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The Journal of Neuroscience, August 15, 1998, 18(16):6147-6162
Calcium Dependence and Recovery Kinetics of Presynaptic
Depression at the Climbing Fiber to Purkinje Cell Synapse
Jeremy S.
Dittman and
Wade G.
Regehr
Department of Neurobiology, Harvard Medical School, Boston,
Massachusetts 02115
Short-term depression is a widespread form of use-dependent
plasticity found in the peripheral and central nervous systems of
invertebrates and vertebrates. The mechanism behind this transient decrease in synaptic strength is thought to be primarily the result of
presynaptic "depletion" of a readily releasable neurotransmitter pool, which typically recovers with a time constant of a few seconds. We studied the mechanism and dynamics of recovery from depression at
the climbing fiber to Purkinje cell synapse, where marked presynaptic depression has been described previously. Climbing fibers are well
suited to studies of recovery from depression because they display
little, if any, facilitation (even under conditions of low-release
probability), which can obscure rapid recovery from depression for
hundreds of milliseconds after release. We found that recovery from
depression occurred in three kinetic phases. The fast and intermediate
components could be approximated by exponentials with time constants of
100 msec and 3 sec at 24° C. A much slower recovery phase was also
present, but it was only prominent during prolonged stimulus trains.
The fast component was enhanced by raising extracellular calcium and
was eliminated by lowering presynaptic calcium, suggesting that, on
short time scales, recovery from depression is driven by residual
calcium. During regular and Poisson stimulus trains, recovery from
depression was dramatically accelerated by accumulation of presynaptic
residual calcium, maintaining synaptic efficacy under conditions that
would otherwise deplete the available transmitter pool. This represents a novel form of presynaptic plasticity in that high levels of activity
modulate the rate of recovery as well as the magnitude of
depression.
Key words:
presynaptic depression; paired-pulse depression; Purkinje
cell; climbing fiber; inferior olive neuron; Poisson stimulus
Copyright © 1998 Society for Neuroscience 0270-6474/98/18166147-16$05.00/0
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809 - 824.
[Abstract]
[Full Text]
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M. A. Xu-Friedman, K. M. Harris, and W. G. Regehr
Three-Dimensional Comparison of Ultrastructural Characteristics at Depressing and Facilitating Synapses onto Cerebellar Purkinje Cells
J. Neurosci.,
September 1, 2001;
21(17):
6666 - 6672.
[Abstract]
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J. D. Hunter and J. G. Milton
Synaptic Heterogeneity and Stimulus-Induced Modulation of Depression in Central Synapses
J. Neurosci.,
August 1, 2001;
21(15):
5781 - 5793.
[Abstract]
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S. Iwasaki and T. Takahashi
Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem
J. Physiol.,
August 1, 2001;
534(3):
861 - 871.
[Abstract]
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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;
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2324 - 2334.
[Abstract]
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J. Kilbride, A. M. Rush, M. J. Rowan, and R. Anwyl
Presynaptic Group II mGluR Inhibition of Short-Term Depression in the Medial Perforant Path of the Dentate Gyrus In Vitro
J Neurophysiol,
June 1, 2001;
85(6):
2509 - 2515.
[Abstract]
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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;
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[Abstract]
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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]
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Y. Li and R. E. Burke
Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord: Effects of Calcium and Temperature
J Neurophysiol,
May 1, 2001;
85(5):
2047 - 2062.
[Abstract]
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J. S. Fitzpatrick, G. Akopian, and J. P. Walsh
Short-Term Plasticity at Inhibitory Synapses in Rat Striatum and Its Effects on Striatal Output
J Neurophysiol,
May 1, 2001;
85(5):
2088 - 2099.
[Abstract]
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S. Brenowitz and L. O. Trussell
Minimizing Synaptic Depression by Control of Release Probability
J. Neurosci.,
March 15, 2001;
21(6):
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E. Hanse and B. Gustafsson
Vesicle release probability and pre-primed pool at glutamatergic synapses in area CA1 of the rat neonatal hippocampus
J. Physiol.,
March 1, 2001;
531(2):
481 - 493.
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T. Sakaba and E. Neher
Quantitative Relationship between Transmitter Release and Calcium Current at the Calyx of Held Synapse
J. Neurosci.,
January 15, 2001;
21(2):
462 - 476.
[Abstract]
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V. Matveev and X.-J. Wang
Differential Short-term Synaptic Plasticity and Transmission of Complex Spike Trains: to Depress or to Facilitate?
Cereb Cortex,
November 1, 2000;
10(11):
1143 - 1153.
[Abstract]
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[PDF]
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S. Gasparini, C. Saviane, L. L. Voronin, and E. Cherubini
Silent synapses in the developing hippocampus: Lack of functional AMPA receptors or low probability of glutamate release?
PNAS,
August 6, 2000;
(2000)
170032297.
[Abstract]
[Full Text]
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U. Kraushaar and P. Jonas
Efficacy and Stability of Quantal GABA Release at a Hippocampal Interneuron-Principal Neuron Synapse
J. Neurosci.,
August 1, 2000;
20(15):
5594 - 5607.
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T. Takahashi, T. Hori, Y. Kajikawa, and T. Tsujimoto
The Role of GTP-Binding Protein Activity in Fast Central Synaptic Transmission
Science,
July 21, 2000;
289(5478):
460 - 463.
[Abstract]
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R. M. Smith, B. Baibakov, Y. Ikebuchi, B. H. White, N. A. Lambert, L. K. Kaczmarek, and S. S. Vogel
Exocytotic Insertion of Calcium Channels Constrains Compensatory Endocytosis to Sites of Exocytosis
J. Cell Biol.,
February 21, 2000;
148(4):
755 - 768.
[Abstract]
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A. C. Kreitzer and W. G. Regehr
Modulation of Transmission during Trains at a Cerebellar Synapse
J. Neurosci.,
February 15, 2000;
20(4):
1348 - 1357.
[Abstract]
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J. S. Dittman, A. C. Kreitzer, and W. G. Regehr
Interplay between Facilitation, Depression, and Residual Calcium at Three Presynaptic Terminals
J. Neurosci.,
February 15, 2000;
20(4):
1374 - 1385.
[Abstract]
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V. Matveev and X.-J. Wang
Implications of All-or-None Synaptic Transmission and Short-Term Depression beyond Vesicle Depletion: A Computational Study
J. Neurosci.,
February 15, 2000;
20(4):
1575 - 1588.
[Abstract]
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J. Burrone and L. Lagnado
Synaptic Depression and the Kinetics of Exocytosis in Retinal Bipolar Cells
J. Neurosci.,
January 15, 2000;
20(2):
568 - 578.
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M. Galarreta and S. Hestrin
Burst Firing Induces a Rebound of Synaptic Strength at Unitary Neocortical Synapses
J Neurophysiol,
January 1, 2000;
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621 - 624.
[Abstract]
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C. Chen and W. G. Regehr
Contributions of Residual Calcium to Fast Synaptic Transmission
J. Neurosci.,
August 1, 1999;
19(15):
6257 - 6266.
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A. Gomis, J. Burrone, and L. Lagnado
Two Actions of Calcium Regulate the Supply of Releasable Vesicles at the Ribbon Synapse of Retinal Bipolar Cells
J. Neurosci.,
August 1, 1999;
19(15):
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K. Jensen, J. D. C. Lambert, and M. S. Jensen
Activity-Dependent Depression of GABAergic IPSCs in Cultured Hippocampal Neurons
J Neurophysiol,
July 1, 1999;
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42 - 49.
[Abstract]
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J. A. Dzubay and C. E. Jahr
The Concentration of Synaptically Released Glutamate Outside of the Climbing Fiber-Purkinje Cell Synaptic Cleft
J. Neurosci.,
July 1, 1999;
19(13):
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J. A. Varela, S. Song, G. G. Turrigiano, and S. B. Nelson
Differential Depression at Excitatory and Inhibitory Synapses in Visual Cortex
J. Neurosci.,
June 1, 1999;
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R. J. Perrin, W. S. Woods, D. F. Clayton, and J. M. George
Interaction of Human alpha -Synuclein and Parkinson's Disease Variants with Phospholipids. STRUCTURAL ANALYSIS USING SITE-DIRECTED MUTAGENESIS
J. Biol. Chem.,
October 27, 2000;
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[Abstract]
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S. Gasparini, C. Saviane, L. L. Voronin, and E. Cherubini
Silent synapses in the developing hippocampus: Lack of functional AMPA receptors or low probability of glutamate release?
PNAS,
August 15, 2000;
97(17):
9741 - 9746.
[Abstract]
[Full Text]
[PDF]
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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):
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[Abstract]
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