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Activity-dependent switch from synapse formation to synapse elimination during development of neuromuscular junctions

  • Published:
Journal of Neurocytology

Abstract

The embryonic development of neuromuscular junctions consists of two successive epochs, an early period marked by exuberant synapse formation and a later period marked by synapse elimination. In the frog muscles we have studied, myogenesis is protracted and overlaps the periods of synapse formation and elimination. Thus, the formative and regressive events of synaptic development do not occur in synchrony across different fibers in the muscle. We propose that local activity orchestrates a shift from synaptogenesis to synapse elimination at the level of single muscle fibers. We also present evidence that perisynaptic Schwann cells and the expression of ion channels in the sarcolemma play important roles in the development of neuromuscular junctions. Questions for future study are outlined.

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References

  • AFRAMIAN, D. & GRINNELL, A. D. (1988) Destabilization of junctional ACh receptors by a reinnervating frog motor nerve. Puerto Rico Health Science Journal 7, 8–86.

    Google Scholar 

  • ARMSTRONG, D. L., TURIN, L. & WARNER, A. E. (1983) Muscle activity and the loss of electrical coupling between striated muscle cells in Xenopus embryos. Journal of Neuroscience 3, 141–1421.

    PubMed  Google Scholar 

  • ASTROW, S. H., QIANG, H. & KO, C.-P. (1998) Perisynaptic Schwann cells at neuromuscular junctions revealed by a novel monoclonal antibody. Journal of Neurocytology 27, 66–681.

    PubMed  Google Scholar 

  • 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. Journal of Neuroscience 13, 83–855.

    PubMed  Google Scholar 

  • BALICE-GORDON, R. J. & LICHTMAN, J. W. (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 51–524.

    PubMed  Google Scholar 

  • BARBER, M. J. & LICHTMAN, J. W. (1999) Activity-driven synapse elimination leads paradoxically to domination by inactive neurons. Journal of Neuroscience 19, 997–9985.

    PubMed  Google Scholar 

  • BARRY, J. A. & RIBCHESTER, R. R. (1995) Persistent polyneuronal innervation in partially denervated rat muscle after reinnervation and recovery from prolonged nerve conduction block. Journal of Neuroscience 15, 632–6339.

    PubMed  Google Scholar 

  • BENNETT, M. R. & ROBINSON, J. (1989) Growth and elimination of nerve terminals at synaptic sites during polyneuronal innervation of muscle cells: A trophic hypothesis. Proceedings of the Royal Society of London, Series B 235, 29–320.

    Google Scholar 

  • BETZ, W. J., CALDWELL, J. H. & RIBCHESTER, R. R. (1980) The effects of partial denervation at birth on the development of muscle fibers and motor units in rat lumbrical muscle. Journal of Physiology 303, 26–279.

    PubMed  Google Scholar 

  • BETZ, W. J., CHUA, M. & RIDGE, R. M. (1989) Inhibitory interactions between motoneuron terminals in neonatal rat lumbrical muscle. Journal of Physiology 417, 2–51.

    PubMed  Google Scholar 

  • BETZ, W. J., MAO, F. & BEWICK, G. S. (1992) Activitydependent fluorescent staining and destaining of living vertebrate motor nerve terminals. Journal of Neuroscience 12, 36–375.

    PubMed  Google Scholar 

  • BI, G.-Q. & POO, M.-M. (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Annual Review of Neuroscience 24, 13–166.

    PubMed  Google Scholar 

  • BLACKSHAW, S. E. & WARNER, A. E. (1976) Low resistance junctions between mesoderm cells during development of trunk muscles. Journal of Physiology 255, 20–230.

    PubMed  Google Scholar 

  • BRENOWITZ, G. L., COLLINS, W. F. D. & ERULKAR, S. D. (1983) Dye and electrical coupling between frog motoneurons. Brain Research 274, 37–375.

    PubMed  Google Scholar 

  • BROWN, M. C., HOPKINS, W. G. & KEYNES, R. J. (1982) Short-and long-term effects of paralysis on the motor innervation of two different neonatal mouse muscles. Journal of Physiology 329, 43–450.

    PubMed  Google Scholar 

  • BROWN, M. C., JANSEN, J. K. S. & VAN ESSEN, D. (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. Journal of Physiology 261, 38–422.

    PubMed  Google Scholar 

  • BUFFELLI, M., BUSETTO, G., CANGIANO, L. & CANGIANO, A. (2002) Perinatal switch from synchronous to asynchronous activity of motoneurons: Link with synapse elimination. Proceedings of the National Academy of Sciences, USA 99, 1320–13205.

    Google Scholar 

  • BUSETTO, G., BUFFELLI, M., TOGNANA, E., BELLICO, F. & CANGIANO A. (2000) Hebbian mechanisms revealed by electrical stimulation at developing rat neuromuscular junctions. Journal of Neuroscience 20, 68–695.

    PubMed  Google Scholar 

  • CALLAWAY, E., SOHA, J. M. & VAN ESSEN, D. C. (1989) Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons. Journal of Neuroscience 9, 180–1824.

    PubMed  Google Scholar 

  • CARONI, P. & BECKER, M. (1992) The downregulation of growth-associated proteins in motoneurons at the onset of synapse elimination is controlled by muscle activity and IGF1. Journal of Neuroscience 12, 384–3861.

    PubMed  Google Scholar 

  • CHANG, Q. & BALICE-GORDON, R. J. (2000) Gap junctional communication among developing and injured motor neurons. Brain Research Reviews 32, 24–249.

    PubMed  Google Scholar 

  • CHANG, Q., GONZALEZ, M., PINTER, M. J. & BALICEGORDON, R. J. (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. Journal of Neuroscience 19, 1081–10828.

    PubMed  Google Scholar 

  • CHEN, L. & KO, C.-P. (1994) Extension of synaptic extracellular matrix during nerve terminal sprouting in living frog neuromuscular junctions. Journal of Neuroscience 14, 79–808.

    PubMed  Google Scholar 

  • COLLINS, W. F. I. (1983) Organization of electrical coupling between frog lumbar motoneurons. Journal of Neurophysiology 49, 73–744.

    PubMed  Google Scholar 

  • COLMAN, H., NABEKURA, J. & LICHTMAN, J. W. (1977) Alterations in synaptic strength preceding axon withdrawal. Science 275, 35–361.

    Google Scholar 

  • CONSTANTIN, B. & CRONIER, L. (2000) Involvement of gap junctional communication in myogenesis. International Review of Cytology 196, –65.

    PubMed  Google Scholar 

  • COSTANZO, E. M., BARRY, J. A. & RIBCHESTER, R. R. (1999) Co-regulation of synaptic efficacy at stable polyneuronally innervated neuromuscular junctions in reinnervated rat muscle. Journal of Physiology 521, 36–374.

    PubMed  Google Scholar 

  • COSTANZO, E. M., BARRY, J. A. & RIBCHESTER, R. R. (2000) Competition at silent synapses in reinnervated skeletal muscle. Nature Neuroscience 3, 69–700.

    PubMed  Google Scholar 

  • CREPEL, F., MARIANI, J. & DELHAYE-BOUCHAUD, N. (1976) Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. Journal of Neurobiology 7, 56–578.

    PubMed  Google Scholar 

  • CULICAN, S. M., NELSON, C. C. & LICHTMAN, J. W. (1998) Axon withdrawal during synapse elimination at the neuromuscular junction is accompanied by disassembly of the postsynaptic specialization and withdrawal of Schwann cell processes. Journal of Neuroscience 18, 495–4965.

    PubMed  Google Scholar 

  • DAHM, L. M. & LANDMESSER, L. T. (1991) The regulation of synaptogenesis during normal development and following activity blockade. Journal of Neuroscience 11, 23–255.

    PubMed  Google Scholar 

  • DAN, Y. & POO, M. M. (1992) Hebbian depression of isolated neuromuscular synapses in vitro. Science 256, 157–1573.

    PubMed  Google Scholar 

  • DECINO, P. & KIDOKORO, Y. (1985) Development and subsequent neural tube effects on the excitability of cultured Xenopus myocytes. Journal of Neuroscience 5, 147–1482.

    PubMed  Google Scholar 

  • DENNIS, M. J., ZISKIND-CONHAIM, L. & HARRIS, A. J. (1981) Development of neuromuscular junctions in rat embryos. Developmental Biology 81, 26–279.

    PubMed  Google Scholar 

  • DIAZ, J. & PECOT-DECHAVASSINE, M. (1988) Electrophysiological and morphological study of polyneuronal innervation in the cutaneous pectoris muscle of adult frog. Journal of Neurocytology 17, 27–292.

    PubMed  Google Scholar 

  • DING, R., JANSEN, J. K., LAING, N. G. & TONNESON, H. (1983) The innervation of skeletal muscles in chickens curarized during early development. Journal of Neurocytology 12, 88–919.

    PubMed  Google Scholar 

  • DUNIA, R. & HERRERA, A. A. (1993) Synapse formation and elimination during growth of the pectoral muscle of Xenopus laevis. Journal of Physiology 469, 50–509.

    PubMed  Google Scholar 

  • ENGLISH, A. W. & SCHWARTZ, G. (1995) Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing muscle fibers. Developmental Biology 169, 5–64.

    PubMed  Google Scholar 

  • ERNSBERGER, U. & SPITZER, N. C. (1995) Convertible modes of inactivation of potassium channels in Xenopus myocytes differentiating in vitro. Journal of Physiology 484, 31–329.

    PubMed  Google Scholar 

  • FERRARI, M. B. & SPITZER, N. C. (1999) Calcium signaling in the developing Xenopus myotome. Developmental Biology 213, 26–282.

    PubMed  Google Scholar 

  • FLADBY, T. & JANSEN, J. K. (1987) Postnatal loss of synaptic terminals in the partially denervated mouse soleus muscle. Acta Physiologica Scandinavica 129, 23–246.

    PubMed  Google Scholar 

  • FRELIN, C., VIJVERBERG, H. P., ROMEY, G., VIGNE, P. & LAZDUNSKI, M. (1984) Different functional states of tetrodotoxin sensitive and tetrodotoxin resistant Na+ channels occur during the in vitro development of rat skeletal muscle. Pflügers Archives—European Journal of Physiology 402, 12–128.

    Google Scholar 

  • FRY, M. & MOODY-CORBETT, F. (1999) Localization of sodium and potassium currents at sites of nerve-muscle contact in embryonic Xenopus muscle cells in culture. Pflügers Archives—European Journal of Physiology 437, 89–902.

    Google Scholar 

  • GRINNELL, A. D. & DO, J. (1991) Effect of denervation and regeneration on the stability of junctional ACh receptors in mature frog muscles. In Plasticity of Motoneuronal Connections, Elsevier, pp. 15–161.

  • GRINNELL, A. D. & HARADA, Y. (1996) Specificity and development of innervation pattern of Xenopus pectoralis muscle. Journal of Neurobiology 31, 41–432.

    PubMed  Google Scholar 

  • GU, X. & SPITZER, N. C. (1997) Breaking the code: Regulation of neuronal differentiation by spontaneous calcium transients. Developmental Neuroscience 19, 3–41.

    PubMed  Google Scholar 

  • HAIMANN, C., MALLART, A., TOMÁS I FERRÉ, J. & ZILBER-GACHELIN, N. F. (1981) Patterns of motor innervation in the pectoral muscle of Xenopus laevis: Evidence for possible synaptic remodelling. Journal of Physiology 310, 24–256.

    PubMed  Google Scholar 

  • HAMILL, O. P., MARTY, A., NEHER, E., SAKMANN, B. & SIGWORTH, F. J. (1981) Improved patchclamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archives—European Journal of Physiology 391, 8–100.

    Google Scholar 

  • HANCOCK, S., MOODY-CORBETT, F. L. & VIRGO, N. S. (1996) Potassium inward rectifier and acetylcholine receptor channels in embryonic Xenopus muscle cells in culture. Journal of Neurobiology 29, 35–366.

    PubMed  Google Scholar 

  • HARADA, Y. & GRINNELL, A. D. (1996) Regeneration of specific innervation in Xenopus pectoralis muscle. Journal of Neurobiology 31, 43–448.

    PubMed  Google Scholar 

  • HASHIMOTO, K. & KANO, M. (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38, 78–796.

    PubMed  Google Scholar 

  • HEBB, D. O. (1949) The Organization of Behavior. New York: Wiley.

    Google Scholar 

  • HERRERA, A. A. (1984) Polyneuronal innervation and quantal transmitter release in formamidetreated frog sartorius muscles. Journal of Physiology 355, 26–280.

    PubMed  Google Scholar 

  • HERRERA, A. A., BANNER, L. R. & NAGAYA, N. (1990) Repeated, in vivo observation of frog neuromuscular junctions: Remodelling involves concurrent growth and retraction. Journal of Neurocytology 19, 8–99.

    PubMed  Google Scholar 

  • HERRERA, A. A., BANNER, L. R., WERLE, M. J., REGNIER, M. & NAGAYA, N. (1991) Postmetamorphic development of the frog cutaneous pectoris muscle. Journal of Neurobiology 22, 1–28.

    PubMed  Google Scholar 

  • HERRERA, A. A. & GRINNELL, A. D. (1980) Transmitter release from frog motor nerve terminals depends on motor unit size. Nature 287, 64–651.

    PubMed  Google Scholar 

  • HERRERA, A. A., QIANG, H. & KO, C.-P. (2000) The role of perisynaptic Schwann cells in development of neuromuscular junctions in the frog (Xenopus laevis). Journal of Neuroscience 45, 23–254.

    Google Scholar 

  • HERRERA, A. A. & WERLE, M. J. (1990) Mechanisms of elimination, remodelling, and competition at frog neuromuscular junctions. Journal of Neurobiology 21, 7–98.

    PubMed  Google Scholar 

  • HERRERA, A. A. & WERLE, M. J. (1991) Elevated levels of polyneuronal innervation persist for as long as two years in reinnervated frog neuromuscular junctions. Journal of Neurobiology 22, 9–103.

    PubMed  Google Scholar 

  • HIRATA, K., ZHOU, C., NAKAMURA, K. & KAWABUCHI, M. (1997) Postnatal development of Schwann cells at neuromuscular junctions, with special reference to synapse elimination. Journal of Neurocytology 26, 79–809.

    PubMed  Google Scholar 

  • HONORÉ, E. & LAZDUNSKI, M. (1995) Biophysical, pharmacological and developmental properties of ATPsensitive K+ channels in cultured myotomal muscle cells from Xenopus embryos. Pflügers Archives—European Journal of Physiology 429, 60–616.

    Google Scholar 

  • HUME, R. I. & PURVES, D. (1983) Apportionment of the terminals from single preganglionic axons to target neurones in the rabbit ciliary ganglion. Journal of Physiology 338, 25–275.

    PubMed  Google Scholar 

  • JENNINGS, C. (1994) Developmental neurobiology. Death of a synapse. Nature 372, 51–524.

    PubMed  Google Scholar 

  • JORDAN, C. L. (1996) Ciliary neurotrophic factor may act in target musculature to regulate developmental synapse elimination. Developmental Neuroscience 18, 18–198.

    PubMed  Google Scholar 

  • JORDAN, C. L., WATAMURA, S. & ARNOLD, A. P. (1995) Androgenic, not estrogenic, steroids alter neuromuscular synapse elimination in rat levator ani. Developmental Brain Research 84, 21–224.

    Google Scholar 

  • KELLER-PECK, C. R., FENG, G., SANES, J. R., YAN, Q., LICHTMAN, J. W. & SNIDER, W. D. (2001) Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. Journal of Neuroscience 21, 613–6146.

    PubMed  Google Scholar 

  • KIDOKORO, Y. (1992) Initial uncoordinated expression of three types of voltage-gated currents in cultured Xenopus myocytes. Neuroscience Research 13, 18–197.

    PubMed  Google Scholar 

  • KIEHN, O. & TRESCH, M. C. (2002) Gap junctions and motor behavior. Trends in Neurosciences 25, 10–115.

    PubMed  Google Scholar 

  • KO, C.-P. & CHEN, L. (1996) Synaptic remodeling revealed by repeated, in vivo observations and electron microscopy of identified frog neuromuscular junctions. Journal of Neuroscience 16, 178–1790.

    PubMed  Google Scholar 

  • KOIRALA, S., HERRERA, A. A. & KO, C.-P. (2001) Perisynaptic Schwann cell processes lead nerve terminal growth at developing neuromuscular junctions in tadpoles. Society for Neuroscience Abstracts 27.

  • KOIRALA, S., REDDY, L. V. & KO, C.-P. (2003) Roles of glial cells in the formation, function, and maintenance of the neuromuscular junction. Journal of Neurocytology, this issue.

  • KOIRALA, S., QIANG, H., ASTROW, S. H. & KO, C.-P. (2000) Reciprocal interactions between perisynaptic Schwann cells and regenerating nerve terminals at the frog neuromuscular junction. Journal of Neurobiology 45, 23–254.

    PubMed  Google Scholar 

  • KUFFLER, D., THOMPSON, W. & JANSEN, J. K. S. (1977) The elimination of synapses in multiply-innervated skeletal muscle fibres of the rat: Dependence on distance between end-plates. Brain Research 138, 35–358.

    PubMed  Google Scholar 

  • KULLBERG, R. W., LENTZ, T. L. & COHEN, M. W. (1977) Development of the myotomal neuromuscular junction in Xenopus laevis: An electrophysiological and fine-structural study. Developmental Biology 60, 10–129.

    PubMed  Google Scholar 

  • KWON, Y. W., ABBONDANZO, S. J., STEWART, C. L. & GURNEY, M. E. (1995) Leukemia inhibitory factor influences the timing of programmed synapse withdrawal from neonatal muscles. Journal of Neurobiology 28, 3–50.

    PubMed  Google Scholar 

  • KWON, Y. W. & GURNEY, M. E. (1996) Brain-derived neurotrophic factor transiently stabilizes silent synapses on developing neuromuscular junctions. Journal of Neurobiology 29, 50–516.

    PubMed  Google Scholar 

  • LI, M.-X., JIA, M., YANG, L.-X., DUNLAP, V. & NELSON, P. G. (2002) Pre-and postsynaptic mechanisms in Hebbian activity-dependent synapse modification. Journal of Neurobiology 52, 24–250.

    PubMed  Google Scholar 

  • LIN, W., SANCHEZ, H. B., DEERNICK, T., MORRIS, J. K., ELLISMAN, M. & LEE, K.-F. (2000) Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proceedings of the National Academy of Sciences, USA 97, 129–1304.

    Google Scholar 

  • LINDEN, D. C. & LETINSKY, M. S. (1988) Correlated muscle and nerve development in the bullfrog cutaneous pectoris. Experimental Neurology 99, 70–734.

    PubMed  Google Scholar 

  • LINDEN, D. C., JERIAN, S. M. & LETINSKY, M. S. (1988) Neuromuscular junction development in the cutaneous pectoris muscle of Rana catesbeiana. Experimental Neurology 99, 73–760.

    PubMed  Google Scholar 

  • LINSDELL, P. & MOODY, W. J. (1994) Na+ channel misexpression accelerates K+ channel development in embryonic Xenopus laevis skeletal muscle. Journal of Physiology 480, 40–410.

    PubMed  Google Scholar 

  • LINSDELL, P. & MOODY, W. J. (1995) Electrical activity and calcium influx regulate ion channel development in embryonic Xenopus skeletal muscle. Journal of Neuroscience 15, 450–4514.

    PubMed  Google Scholar 

  • LIOU, J.-C., YANG, R.-S. & FU, W.-M. (1997) Regulation of quantal secretion by neurotrophic factors at developing motoneurons in Xenopus cell cultures. Journal of Physiology 503, 12–139.

    PubMed  Google Scholar 

  • LIU, Y., FIELDS, R. D., FITZGERALD, S., FESTOFF, B. W. & NELSON, P. G. (1994) Proteolytic activity, synapse elimination, and the Hebb synapse. Journal of Neurobiology 25, 32–335.

    PubMed  Google Scholar 

  • LO, Y. J. & POO, M.-M. (1991) Activity-dependent synaptic competition in vitro: Heterosynaptic suppression of developing synapses. Science 254, 101–1022.

    PubMed  Google Scholar 

  • LO, Y. J. & POO, M.-M. (1994) Heterosynaptic suppression of developing neuromuscular synapses in culture. Journal of Neuroscience 14, 468–4693.

    PubMed  Google Scholar 

  • LOHOF, A. M., DELHAYE-BOUCHAUD, N. & MARIANI, J. (1996) Synapse elimination in the central nervous system: Functional significance and cellular mechanisms. Reviews in the Neurosciences 7, 8–101.

    PubMed  Google Scholar 

  • LOHOF, A. M., IP, N. Y. & POO, M.-M. (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 35–353.

    PubMed  Google Scholar 

  • LOVE, F. M., SON, Y.-J. & THOMPSON, W. J. (2003) Activity alters muscle reinnervation and terminal sprouting by reducing the number of Schwann cell pathways that grow to link synaptic sites. Journal of Neurobiology 54, 56–576.

    PubMed  Google Scholar 

  • LOVE, F. M. & THOMPSON, W. J. (1998) Schwann cells proliferate at rat neuromuscular junctions during development and regeneration. Journal of Neuroscience 18, 937–9385.

    PubMed  Google Scholar 

  • MACLEOD, G. T., DICKENS, P. A. & BENNETT, M. R. (2001) Formation and function of synapses with respect to Schwann cells at the end of motor nerve terminal branches on mature amphibian (Bufo marinus) muscle. Journal of Neuroscience 21, 238–2392.

    PubMed  Google Scholar 

  • MAGHERINI, P. C. & PRECHT, W. (1976) Evidence for electrotonic coupling between frog motoneurons in the in situ spinal cord. Journal of Neurophysiology 39, 47–483.

    PubMed  Google Scholar 

  • MCARDLE, J. J. (1975) Complex end-plate potentials at the regenerating neuromuscular junction of the rat. Experimental Neurology 49, 2–63.

    Google Scholar 

  • MILNER, L. D. & LANDMESSER, L. T. (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. Journal of Neuroscience 19, 300–3022.

    PubMed  Google Scholar 

  • MOODY, W. J., SIMONCINI, L. COOMBS, J. L., SPRUCE, A. E. & VILLAZ, M. (1991) Development of ion channels in early embryos. Journal of Neurobiology 22, 67–684.

    PubMed  Google Scholar 

  • MOODY-CORBETT, F. & GILBERT, R. (1992) Two classes of potassium currents in Xenopus muscle cells in young cultures. Neuroreport 3, 31–322.

    PubMed  Google Scholar 

  • MOODY-CORBETT, F., GILBERT, R., AKBARALI, H. & HALL, J. (1989) Calcium current in embryonic Xenopus muscle cells in culture. Canadian Journal of Physiology and Pharmacology 67, 125–1264.

    PubMed  Google Scholar 

  • NASLEDOV, G. A., KATINA, I. E., TERENTYEV, D. A., TOMILIN, N. V. & LUKYANENKO, V. I. (1999) Development of muscle-specific features in cultured frog embryonic skeletal myocytes. Journal of Muscle Research and Cell Motility 20, 51–527.

    PubMed  Google Scholar 

  • NAVARRETE, R. & VRBOVÁ, G. (1993) Activitydependent interactions between motoneurones and muscles: Their role in the development of the motor unit. Progress in Neurobiology 41, 9–124.

    PubMed  Google Scholar 

  • NELSON, P. G., FIELDS, R. D. & LIU, Y. (1995) Neural activity, neuron-glia relationships, and synapse development. Perspectives in Developmental Neurobiology 2, 39–407.

    Google Scholar 

  • NGUYEN, Q. T., PARSADANIAN, A. S., SNIDER, W. D. & LICHTMAN, J. W. (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279, 172–1729.

    PubMed  Google Scholar 

  • NIEUWKOOP, P. D. & FABER, J. (1994) Normal Table of Xenopus laevis (Daudin): A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. New York: Garland, 252 pp.

    Google Scholar 

  • NUDELL, B. M. & GRINNELL, A. D. (1983) Regulation of synaptic position, size, and strength in anuran skeletal muscle. Journal of Neuroscience 3, 16–176.

    PubMed  Google Scholar 

  • O'DONOVAN, M. J. (1999) The origin of spontaneous activity in developing networks of the vertebrate nervous system. Current Opinion in Neurobiology 9, 9–104.

    PubMed  Google Scholar 

  • O'MALLEY, J. P., MANISHA, T. W. & BALICEGORDON, R. J. (1999) In vivo observations of terminal Schwann cells at normal, denervated, and reinnervated mouse neuromuscular junctions. Journal of Neurobiology 38, 27–286.

    PubMed  Google Scholar 

  • PECOT-DECHAVASSINE, M., WERNIG, A. & STOVER, H. (1979) A combined silver and cholinesterase method for studying exact relations between the pre-and the postsynaptic elements at the frog neuromuscular junction. Stain Technology 54, 2–28.

    PubMed  Google Scholar 

  • PERRINS, R. & ROBERTS, A. (1995a) Cholinergic and electrical synapses between synergistic spinal motoneurons in the Xenopus laevis embryo. Journal of Physiology 485, 13–144.

    PubMed  Google Scholar 

  • PERRINS, R. & ROBERTS, A. (1995b) Cholinergic and electrical motoneuron-to-motoneuron synapses contribute to on-cycle excitation during swimming in Xenopus embryos. Journal of Neurophysiology 73, 100–1012.

    PubMed  Google Scholar 

  • PERSONIUS, K. E. & BALICE-GORDON, R. J. (2001) Loss of correlated motor neuron activity during synaptic competition at developing neuromuscular synapses. Neuron 31, 39–408.

    PubMed  Google Scholar 

  • PITAEVSKI, V. & HERRERA, A. A. (1999) Focal application of ?-bungarotoxin leads to long-lasting suppression of neurotransmitter release in frog neuromuscular junctions. Society for Neuroscience Abstracts 25, 1022.

    Google Scholar 

  • PLOMP, J. J. & MOLENAAR, P. C. (1996) Involvement of protein kinases in the upregulation of acetylcholine release at endplates of alpha-bungarotoxin-treated rats. Journal of Physiology 493, 17–186.

    PubMed  Google Scholar 

  • 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. Journal of Physiology 478, 12–136.

    PubMed  Google Scholar 

  • POCKETT, S. & SLACK, J. R. (1983) Ability of motoneurons to regulate quantal release and terminal growth after reduction in motor unit size. Brain Research 258, 29– 298.

    PubMed  Google Scholar 

  • PRABHAKAR, E., BARNES, T. & SPRUCE, A. E. (1996) A neural influence on the appearance of sodium current in Xenopus embryonic myocytes. Neuroscience Letters 207, 20–205.

    PubMed  Google Scholar 

  • PURVES, D. & HUME, R. I. (1981) The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells. Journal of Neuroscience 1, 44–452.

    PubMed  Google Scholar 

  • REDDY, L. V., KOIRALA, S. & KO, C.-P. (1999) Selective ablation of perisynaptic Schwann cells (PSCs) from the frog neuromuscular junction (NMJ) in vivo. Society for Neuroscience Abstracts 25, 2032.

    Google Scholar 

  • REYNOLDS, M. L. & WOOLF, C. J. (1992) Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. Journal of Neurocytology 21, 5–66.

    PubMed  Google Scholar 

  • RIBCHESTER, R. R. & TAXT, T. (1983) Motor unit size and synaptic competition in rat lumbrical muscles reinnervated by active and inactive motor axons. Journal of Physiology 344, 8–111.

    PubMed  Google Scholar 

  • RIBERA, A. B. & SPITZER, N. C. (1991) Differentiation of delayed rectifier potassium current in embryonic amphibian myocytes. Developmental Biology 144, 11–128.

    PubMed  Google Scholar 

  • RICH, M. M. & LICHTMAN, J. W. (1989) In vivo visualization of pre-and postsynaptic changes during synapse elimination in reinnervated mouse muscles. Journal of Neuroscience 9, 178–1805.

    PubMed  Google Scholar 

  • RIDGE, R. M. A. P. & BETZ, W. J. (1984) The effect of selective chronic stimulation on motor unit size in developing rat muscle. Journal of Neuroscience 4, 261–2620.

    PubMed  Google Scholar 

  • ROCHEL, S. & ROBBINS, N. (1988) The effects of partial denervation and terminal field expansion on motor nerve terminal structure and function. Journal of Neuroscience 8, 33–338.

    PubMed  Google Scholar 

  • SAINT-AMANT, L. & DRAPEAU, P. (2000) Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. Journal of Neuroscience 20, 396–3972.

    PubMed  Google Scholar 

  • SANES, J. R. & LICHTMAN J. W. (1999) Development of the vertebrate neuromuscular junction. Annual Review of Neuroscience 22, 38–442.

    PubMed  Google Scholar 

  • SCHMALBRUCH, H. (1982) Skeletal muscle fibers of newborn rats are coupled through gap junctions. Developmental Biology 91, 48–490.

    PubMed  Google Scholar 

  • SILLAR, K. T. & SIMMERS, A. J. (1994a) Oscillatory membrane properties of spinal cord neurons that are active during fictive swimming in Rana temporaria embryos. European Journal of Morphology 32, 18–192.

    PubMed  Google Scholar 

  • SILLAR, K. T. & SIMMERS, A. J. (1994b) Electrical coupling and intrinsic neuronal oscillators in Rana temporaria spinal cord. European Journal of Morphology 32, 29–298.

    PubMed  Google Scholar 

  • SON, Y.-J. & THOMPSON, W. J. (1995a) Schwann cell processes guide regeneration of peripheral axons. Neuron 14, 12–132.

    PubMed  Google Scholar 

  • SON, Y.-J. & THOMPSON, W. J. (1995b) Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14, 13–141.

    PubMed  Google Scholar 

  • SON, Y. J., TRACHTENBERG, J. T. & THOMPSON, W. J. (1996) Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends in Neuroscience 19, 28–285.

    PubMed  Google Scholar 

  • SONNHOF, U., RICHTER, D. W. & TAUGNER, R. (1977) Electrotonic coupling between frog spinal motoneurons. An electrophysiological and morphological study. Brain Research 138, 19–215.

    PubMed  Google Scholar 

  • SPITZER, N. C. (1991) A developmental handshake: Neuronal control of ionic currents and their control of neuronal differentiation. Journal of Neurobiology 22, 65– 673.

    PubMed  Google Scholar 

  • SPITZER, N. C., VINCENT, A. & LAUTERMILCH, N. J. (2000) Differentiation of electrical excitability in motoneurons. Brain Research Bulletin 53, 54–552.

    PubMed  Google Scholar 

  • SPRUCE, A. E. & MOODY, W. J. (1992) Developmental sequence of expression of voltage-dependent currents in embryonic Xenopus laevis myotcytes. Developmental Biology 154, 1–22.

    PubMed  Google Scholar 

  • STANCO, A. M. & WERLE, M. J. (1997) Agrin and acetylcholine receptors are removed from abandoned synaptic sites at reinnervated frog neuromuscular junctions. Journal of Neurobiology 33, 99–1018.

    PubMed  Google Scholar 

  • STENT, G. (1973) Aphysiological mechanism for Hebb's postulate of learning. Proceedings of the National Academy of Sciences, USA 70, 99–1001.

    Google Scholar 

  • STOOP, R. & POO, M.-M. (1996) Synaptic modulation by neurotrophic factors: Differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. Journal of Neuroscience 16, 325–3264.

    PubMed  Google Scholar 

  • TAUGNER, R., SONNHOF, U., RICHTER, D. W. & SCHILLER, A. (1978) Mixed (chemical and electrical) synapses on frog spinal motoneurons. Cell and Tissue Research 193, 4–59.

    PubMed  Google Scholar 

  • THOMPSON, W. J. (1983) Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use. Nature 302, 61–616.

    PubMed  Google Scholar 

  • THOMPSON, W. J. (1985) Activity and synapse elimination at the neuromuscular junction. Cellular and Molecular Neurobiology 5, 16–182.

    PubMed  Google Scholar 

  • THOMPSON, W. & JANSEN, J. K. S. (1977) The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2, 52–535.

    PubMed  Google Scholar 

  • TRACHTENBERG, J. T. & THOMPSON, W. J. (1997) Nerve terminal withdrawal from rat neuromuscular junctions induced by neuregulin and Schwann cells. Journal of Neuroscience 17, 624–6255.

    PubMed  Google Scholar 

  • TRESCH, M. C. & KIEHN, O. (2000) Motor coordination without action potentials in the mammalian spinal cord. Nature Neuroscience 3, 59–599.

    PubMed  Google Scholar 

  • TRESCH, M. C. & KIEHN, O. (2002) Synchronization of motor neurons during locomotion in the neonatal rat: Predictors and mechanisms. Journal of Neuroscience 22, 999–10008.

    PubMed  Google Scholar 

  • TYC, F. & VRBOVÁ, G. (1995) Stabilization of neuromuscular junctions by leupeptin increases motor unit size in partially denervated rat muscles. Developmental Brain Research 88, 18–193.

    PubMed  Google Scholar 

  • VAN SAUN, M. & WERLE, M. J. (2000) Matrix metalloproteinase-3 removes agrin from synaptic basal lamina. Journal of Neurobiology 43, 14–149.

    PubMed  Google Scholar 

  • WALSH, M. K. & LICHTMAN, J. W. (2003) In vivo timelapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37, 6–73.

    PubMed  Google Scholar 

  • WAN, J.-J. & POO, M.-M. (1999) Activity-induced potentiation of developing neuromuscular synapses. Science 285, 172–1728.

    PubMed  Google Scholar 

  • WANG, X.-H. & POO, M.-M. (1997) Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron 19, 82–835.

    PubMed  Google Scholar 

  • WANG, T., XIE, Z. & LU, B. (1995) Nitric oxide mediates activity dependent synaptic suppression at developing neuromuscular synapses. Nature 374, 26–266.

    PubMed  Google Scholar 

  • WERLE, M. J. & HERRERA, A. A. (1987) Synaptic competition and the persistence of polyneuronal innervation at frog neuromuscular junctions. Journal of Neurobiology 18, 37–389.

    PubMed  Google Scholar 

  • WERLE, M. J. & HERRERA, A. A. (1988) Synaptic competition and the elimination of polyneuronal innervation following reinnervation of adult frog sartorius muscles. Journal of Neurobiology 19, 46–481.

    PubMed  Google Scholar 

  • WERLE, M. J. & SOJKA, M. M. (1996) Anti-agrin staining is absent at abandoned synaptic sites of frog neuromuscular junctions. Journal of Neurobiology 30, 29–302.

    PubMed  Google Scholar 

  • WESTERFIELD, M. & FRANK, E. (1982) Specificity of electrical coupling among neurons innervating forelimb muscles of the adult bullfrog. Journal of Neurophysiology 48, 90–913.

    PubMed  Google Scholar 

  • WOLDEYESUS, M. T., BRITSCH, S., RIETHMACHER, D., XU, L., SONNENBERG-RIETHMACHER, E., ABOU-REBYEH, F., HARVEY, R., CARONI, P. & BIRCHMEIER, C. (1999) Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes & Development 13, 253– 2548.

    Google Scholar 

  • XIE, K., WANG, T. OLAFSSON, MIZUNO, K. & LU, B. (1997) Activity-dependent expression of NT-3 in muscle cells in culture: Implications in the development of neuromuscular junctions. Journal of Neuroscience 17, 294–2958.

    PubMed  Google Scholar 

  • ZHAO, F.-Y., WOLF, E. & ROBERTS, A. (1998) Longitudinal distribution of components of excitatory synaptic input to motoneurones during swimming in young Xenopus tadpoles: Experiments with antagonists. Journal of Physiology 511, 88–901.

    PubMed  Google Scholar 

  • ZOUBINE, M. N., MA, J. Y., SMIRNOVA, I. V., CITRON, B. A. & FESTOFF, B. W. (1996) Amolecular mechanism for synapse elimination: Novel inhibition of locally generated thrombin delays synapse loss in neonatal mouse muscle. Developmental Biology 179, 44–457.

    PubMed  Google Scholar 

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  1. Neurobiology Section, Department of Biological Sciences, University of Southern California, Los Angeles, CA, 90089-2520, USA

    Albert A. Herrera & Yu Zeng

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Herrera, A.A., Zeng, Y. Activity-dependent switch from synapse formation to synapse elimination during development of neuromuscular junctions. J Neurocytol 32, 817–833 (2003). https://doi.org/10.1023/B:NEUR.0000020626.29900.fb

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