA, T., ENGEL, A. G., LANG, B., NEWSOM-DAVIS, J., PRIOR, C. & WRAY, D. W. (1987) Lambert-Eaton myasthenic syndrome: I. Early morphological effects of IgG on the presynaptic membrane active zones. Ann. Neurol. 22, 193-199.
43. GAUTAM, M., DECHIARA, T. M., GLASS, D. J., YANCOPOULOS, G. D. & SANES, J. R. (1999) Distinct phenotypes of mutant mice lacking agrin, MuSK, or rapsyn. Brain Res. Dev. Brain Res. 114, 171-178.
44. GAUTAM, M., NOAKES, P. G., MUDD, J., NICHOL, M., CHU, G. C., SANES, J. R. & MERLIE, J. P. (1995) Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
45. GEE, S. H., MADHAVAN, R., LEVINSON, S. R., CALDWELL, J. H., SEALOCK, R. & FROEHNER, S. C. (1998) Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J. Neurosci. 18, 128-137.
46. GERTLER, R. A. & ROBBINS, N. (1978) Differences in neuromuscular transmission in red and white muscles. Brain Res. 142, 160-164.
47. GLASS, D. J., BOWEN, D. C., STITT, T. N., RADZIEJEWSKI, C., BRUNO, J., RYAN, T. E., GIES, D. R., SHAH, S., MATTSSON, K., BURDEN, S. J., DISTEFANO, P. S., VALENZUELA, D. M., DECHIARA, T. M. & YANCOPOULOS, G. D. (1996) Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
48. GOLDIN, A. L., BARCHI, R. L., CALDWELL, J. H., HOFMANN, F., HOWE, J. R., HUNTER, J. C., KALLEN, R. G., MANDEL, G., MEISLER, M. H., NETTER, Y. B., NODA, M., TAMKUN, M. M., WAXMAN, S. G., WOOD, J. N. & CATTERALL, W. A. (2000) Nomenclature of voltage-gated sodium channels. Neuron 28, 365-368.
49. GRADY, R. M., MERLIE, J. P. & SANES, J. R. (1997) Subtle neuromuscular defects in utrophin-deficient mice. J. Cell Biol. 136, 871-882.
50. GRADY, R. M., ZHOU, H., CUNNINGHAM, J. M., HENRY, M. D., CAMPBELL, K. P. & SANES, J. R. (2000) Maturation and maintenance of the neuromuscular synapse: Genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25, 279-293.
51. HARLOW, M. L., RESS, D., STOSCHEK, A., MARSHALL, R. M. & MCMAHAN, U. J. (2001) The architecture of active zone material at the frog's neuromuscular junction. Nature 409, 479-484.
52. HARRIS, C. P., ALDERSON, K., NEBEKER, J., HOLDS, J. B. & ANDERSON, R. L. (1991) Histologic features of human orbicularis oculi treated with botulinum A toxin. Arch. Ophthalmol. 109, 393-395.
53. HARTSHORNE, R. P. & CATTERALL, W. A. (1981) Purification of the saxitoxin receptor of the sodium channel from rat brain. Proc. Natl. Acad. Sci. U.S.A. 78, 4620-4624.
54. HARTZELL, H. C., KUFFLER, S. W. & YOSHIKAMI, D. (1975) Post-synaptic potentiation: Interaction between quanta of acetylcholine at the skeletal neuromuscular synapse. J. Physiol. (Lond.) 251, 427-463.
55. HENNIG, R. & LØMO, T. (1985) Firing patterns of motor units in normal rats. Nature 314, 164-166.
56. HERRERA, A. A. (1984) Polyneuronal innervation and quantal transmitter release in formamide-treated frog sartorius muscles. J. Physiol. 355, 267-280.
57. HEUSER, J. E., REESE, T. S., DENNIS, M. J., JAN, Y., JAN, L. & EVANS, L. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81, 275-300.
58. HOLDS, J. B., ALDERSON, K., FOGG, S. G. & ANDERSON, R. L. (1990) Motor nerve sprouting in human orbicularis muscle after botulinum A injection. Invest Ophthalmol. Vis. Sci. 31, 964-967.
59. HUBBARD, J. I., LLINAS, R. & QUASTEL, D. M. J. (1969). Electrophysiological Analysis of Synaptic Transmission. Edward Arnold (Publishers) Ltd.
60. JACOB, M. & LENTZ, T. L. (1979) Localization of acetylcholine receptors by means of horseradish peroxidase-alpha-bungarotoxin during formation and development of the neuromuscular junction in the chick embryo. J. Cell Biol. 82, 195-211.
61. JANKOVIC, J. & HALLETT, M. (1994). Therapy with botulinum toxin. New York: Marcel Dekker, Inc.
62. JENKINS, S. M. & BENNETT, V. (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155, 739-746.
63. JENKINS, S. M. & BENNETT, V. (2002) Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion. Proc. Natl. Acad. Sci. U.S.A. 99, 2303-2308.
64. JERUSALEM, F., ENGEL, A. G. & GOMEZ, M. R. (1974) Duchenne dystrophy. II. Morphometric study of motor end-plate fine structure. Brain 97, 123-130.
65. JONES, G., MEIER, T., LICHTSTEINER, M., WITZEMANN, V., SAKMANN, B. & BRENNER, H. R. (1997) Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl. Acad. Sci. U.S.A. 94, 2654-2659.
66. KAMENSKAYA, M. A., ELMQVIST, D. & THESLEFF, S. (1975) Guanidine and neuromuscular transmission. II. Effect on transmitter release in response to repetitive nerve stimulation. Arch. Neurol. 32, 510-518.
67. KATZ, B. (1996) Neural transmitter release: From quantal secretion to exocytosis and beyond. The Fenn Lecture. J. Neurocytol. 25, 677-686.
68. KATZ, B. & MILEDI, R. (1979) Estimates of quantal content during 'chemical potentiation' of transmitter release. Proc. R. Soc. Lond B Biol. Sci. 205, 369-378.
69. KELLY, A. M. & ZACKS, S. I. (1969) The fine structure of motor endplate morphogenesis. J. Cell Biol. 42, 154-169.
70. KORDELI, E., LUDOSKY, M. A., DEPRETTE, C., FRAPPIER, T. & CARTAUD, J. (1998) AnkyrinG is associated with the postsynaptic membrane and the sarcoplasmic reticulum in the skeletal muscle fiber. J. Cell Sci. 111, (Pt 15), 2197-2207.
71. KRAMARCY, N. R. & SEALOCK, R. (2000) Syntrophin isoforms at the neuromuscular junction: Developmental time course and differential localization. Mol. Cell Neurosci. 15, 262-274.
72. KUES, W. A., SAKMANN, B. & WITZEMANN, V. (1995) Differential expression patterns of five acetylcholine receptor subunit genes in rat muscle during development. Eur. J. Neurosci. 7, 1376-1385.
73. KUMMER, T. T., MISGELD, T., LICHTMAN, J. W. & SANES, J. R. (2002) Formation of a mature, branched postsynaptic apparatus in aneural muscle. 2002 Abstract Viewer/Itinerary Planner.
74. KUNO, M. (1995). The Synapse: Function, Plasticity and Neurotrophism. Oxford: Oxford University Press.
75. LAND, B. R., SALPETER, E. E. & SALPETER, M. M. (1981) Kinetic parameters for acetylcholine interaction in intact neuromuscular junction. Proc. Natl. Acad. Sci. U.S.A. 78, 7200-7204.
76. LIN, W., BURGESS, R. W., DOMINGUEZ, B., PFAFF, S. L., SANES, J. R. & LEE, K. F. (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410, 1057-1064.
77. LØMO, T. & SLATER, C. R. (1980) Control of junctional acetylcholinesterase by neural and muscular influences in the rat. J. Physiol. 303, 191-202.
78. LOVE, F. M. & THOMPSON, W. J. (1999) Glial cells promote muscle reinnervation by responding to activity-dependent postsynaptic signals. J. Neurosci. 19, 10390-10396.
79. LUPA, M. T., KRZEMIEN, D. M., SCHALLER, K. L. & CALDWELL, J. H. (1993) Aggregation of sodium channels during development and maturation of the neuromuscular junction. J. Neurosci. 13, 1326-1336.
80. MAGLEBY, K. L. (1979) Facilitation, augmentation, and potentiation of transmitter release. Prog. Brain Res. 49, 175-182.
81. MALHOTRA, J. D., KOOPMANN, M. C., KAZEN-GILLESPIE, K. A., FETTMAN, N., HORTSCH, M. & ISOM, L. L. (2002) Structural requirements for interaction of sodium channel Beta 1 subunits with ankyrin. J. Biol. Chem. 277, 26681-26688.
82. MARQUES, M. J., CONCHELLO, J. A. & LICHTMAN, J. W. (2000) From plaque to pretzel: Fold formation and acetylcholine receptor loss at the developing neuromuscular junction. J. Neurosci. 20, 3663-3675.
83. MARTIN, A. R. (1994) Amplification of neuromuscular transmission by postjunctional folds. Proc. R. Soc. Lond B Biol. Sci. 258, 179-187.
84. MATHIESEN, I., RIMER, M., ASHTARI, O., COHEN, I., MCMAHAN, U. J. & LØMO, T. (1999) Regulation of the size and distribution of agrin-induced postsynaptic-like apparatus in adult skeletal muscle by electrical muscle activity. Mol. Cell Neurosci. 13, 207-217.
85. MATTHEWS-BELLINGER, J. A. & SALPETER, M. M. (1983) Fine structural distribution of acetylcholine receptors at developing mouse neuromuscular junctions. J. Neurosci. 3, 644-657.
86. MCMAHAN, U. J. (1990) The agrin hypothesis. Cold Spring Harb. Symp. Quant. Biol. 55, 407-418.
87. MERLIE, J. P. & SANES, J. R. (1985) Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres. Nature 317, 66-68.
88. MOORE, C., LEU, M., MULLER, U. & BRENNER, H. R. (2001) Induction of multiple signaling loops by MuSK during neuromuscular synapse formation. Proc. Natl. Acad. Sci. U.S.A. 98, 14655-14660.
89. MSGHINA, M., GOVIND, C. K. & ATWOOD, H. L. (1998) Synaptic structure and transmitter release in crustacean phasic and tonic motor neurons. J. Neurosci. 18, 1374-1382.
90. MURTHY, V. N., SCHIKORSKI, T., STEVENS, C. F. & ZHU, Y. (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32, 673-682.
91. NOAKES, P. G., PHILLIPS, W. D., HANLEY, T. A., SANES, J. R. & MERLIE, J. P. (1993) 43K protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev. Biol. 155, 275-280.
92. PANG, K., QUINBY, J., EYRE, J. & SLATER, C. (2002) The neuromuscular junction in cerebral palsy and its response to botulinum toxin-A. Developmental Medicine & Child Neurology 43 (Suppl. 90), 13.
93. PAWSON, P. A., GRINNELL, A. D. & WOLOWSKE, B. (1998) Quantitative freeze-fracture analysis of the frog neuromuscular junction synapse - II. Proximal-distal measurements. J. Neurocytol. 27, 379-391.
94. PESTRONK, A. & DRACHMAN, D. B. (1978) Motor nerve sprouting and acetylcholine receptors. Science 199, 1223-1225.
95. PETERS, M. F., KRAMARCY, N. R., SEALOCK, R. & FROEHNER, S. C. (1994) beta 2-Syntrophin: Localization at the neuromuscular junction in skeletal muscle. Neuroreport 5, 1577-1580.
96. PHILLIPS, W. D., NOAKES, P. G., ROBERDS, S. L., CAMPBELL, K. P. & MERLIE, J. P. (1993) Clustering and immobilization of acetylcholine receptors by the 43-kD protein: A possible role for dystrophin-related protein. J. Cell Biol. 123, 729-740.
97. PIETTE, J., HUCHET, M., HOUZELSTEIN, D. & CHANGEUX, J. P. (1993) Compartmentalized expression of the alpha-and gamma-subunits of the acetylcholine receptor in recently fused myofibers. Dev. Biol. 157, 205-213.
98. PLOMP, J. J., VAN KEMPEN, G. T., DE BAETS, M. B., GRAUS, Y. M., KUKS, J. B. & MOLENAAR, P. C. (1995) Acetylcholine release in myasthenia gravis: Regulation at single end-plate level. Ann. Neurol. 37, 627-636.
99. PLOMP, J. J., VAN KEMPEN, G. T. & MOLENAAR, P. C. (1994) The upregulation of acetylcholine release at endplates of alpha-bungarotoxin-treated rats: Its dependency on calcium. J. Physiol. 478 (Pt 1), 125-136.
100. REGEHR, W. G. & STEVENS, C. E. (2001) Physiology of synaptic transmission and short-term plasticity. In Synapses (edited by Cowen, Sudhof, & Stevens), pp. 135-175. Baltimore and London: The Johns Hopkins University Press.
101. REID, B., SLATER, C. R. & BEWICK, G. S. (1999) Synaptic vesicle dynamics in rat fast and slow motor nerve terminals. J. Neurosci. 19, 2511-2521.
102. RUFF, R. L. (1996) Effects of length changes on Na+ current amplitude and excitability near and far from the end-plate. Muscle Nerve 19, 1084-1092.
103. SAKMANN, B. & BRENNER, H. R. (1978) Change in synaptic channel gating during neuromuscular development. Nature 276, 401-402.
104. SALPETER, M. M. (1987) Vertebrate neuromuscular junctions: General morphology, molecular organization, and functional consequences. In The Vertebrate Neuromuscular Junction (edited by Salpeter) pp. 1-54. New York: Alan R. Liss, Inc.
105. SANES, J. R. & LICHTMAN, J. W. (1999) Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22, 389-442.
106. SANES, J. R. & LICHTMAN, J. W. (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2, 791-805.
107. SANTA, T., ENGEL, A. G. & LAMBERT, E. H. (1972) Histometric study of neuromuscular junction ultrastructure. I. Myasthenia gravis. Neurology 22, 71-82.
108. SHERRINGTON, C. (1906). The integrative action of the nervous system. New Haven: Yale University Press.
109. SKORPEN, J., LAFOND-BENESTAD, S. & LØMO, T. (1999) Regulation of the size and distribution of ectopic neuromuscular junctions in adult skeletal muscle by nerve-derived trophic factor and electrical muscle activity. Mol. Cell Neurosci. 13, 192-206.
110. SLATER, C. R. (1982a) Neural influence on the postnatal changes in acetylcholine receptor distribution at nerve-muscle junctions in the mouse. Dev. Biol. 94, 23-30.
111. SLATER, C. R. (1982b) Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse. Dev. Biol. 94, 11-22.
112. SLATER, C. R., LYONS, P. R., WALLS, T. J., FAWCETT, P. R. & YOUNG, C. (1992) Structure and function of neuromuscular junctions in the vastus lateralis of man. A motor point biopsy study of two groups of patients. Brain 115 (Pt 2), 451-478.
113. SLATER, C. R., YOUNG, C., WOOD, S. J., BEWICK, G. S., ANDERSON, L. V., BAXTER, P., FAWCETT, P. R., ROBERTS, M., JACOBSON, L., KUKS, J., VINCENT, A. & NEWSOM-DAVIS, J. (1997) Utrophin abundance is reduced at neuromuscular junctions of patients with both inherited and acquired acetylcholine receptor deficiencies. Brain 120 (Pt 9), 1513-1531.
114. SMIT, L. M., HAGEMAN, G., VELDMAN, H., MOLENAAR, P. C., OEN, B. S. & JENNEKENS, F. G. (1988) A myasthenic syndrome with congenital paucity of secondary synaptic clefts: CPSC syndrome. Muscle Nerve 11, 337-348.
115. SMIT, L. M., VELDMAN, H., JENNEKENS, F. G., MOLENAAR, P. C. & OEN, B. S. (1987) A congenital myasthenic disorder with paucity of secondary synaptic clefts: Deficiency and altered distribution of acetylcholine receptors. Ann. N.Y. Acad. Sci. 505, 346-356.
116. SMITH, M. A. & SLATER, C. R. (1983) Spatial distribution of acetylcholine receptors at developing chick neuromuscular junctions. J. Neurocytol. 12, 993-1005.
117. SON, Y. J., TRACHTENBERG, J. T. & THOMPSON, W. J. (1996) Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci. 19, 280-285.
118. SRINIVASAN, Y., ELMER, L., DAVIS, J., BENNETT, V. & ANGELIDES, K. (1988) Ankyrin and spectrin associate with voltage-dependent sodium channels in brain. Nature 333, 177-180.
119. STOCKSLEY, M. A. (2000) Neural control of the distribution of voltage-gated sodium channels during development of the rat neuromuscular junction. PhD Thesis University of Newcastle upon Tyne.
120. STOCKSLEY, M. A. & SLATER, C. R. (1999) Voltage gated sodium channels increase in density in junctional, perijunctional and non-junctional regions of developing rat muscle fibres. Brit. Neurosci. Soc. Abst. 15, 75.
121. TAM, S. L., ARCHIBALD, V., JASSAR, B., TYREMAN, N. & GORDON, T. (2001) Increased neuromuscular activity reduces sprouting in partially denervated muscles. J. Neurosci. 21, 654-667.
122. TRIMMER, J. S., COOPERMAN, S. S., TOMIKO, S. A., ZHOU, J. Y., CREAN, S. M., BOYLE, M. B., KALLEN, R. G., SHENG, Z. H., BARCHI, R. L. & SIGWORTH, F. J. (1989) Primary structure and functional expression of a mammalian skeletal muscle sodium channel. Neuron 3, 33-49.
123. VINCENT, A. (1999) Immunology of the neuromuscular junction and presynaptic nerve terminal. Curr. Opin. Neurol. 12, 545-551.
124. VINCENT, A., BEESON, D. & LANG, B. (2000) Molecular targets for autoimmune and genetic disorders of neuromuscular transmission. Eur. J. Biochem. 267, 6717-6728.
125. VINCENT, A., CULL-CANDY, S. G., NEWSOM-DAVIS, J., TRAUTMANN, A., MOLENAAR, P. C. & POLAK, R. L. (1981) Congenital myasthenia: End-plate acetylcholine receptors and electrophysiology in five cases. Muscle Nerve 4, 306-318.
126. WOOD, S. J., SHEWRY, K., YOUNG, C. & SLATER, C. R. (1998) An early stage in sodium channel clustering at developing rat neuromuscular junctions. Neuroreport 9, 1991-1995.
127. WOOD, S. J. & SLATER, C. R. (1994) Action potential generation in the isolated rat soleus muscle. J. Physiol. (Lond.) 480,125P.
128. WOOD, S. J. & SLATER, C. R. (1995) Action potential generation in rat slow-and fast-twitch muscles. J. Physiol. 486 (Pt 2), 401-410.
129. WOOD, S. J. & SLATER, C. R. (1997) The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast-and slow-twitch muscles. J. Physiol. 500 (Pt 1), 165-176.
130. WOOD, S. J. & SLATER, C. R. (1998) beta-Spectrin is colocalized with both voltage-gated sodium channels and ankyrinG at the adult rat neuromuscular junction. J. Cell Biol. 140, 675-684.
131. WOOD, S. J. & SLATER, C. R. (2001) Safety factor at the neuromuscular junction. Prog. Neurobiol. 64, 393-429.
132. YANG, X., ARBER, S., WILLIAM, C., LI, L., TANABE, Y., JESSELL, T. M., BIRCHMEIER, C. & BURDEN, S. J. (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30, 399-410.
133. YEE, W. C. & PESTRONK, A. (1987) Mechanisms of post-synaptic plasticity: Remodeling of the junctional acetylcholine receptor cluster induced by motor nerve terminal outgrowth. J. Neurosci. 7, 2019-2024.
134. YOUNG, C., LINDSAY, S., VATER, R. & SLATER, C. R. (1998) An improved method for the simultaneous demonstration of mRNA and esterase activity at the human neuromuscular junction. Histochem. J. 30, 7-11.