 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, April 1, 2000, 20(7):2480-2494
Release-Independent Short-Term Synaptic Depression in Cultured Hippocampal Neurons
David L. Brody and David T. Yue The Johns Hopkins University School of Medicine, Departments of Biomedical Engineering and Neuroscience, Program in Molecular and Cellular Systems Physiology, Baltimore, Maryland 21205
Short-term synaptic plasticity may dramatically influence neuronal information transfer, yet the underlying mechanisms remain incompletely understood. In autapses (self-synapses) formed by cultured hippocampal neurons, short-term synaptic depression (STD) had several unusual features. (1) Reduction of neurotransmitter release probability with Cd2+, a blocker of voltage-gated calcium channels, did not change depression. (2) Lowering [Ca2+]o and/or raising [Mg2+]o had little effect on STD in cells with strong baseline depression, but in cells with more modest baseline depression, it reduced the depression. (3) Random variations in the size of initial EPSCs did not influence successive EPSC sizes. These findings were inconsistent with release-dependent mechanisms, such as vesicle depletion, post-synaptic receptor desensitization, and autoreceptor inhibition. Instead, other results suggested that changes in action potentials (APs) contributed to depression. The somatic APs declined in amplitude with repetitive stimulation, and modest reduction of AP amplitudes with tetrodotoxin inhibited EPSCs. Notably, tetrodotoxin also increased depression. Similar changes in axonal APs could produce STD in at least two ways. First, decreasing presynaptic spike amplitudes could reduce calcium entry and release probability. Alternatively, APs could fail to propagate through some axonal branches, reducing the number of active synapses. To explore these possibilities, we derived the expected variance of EPSCs for the two scenarios. Experimentally, the variance increased and then decreased on average with successive responses during trains of APs, confirming a unique prediction from the conduction failure scenario. Thus, STD had surprising properties, incompatible with commonly postulated mechanisms but consistent with AP conduction failure at axonal branches.
Key words: short-term synaptic plasticity; short-term synaptic depression; autapse; microisland; cell culture; hippocampus; cadmium; calcium; magnesium; correlation analysis; miniature EPSC; action potential; tetrodotoxin; variance analysis; simulation; branch-point failure; conduction failure; propagation failure
Copyright © 2000 Society for Neuroscience 0270-6474/00/2072480-15$05.00/0
This article has been cited by other articles:
A. W. Ballo and D. Bucher
Complex Intrinsic Membrane Properties and Dopamine Shape Spiking Activity in a Motor Axon
J. Neurosci., April 22, 2009; 29(16): 5062 - 5074.
[Abstract] [Full Text] [PDF]
J. E. Rubin, J. A. Hayes, J. L. Mendenhall, and C. A. Del Negro
Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations
PNAS, February 24, 2009; 106(8): 2939 - 2944.
[Abstract] [Full Text] [PDF]
C. F. Stevens and J. H. Williams
Discharge of the Readily Releasable Pool With Action Potentials at Hippocampal Synapses
J Neurophysiol, December 1, 2007; 98(6): 3221 - 3229.
[Abstract] [Full Text] [PDF]
M. Xie, X. Li, J. Han, D. L. Vogt, S. Wittemann, M. D. Mark, and S. Herlitze
Facilitation versus depression in cultured hippocampal neurons determined by targeting of Ca2+ channel Cav{beta}4 versus Cav{beta}2 subunits to synaptic terminals
J. Cell Biol., July 24, 2007; 178(3): 489 - 502.
[Abstract] [Full Text] [PDF]
G. B. Awatramani, J. D. Boyd, K. R. Delaney, and T. H. Murphy
Effective release rates at single rat Schaffer collateral-CA1 synapses during sustained theta-burst activity revealed by optical imaging
J. Physiol., July 15, 2007; 582(2): 583 - 595.
[Abstract] [Full Text] [PDF]
S. Meunier, J. Kwon, H. Russmann, S. Ravindran, R. Mazzocchio, and L. Cohen
Spinal use-dependent plasticity of synaptic transmission in humans after a single cycling session
J. Physiol., March 1, 2007; 579(2): 375 - 388.
[Abstract] [Full Text] [PDF]
H. Tokuoka and Y. Goda
Myosin Light Chain Kinase Is Not a Regulator of Synaptic Vesicle Trafficking during Repetitive Exocytosis in Cultured Hippocampal Neurons.
J. Neurosci., November 8, 2006; 26(45): 11606 - 11614.
[Abstract] [Full Text] [PDF]
K. L. Moulder and S. Mennerick
Synaptic Vesicles: Turning Reluctance Into Action
Neuroscientist, February 1, 2006; 12(1): 11 - 15.
[Abstract] [PDF]
H. Y. Sun, S. A Lyons, and L. E Dobrunz
Mechanisms of target-cell specific short-term plasticity at Schaffer collateral synapses onto interneurones versus pyramidal cells in juvenile rats
J. Physiol., November 1, 2005; 568(3): 815 - 840.
[Abstract] [Full Text] [PDF]
Y. Wu, F. Kawasaki, and R. W. Ordway
Properties of Short-Term Synaptic Depression at Larval Neuromuscular Synapses in Wild-Type and Temperature-Sensitive Paralytic Mutants of Drosophila
J Neurophysiol, May 1, 2005; 93(5): 2396 - 2405.
[Abstract] [Full Text] [PDF]
K. L. Moulder and S. Mennerick
Reluctant Vesicles Contribute to the Total Readily Releasable Pool in Glutamatergic Hippocampal Neurons
J. Neurosci., April 13, 2005; 25(15): 3842 - 3850.
[Abstract] [Full Text] [PDF]
A. F Soleng, A Baginskas, P Andersen, and M Raastad
Activity-dependent excitability changes in hippocampal CA3 cell Schaffer axons
J. Physiol., October 15, 2004; 560(2): 491 - 503.
[Abstract] [Full Text] [PDF]
J. Munoz-Cuevas, H. Vara, and A. Colino
Characterization of release-independent short-term depression in the juvenile rat hippocampus
J. Physiol., July 15, 2004; 558(2): 527 - 548.
[Abstract] [Full Text] [PDF]
G. Fuhrmann, A. Cowan, I. Segev, M. Tsodyks, and C. Stricker
Multiple mechanisms govern the dynamics of depression at neocortical synapses of young rats
J. Physiol., June 1, 2004; 557(2): 415 - 438.
[Abstract] [Full Text] [PDF]
G. Chen, N. C. Harata, and R. W. Tsien
From the Cover: Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses
PNAS, January 27, 2004; 101(4): 1063 - 1068.
[Abstract] [Full Text] [PDF]
Y. Otsu, V. Shahrezaei, B. Li, L. A. Raymond, K. R. Delaney, and T. H. Murphy
Competition between Phasic and Asynchronous Release for Recovered Synaptic Vesicles at Developing Hippocampal Autaptic Synapses
J. Neurosci., January 14, 2004; 24(2): 420 - 433.
[Abstract] [Full Text] [PDF]
G. Daoudal and D. Debanne
Long-Term Plasticity of Intrinsic Excitability: Learning Rules and Mechanisms
Learn. Mem., November 1, 2003; 10(6): 456 - 465.
[Abstract] [Full Text] [PDF]
C. Gu, Y. N. Jan, and L. Y. Jan
A Conserved Domain in Axonal Targeting of Kv1 (Shaker) Voltage-Gated Potassium Channels
Science, August 1, 2003; 301(5633): 646 - 649.
[Abstract] [Full Text] [PDF]
D. Debanne and M. Russier
Axonal propagation: does the spike stop here?
J. Physiol., May 1, 2003; 548(3): 663 - 663.
[Full Text] [PDF]
M. Raastad and G. M G Shepherd
Single-axon action potentials in the rat hippocampal cortex
J. Physiol., May 1, 2003; 548(3): 745 - 752.
[Abstract] [Full Text] [PDF]
C. M. Pedroarena and C. Schwarz
Efficacy and Short-Term Plasticity at GABAergic Synapses Between Purkinje and Cerebellar Nuclei Neurons
J Neurophysiol, February 1, 2003; 89(2): 704 - 715.
[Abstract] [Full Text] [PDF]
C. Saviane, L. P Savtchenko, G. Raffaelli, L. L Voronin, and E. Cherubini
Frequency-dependent shift from paired-pulse facilitation to paired-pulse depression at unitary CA3-CA3 synapses in the rat hippocampus
J. Physiol., October 15, 2002; 544(2): 469 - 476.
[Abstract] [Full Text] [PDF]
S. Kirischuk, J. D Clements, and R. Grantyn
Presynaptic and postsynaptic mechanisms underlie paired pulse depression at single GABAergic boutons in rat collicular cultures
J. Physiol., August 15, 2002; 543(1): 99 - 116.
[Abstract] [Full Text] [PDF]
Z. Xiang, J. R. Huguenard, and D. A. Prince
Synaptic Inhibition of Pyramidal Cells Evoked by Different Interneuronal Subtypes in Layer V of Rat Visual Cortex
J Neurophysiol, August 1, 2002; 88(2): 740 - 750.
[Abstract] [Full Text] [PDF]
J. H L Chan, C. S-Y Lin, E. Pierrot-Deseilligny, and D. Burke
Excitability changes in human peripheral nerve axons in a paradigm mimicking paired-pulse transcranial magnetic stimulation
J. Physiol., August 1, 2002; 542(3): 951 - 961.
[Abstract] [Full Text] [PDF]
M. Melis, R. Camarini, M. A. Ungless, and A. Bonci
Long-Lasting Potentiation of GABAergic Synapses in Dopamine Neurons after a Single In Vivo Ethanol Exposure
J. Neurosci., March 15, 2002; 22(6): 2074 - 2082.
[Abstract] [Full Text] [PDF]
T. D. Gover, X.-Y. Jiang, and T. W. Abrams
Persistent, Exocytosis-Independent Silencing of Release Sites Underlies Homosynaptic Depression at Sensory Synapses in Aplysia
J. Neurosci., March 1, 2002; 22(5): 1942 - 1955.
[Abstract] [Full Text] [PDF]
S. J Pyott and C. Rosenmund
The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons
J. Physiol., March 1, 2002; 539(2): 523 - 535.
[Abstract] [Full Text] [PDF]
S. Hefft, U. Kraushaar, J. R P Geiger, and P. Jonas
Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus
J. Physiol., February 15, 2002; 539(1): 201 - 208.
[Abstract] [Full Text] [PDF]
Y. He, C. F. Zorumski, and S. Mennerick
Contribution of Presynaptic Na+ Channel Inactivation to Paired-Pulse Synaptic Depression in Cultured Hippocampal Neurons
J Neurophysiol, February 1, 2002; 87(2): 925 - 936.
[Abstract] [Full Text] [PDF]
J. Kim and B. E. Alger
Random Response Fluctuations Lead to Spurious Paired-Pulse Facilitation
J. Neurosci., December 15, 2001; 21(24): 9608 - 9618.
[Abstract] [Full Text] [PDF]
C. Rozas, H. Frank, A. J. Heynen, B. Morales, M. F. Bear, and A. Kirkwood
Developmental Inhibitory Gate Controls the Relay of Activity to the Superficial Layers of the Visual Cortex
J. Neurosci., September 1, 2001; 21(17): 6791 - 6801.
[Abstract] [Full Text] [PDF]
D. J. Hagler Jr. and Y. Goda
Properties of Synchronous and Asynchronous Release During Pulse Train Depression in Cultured Hippocampal Neurons
J Neurophysiol, June 1, 2001; 85(6): 2324 - 2334.
[Abstract] [Full Text] [PDF]
T. Ishikawa and T. Takahashi
Mechanisms underlying presynaptic facilitatory effect of cyclothiazide at the calyx of Held of juvenile rats
J. Physiol., June 1, 2001; 533(2): 423 - 431.
[Abstract] [Full Text] [PDF]
R. D. King, M. C. Wiest, and P. R. Montague
Extracellular Calcium Depletion as a Mechanism of Short-Term Synaptic Depression
J Neurophysiol, May 1, 2001; 85(5): 1952 - 1959.
[Abstract] [Full Text] [PDF]
S. J Pyott and C. Rosenmund
The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons
J. Physiol., March 1, 2002; 539(2): 523 - 535.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|