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Multiple Innervation Of Tonic Endplates Revealed By Activity-dependent Uptake Of Fluorescent Probes

J. Lichtman, R. Wilkinson, M. Rich
Published 1985 · Biology, Medicine

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During development of the vertebrate nervous system, there is a widespread reduction in the number of axons innervating target cells1. This phenomenon, often called synapse elimination, has been particularly well studied at the neuromuscular junction of developing twitch muscle fibres2,3: following a period of polyneuronal innervation, axonal branches are retracted, usually leaving each twitch fibre endplate innervated by only one axon. Here we describe a hew technique for the study of synapse elimination—activity-mediated uptake of fluorescent probes. These probes selectively and supravitally label all the terminals of individual axons. The technique is used here in adult and embryonic snakes to study the innervation pattern of a thin muscle containing two fibre types: twitch fibres, which are fast-contracting and have propagated action potentials, and tonic fibres, which are slow-contracting and lack action potentials. We find that twitch muscle fibres, as expected, eliminate all polyneuronal innervation during development; in contrast, tonic fibre endplates remain polyneuronally innervated into adulthood. The persistence of multiple innervation at tonic endplates may be related to the lack of action potential activity in tonic muscle fibres.
This paper references
10.1113/jphysiol.1979.sp012733
Dual innervation of end‐plate sites and its consequences for neuromuscular transmission in muscles of adult Xenopus laevis.
D. Angaut-Petit (1979)
10.1038/302614A0
Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use
W. Thompson (1983)
10.1007/BF01257985
The effect of postsynaptic block on development of the neuromuscular junction in postnatal rats
M. Duxson (1982)
10.1113/jphysiol.1974.sp010670
The formation of synapses in striated muscle during development
M. Bennett (1974)
10.1126/SCIENCE.6206565
Illumination induces dye incorporation in photoreceptor cells.
M. Wilcox (1984)
10.1016/0306-4522(79)90088-5
The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers
W. Thompson (1979)
10.1113/jphysiol.1971.sp009578
Different types of extrafusal muscle fibres in snake costocutaneous muscles
R. Ridge (1971)
10.1038/310053A0
Staining of living presynaptic nerve terminals with selective fluorescent dyes
D. Yoshikami (1984)
10.1113/jphysiol.1978.sp012482
Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle.
R. O'brien (1978)
10.1016/0300-9629(85)90519-5
Principles of neural development
D. Purves (1985)
10.1126/SCIENCE.7414326
Elimination of synapses in the developing nervous system.
D. Purves (1980)
10.1083/JCB.57.2.315
EVIDENCE FOR RECYCLING OF SYNAPTIC VESICLE MEMBRANE DURING TRANSMITTER RELEASE AT THE FROG NEUROMUSCULAR JUNCTION
J. Heuser (1973)
10.1016/0022-1759(81)90183-6
A simple method of reducing the fading of immunofluorescence during microscopy.
G. Johnson (1981)
10.1152/PHYSREV.1970.50.1.40
Vertebrate slow muscle fibers.
A. Hess (1970)
10.1016/0006-8993(78)90760-6
Tenotomy delays the postnatal development of the motor innervation of the rat soleus
Dan A. Riley (1978)
10.2307/1440898
Stages in the Normal Development of the Common Garter Snake, Thamnophis sirtalis sirtalis
David R. Zehr (1962)
10.1038/264705A0
Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks
J. Changeux (1976)
10.1113/jphysiol.1981.sp013869
Restoration of focal multiple innervation in rat muscles by transmission block during a critical stage of development
M. C. Brown (1981)
10.1523/JNEUROSCI.04-10-02614.1984
The effect of selective, chronic stimulation on motor unit size in developing rat muscle
R. Ridge (1984)
10.1007/978-1-4684-1131-7_10
Neuromuscular Synapse Elimination
D. Essen (1982)
10.1016/0006-8993(75)90036-0
Consequences of tenotomy on the evolution of multiineervation in developing rat soleus muscle
P. Benoit (1975)



This paper is referenced by
10.1016/0968-0004(88)90015-1
Antigen processing: an interim report.
S. K. Pierce (1988)
10.1111/j.1471-4159.2006.03987.x
Kiss‐and‐run and full‐collapse fusion as modes of exo‐endocytosis in neurosecretion
N. Harata (2006)
10.1113/jphysiol.1987.sp016827
Properties of motor units in the transversus abdominis muscle of the garter snake.
J. Lichtman (1987)
10.1016/0896-6273(93)90110-D
Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions
R. Balice-Gordon (1993)
10.1023/B:NEUR.0000020605.20628.A3
Maintenance of transmitter release from neuromuscular junctions with different patterns of usage ‘in vivo’
G. Bewick (2003)
10.1113/jphysiol.1989.sp017827
Inhibitory interactions between motoneurone terminals in neonatal rat lumbrical muscle.
W. Betz (1989)
10.1016/S1044-5781(06)80029-0
Synapse disassembly at the neuromuscular junction
J. Lichtman (1995)
10.1002/AR.1092170102
Spatial distribution of twitch and tonic fibres in a snake muscle one myofibre thick
A. J. Robinson (1987)
10.3389/fnmol.2012.00012
Presynaptic Active Zone Density during Development and Synaptic Plasticity
G. L. Clarke (2012)
10.1016/S0896-6273(00)00031-3
Multicolor “DiOlistic” Labeling of the Nervous System Using Lipophilic Dye Combinations
W. Gan (2000)
10.1016/S0079-6123(03)43009-4
Rhythm generation for food-ingestive movements.
Y. Nakamura (2004)
10.1016/0166-2236(86)90159-1
Pathways to progress-the rise of modern neuroanatomical techniques
E. Jones (1986)
10.1023/B:NEUR.0000020608.82235.3E
The nerve-muscle synapse of the garter snake
R. Wilkinson (2003)
The role of neuroplasticity in the response to drugs.
D. Friedman (1987)
10.1111/j.1469-7793.2003.00103.x
‘Delayed’ endocytosis is regulated by extracellular Ca2+ in snake motor boutons
H. Teng (2003)
10.1016/S0959-4388(96)80121-8
Imaging exocytosis and endocytosis
W. Betz (1996)
10.1023/B:NEUR.0000020609.19873.E8
Monitoring synaptic vesicle recycling in frog motor nerve terminals with FM dyes
S. Rizzoli (2003)
10.1113/jphysiol.1992.sp019049
Regulation of single quantal efficacy at the snake neuromuscular junction.
R. Wilkinson (1992)
10.1113/jphysiol.1996.sp021610
Release properties of isolated neuromuscular boutons of the garter snake.
R. Wilkinson (1996)
10.1016/S0896-6273(00)80893-4
Synapse Elimination and Indelible Memory
J. Lichtman (2000)
10.1007/s002210100782
Anatomical evidence for brainstem circuits mediating feeding motor programs in the leopard frog, Rana pipiens
C. W. Anderson (2001)
10.1016/S0166-2236(00)02030-0
Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling
N. Harata (2001)
10.1038/nn.3578
Visualizing presynaptic function
E. Kavalali (2014)
10.1002/NEU.480210107
Understanding synaptic competition in theory and in practice.
J. Lichtman (1990)
10.1007/978-1-4615-3560-7_30
Movement Primitives in the Frog Spinal Cord
S. F. Giszter (1993)
10.1016/S0166-2236(02)02233-6
Response: Raising the speed limit
Knut Holthoff (2002)
10.1016/J.YMETH.2004.01.002
Using FM1-43 to study neuropeptide granule dynamics and exocytosis.
Audrey C. Brumback (2004)
10.1038/nprot.2006.476
Imaging synaptic vesicle exocytosis and endocytosis with FM dyes
Michael A. Gaffield (2007)
10.1007/BF00228693
In vitro eye-blink reflex model: role of excitatory amino acids and labeling of network activity with sulforhodamine
J. Keifer (2004)
10.1016/S0959-4388(96)80015-8
Mechanism of synapse disassembly at the developing neuromuscular junction
Q. T. Nguyen (1996)
10.1016/j.ceca.2017.01.002
Probes for monitoring regulated exocytosis.
W. Li (2017)
10.1016/0165-0270(95)00135-2
A quantitative fluorescence-imaging technique for studying acetylcholine receptor turnover at neuromuscular junctions in living animals
S. G. Turney (1996)
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