Abstract
A study has been made of the formation of synaptic terminals from long processes formed at the end of motor nerve branches of endplates in mature amphibian (Bufo marinus) muscle. Injection of fluorescent dyes into individual motor axons showed the full extent of their branches at single endplates. Synaptic vesicle clusters at these branches were identified with styryl dyes. Some terminal branches consisted of well separated varicosities, each possessing a cluster of functioning synaptic vesicles whilst others formed by the same axon consisted of closely spaced clusters of vesicles in a branch of approximately uniform diameter. All the varicosities gave rise to calcium transients on stimulation of their parent axon. Both types of branches sometimes possessed short processes (<5 μm long) or very long thin processes (>10 μm long) which ended in a bulb that possessed a functional synaptic vesicle cluster. These thin processes could move and form a varicosity along their length in less than 30 min.
Injection of a fluorescent dye into terminal Schwann cells (TSCs) at an endplate showed that they also possessed very long thin processes (>10 μm long) which could move over relatively short times (<30 min). Injecting fluorescent dyes into both axons and their associated TSCs showed that on some occasions long TSC processes were accompanied by a long nerve terminal process and at other times they were not. It is suggested that the mature motor-nerve terminal is a dynamic structure in which the formation of processes by TSCs guides nerve terminal sprouting.
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AHMARI, S. E., BUCHANAN, J. & SMITH, S. J. (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nature Neuroscience 3, 445–451.
ANZIL, A. P., BIESER, A. & WERNIG, A. (1984) Light and electron microscopic identification of nerve terminal sprouting and retraction in normal adult frog muscle. Journal of Physiology 350, 393–399.
ASTROW, S. H., QUIANG, H. & KO, C. P. (1998) Perisynaptic Schwann cells at the neuromuscular junctions revealed by a novel monoclonal antibody. Journal of Neurocytology 27, 667–681.
BALICE-GORDON, R. J. & LICHTMAN, J. W. (1990) In vivo visualization of the growth of pre-and postsynaptic elements of neuromuscular junctions in the mouse. Journal of Neuroscience 10, 894–908.
BENNETT, M. R., KARUNITHI, S. & LAVIDIS, N. A. (1991) Probabilistic secretion of quanta from nerve terminals in toad (Bufo marinus) muscle modulated by adenosine. Journal of Physiology 433, 421–434.
BENNETT, M. R., LAVIDIS, N. A. & LAVIDIS-ARMSON, F. (1989) The probability of quantal secretion at release sites of different length in toad (Bufo marinus) muscle. Journal of Physiology 418, 235–249.
BETZ, W. J., BEWICK, G. S. & RIDGE, R. M. (1992a) Intracellular movements of fluorescently labeled synaptic vesicles in frog motor nerve terminals during nerve stimulation. Neuron 9, 805–813.
BETZ, W. J., MAO, F. & BEWICK, G. S. (1992b) Activitydependent fluorescent staining and destaining of living vertebrate motor nerve terminals. Journal of Neuroscience 12, 363–375.
BIRKS, R., KATZ, B. & MILEDI, R. (1960) Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration. Journal of Physiology 150, 145–168.
CHEN, L. L., FOLSOM, D. B. & KO, C. P. (1991) The remodeling of synaptic extracellular matrix and its dynamic relationship with nerve terminals at living frog neuromuscular junctions. Journal of Neuroscience 11, 2920–2930.
DAI, Z. & PENG, H. B. (1998) Fluorescence microscopy of calcium and synaptic vesicle dynamics during synapse formation in tissue culture. Histochemical Journal 30, 189–196.
D'ALONZO, A. J. & GRINNELL, A. D. (1985) Profiles of evoked release along the length of frog motor-nerve terminals. Journal of Physiology 359, 235–258.
DIAZ, J., MOLGO, J. & PECOT-DECHAVASSINE, M. (1989) Sprouting of frog motor nerve terminals after longterm paralysis by botulinum type A toxin. Neuroscience Letters 96, 127–132.
DIAZ, J. & PECOT-DECHAVASSINE, M. (1989) Terminal nerve sprouting at the frog neuromuscular junction induced by prolonged tetrodotoxin blockade of nerve conduction. Journal of Neurocytology 18, 39–46.
DIEFENBACH, T. J., GUTHRIE, P. R., STIER, H., BILLUPS, B. & KATER, S. B. (1999) Membrane recycling in the neuronal growth cone revealed by FM1-43 labeling. Journal of Neuroscience 19, 9436–9444.
ECKER, A. (1889) The anatomy of the frog, pp96, 109. Amsterdam: Asher.
HARRIS, L. W. & PURVES, D. (1989) Rapid remodeling of sensory endings in the corneas of living mice. Journal of Neuroscience 9, 2210–2214.
HATADA, Y., WU, F., SILVERMAN, R., SCHACHER, S. & GOLDBERG, D. I. (1999) En passant synaptic varicosities form directly from growth cones by transient cessation of growth cone advance but not of actin-based motility. Journal of Neurobiology 41, 242–251.
HERRERA, A. A., BANNER, L. R. & NAGAYA, N. (1990) Repeated, in vivo observation of frog neuromuscular junctions: Remodeling involves concurrent growth and retraction. Journal of Neurocytology 19, 85–99.
HERRERA, A. A., QUIANG, H. & KO, C. P. (2000) The role of perisynaptic Schwann cells in development of neuromuscular junctions in the frog (Xenopus laevis). Journal of Neurobiology 45, 237–254.
HILL, R. R. & ROBBINS, N. (1991) Mode of enlargement of young mouse neuromuscular junctions observed repeatedly in vivo with visualization of pre-and postsynaptic borders. Journal of Neurocytology 20, 183–194.
KO, C. P. (1981) Electrophysiological and free-fracture studied of changes following denervation at frog neuromuscular junctions. Journal of Physiology 321, 627–639.
KO, C. P. (1984) Regeneration of the active zone at the frog neuromuscular junction. Journal of Cell Biology 98, 1685–1695.
KO, C. P. (1985) Formation of the active zone at developing neuromuscular junctions in larval and adult bullfrogs. Journal of Neurocytology 14, 487–512.
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, 1780–1790.
KOIRALA, S., QIANG, H. & KO, C. P. (2000) Reciprocal interactions between perisynaptic Schwann cells and regenerating nerve terminals at the frog neuromuscular junction. Journal of Neurobiology 5, 343–360.
LICHTMAN, J. W., MAGRASSI, L. & PURVES, D. (1987) Visualization of neuromuscular junctions over periods of several months in living mice. Journal of Neuroscience 7, 1215–1222.
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, 2380–2392.
MACLEOD, G. T., GAN, J. & BENNETT, M. R. (1999) Vesicle-associated proteins and quantal release at single active zones of amphibian (Bufo marinus) motornerve terminals. Journal of Neurophysiology 82, 1133–1146.
MANDELL, J. W., MACLEISH, P. R. & TOWNESANDERSON, E. (1993) Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro. Journal of Neuroscience 13, 3533–3548.
O'MALLEY, J. P., WARAN, M. T. & BALICE-GORDON, R. J. (1999) In vivo observations of terminal Schwann cells at normal, denervated, and reinnervated mouse neuromuscular junctions. Journal of Neurobiology 38, 270–286.
PURVES, D., VOYVIDIC, J. T., MAGRASSI, L. & YAWO H. (1987) Nerve terminal remodeling visualized in living mice by repeated examination of the same neuron. Science 238, 1122–1126.
ROBBINS, N. & POLAK, J. (1988) Filopodia, lamellipodia and retractions at mouse neuromuscular junctions. Journal of Neurocytology 17, 545–561.
SON, Y. J. & THOMPSON, W. J. (1995) Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14, 133–141.
WERNIG, A., PECOT-DECHAVASSINE, M. & STOVER, H. (1980) Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare. Journal of Neurocytology 9, 278–303.
WIGSTON, D. J. (1989) Remodeling of neuromuscular junctions in adult mouse soleus. Journal of Neuroscience 9, 639–647.
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Dickens, P., Hill, P. & Bennett, M.R. Schwann cell dynamics with respect to newly formed motor—nerve terminal branches on mature (Bufo marinus) muscle fibers. J Neurocytol 32, 381–392 (2003). https://doi.org/10.1023/B:NEUR.0000011332.96472.b2
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DOI: https://doi.org/10.1023/B:NEUR.0000011332.96472.b2