 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 9, 1523-1539, Copyright © 1989 by Society for Neuroscience
Studies of nerve-muscle interactions in Xenopus cell culture: analysis of early synaptic currents
J Evers, M Laser, YA Sun, ZP Xie and MM Poo
Section of Molecular Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510.
We have studied the spontaneous and nerve-evoked synaptic currents during
the initial period of nerve-muscle contact in Xenopus cell cultures. The
precise timing of the contact was achieved by physically manipulating
embryonic muscle cells into contact with co-cultured spinal neurons.
Previous studies have shown that physical contact of the muscle membrane
induces pulsatile release of acetylcholine (ACh) from the growth cone of
these neurons, resulting in spontaneous synaptic currents (SSCs) in the
muscle cell within seconds following the contact. In the present work, we
first showed that these SSCs at the manipulated nerve-muscle contacts are
similar to those observed at naturally occurring synapses. We then examined
the possible cellular mechanisms responsible for the marked variation in
SSC amplitude and showed that it most likely results from differences in
either the amount of ACh contained in each release event or the extent of
close membrane apposition near the release sites. During the first 20 min
following the nerve-muscle contact, there was an increase in the frequency
and mean amplitude of the SSCs. During a similar period, the evoked
synaptic currents (ESCs), which were induced by suprathreshold electrical
stimulation of the neuronal soma, also showed an increase in the mean
amplitude and a reduction in the delay of onset following the stimulus.
These postcontact changes in the efficacy of synaptic transmission may be
related to an increase in the total area of close membrane apposition
between the nerve and muscle cells. This was suggested by the finding that
neurite-muscle adhesion increases over a similar postcontact period. The
transition from low- to high-efficacy transmission during the early phase
of contact may reflect the process of selective adhesion between the cells,
and thus signify the formation of specific synapse. Analysis of the
fluctuation in the ESC amplitude at the early nerve-muscle contact suggests
that evoked release of ACh occurs as multiples of a quantal unit. However,
this unit is apparently related to only a small subpopulation of SSCs of
relatively high amplitudes.(ABSTRACT TRUNCATED AT 400 WORDS)
This article has been cited by other articles:
|
|
|
|
 
G. Cao and C.-P. Ko
Schwann Cell-Derived Factors Modulate Synaptic Activities at Developing Neuromuscular Synapses
J. Neurosci.,
June 20, 2007;
27(25):
6712 - 6722.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-C. Liou, S.-Y. Ho, M.-R. Shen, Y.-P. Liao, W.-T. Chiu, and K.-H. Kang
A rapid, nongenomic pathway facilitates the synaptic transmission induced by retinoic acid at the developing synapse
J. Cell Sci.,
October 15, 2005;
118(20):
4721 - 4730.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Okamoto, T. Tamura, K. Suzuki, and Y. Kidokoro
External Ca2+ Dependency of Synaptic Transmission in Drosophila synaptotagmin I Mutants
J Neurophysiol,
August 1, 2005;
94(2):
1574 - 1586.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y.-P. Liao, S.-Y. Ho, and J.-C. Liou
Non-genomic regulation of transmitter release by retinoic acid at developing motoneurons in Xenopus cell culture
J. Cell Sci.,
June 15, 2004;
117(14):
2917 - 2924.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Lefebvre, F. Ono, C. Puglielli, G. Seidner, C. Franzini-Armstrong, P. Brehm, and M. Granato
Increased neuromuscular activity causes axonal defects and muscular degeneration
Development,
June 1, 2004;
131(11):
2605 - 2618.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X.-P. Sun, B. Yazejian, and A. D. Grinnell
Electrophysiological properties of BK channels in Xenopus motor nerve terminals
J. Physiol.,
May 15, 2004;
557(1):
207 - 228.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. Li, F. Ono, and P. Brehm
Optical Measurements of Presynaptic Release in Mutant Zebrafish Lacking Postsynaptic Receptors
J. Neurosci.,
November 19, 2003;
23(33):
10467 - 10474.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Yamashita, T. Ishikawa, and T. Takahashi
Developmental Increase in Vesicular Glutamate Content Does Not Cause Saturation of AMPA Receptors at the Calyx of Held Synapse
J. Neurosci.,
May 1, 2003;
23(9):
3633 - 3638.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. M. Franks, C. F. Stevens, and T. J. Sejnowski
Independent Sources of Quantal Variability at Single Glutamatergic Synapses
J. Neurosci.,
April 15, 2003;
23(8):
3186 - 3195.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C.-Y. Wang, F. Yang, X.-P. He, H.-S. Je, J.-Z. Zhou, K. Eckermann, D. Kawamura, L. Feng, L. Shen, and B. Lu
Regulation of Neuromuscular Synapse Development by Glial Cell Line-derived Neurotrophic Factor and Neurturin
J. Biol. Chem.,
March 15, 2002;
277(12):
10614 - 10625.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-D. Yao, J. Rusch, M.-m. Poo, and C.-F. Wu
Spontaneous Acetylcholine Secretion from Developing Growth Cones of Drosophila Central Neurons in Culture: Effects of cAMP-Pathway Mutations
J. Neurosci.,
April 1, 2000;
20(7):
2626 - 2637.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Wan and M. Poo
Activity-Induced Potentiation of Developing Neuromuscular Synapses
Science,
September 10, 1999;
285(5434):
1725 - 1728.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
P. V. Nguyen, L. Aniksztejn, S. Catarsi, and P. Drapeau
Maturation of Neuromuscular Transmission During Early Development in Zebrafish
J Neurophysiol,
June 1, 1999;
81(6):
2852 - 2861.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Chang and S. V. Popov
Long-range signaling within growing neurites mediated by neurotrophin-3
PNAS,
March 30, 1999;
96(7):
4095 - 4100.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Zakharenko, S. Chang, M. O'Donoghue, and S. V. Popov
Neurotransmitter Secretion along Growing Nerve Processes: Comparison with Synaptic Vesicle Exocytosis
J. Cell Biol.,
February 8, 1999;
144(3):
507 - 518.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Song, G. Ming, Z. He, M. Lehmann, L. McKerracher, M. Tessier-Lavigne, and M. Poo
Conversion of Neuronal Growth Cone Responses from Repulsion to Attraction by Cyclic Nucleotides
Science,
September 4, 1998;
281(5382):
1515 - 1518.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
X.-h. Wang, B. Berninger, and M.-m. Poo
Localized Synaptic Actions of Neurotrophin-4
J. Neurosci.,
July 1, 1998;
18(13):
4985 - 4992.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. FITZSIMONDS and M.-M. POO
Retrograde Signaling in the Development and Modification of Synapses
Physiol Rev,
January 1, 1998;
78(1):
143 - 170.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. B. Lowen, S. S. Cash, M.-m. Poo, and M. C. Teich
Quantal Neurotransmitter Secretion Rate Exhibits Fractal Behavior
J. Neurosci.,
August 1, 1997;
17(15):
5666 - 5677.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. S. Hollrigel and I. Soltesz
Slow Kinetics of Miniature IPSCs during Early Postnatal Development in Granule Cells of the Dentate Gyrus
J. Neurosci.,
July 1, 1997;
17(13):
5119 - 5128.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Xie, T. Wang, P. Olafsson, K. Mizuno, and B. Lu
Activity-Dependent Expression of NT-3 in Muscle Cells in Culture: Implications in the Development of Neuromuscular Junctions
J. Neurosci.,
May 1, 1997;
17(9):
2947 - 2958.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Yazejian, D. A. DiGregorio, J. L. Vergara, R. E. Poage, S. D. Meriney, and A. D. Grinnell
Direct Measurements of Presynaptic Calcium and Calcium-Activated Potassium Currents Regulating Neurotransmitter Release at Cultured Xenopus Nerve-Muscle Synapses
J. Neurosci.,
May 1, 1997;
17(9):
2990 - 3001.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. D. Whim, H. Niemann, and L. K. Kaczmarek
The Secretion of Classical and Peptide Cotransmitters from a Single Presynaptic Neuron Involves a Synaptobrevin-Like Molecule
J. Neurosci.,
April 1, 1997;
17(7):
2338 - 2347.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-C. Liou and W.-M. Fu
Regulation of Quantal Secretion from Developing Motoneurons by Postsynaptic Activity-Dependent Release of NT-3
J. Neurosci.,
April 1, 1997;
17(7):
2459 - 2468.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Stoop and M.-m. Poo
Synaptic Modulation by Neurotrophic Factors: Differential and Synergistic Effects of Brain-Derived Neurotrophic Factor and Ciliary Neurotrophic Factor
J. Neurosci.,
May 15, 1996;
16(10):
3256 - 3264.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R Stoop and M. Poo
Potentiation of transmitter release by ciliary neurotrophic factor requires somatic signaling
Science,
February 3, 1995;
267(5198):
695 - 699.
[Abstract]
[PDF]
|
|
|
|
|
|
|
Y. Lo and M. Poo
Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses
Science,
November 15, 1991;
254(5034):
1019 - 1022.
[Abstract]
[PDF]
|
|
|
|
