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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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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] [Full Text] [PDF]


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J. Neurosci.Home page
S. Brenowitz and L. O. Trussell
Minimizing Synaptic Depression by Control of Release Probability
J. Neurosci., March 15, 2001; 21(6): 1857 - 1867.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
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.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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] [Full Text] [PDF]


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Cereb CortexHome page
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] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
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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J. Neurosci.Home page
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.
[Abstract] [Full Text] [PDF]


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ScienceHome page
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] [Full Text]


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JCBHome page
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] [Full Text] [PDF]


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J. Neurosci.Home page
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] [Full Text] [PDF]


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J. Neurosci.Home page
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] [Full Text] [PDF]


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J. Neurosci.Home page
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] [Full Text] [PDF]


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J. Neurosci.Home page
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.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
M. Galarreta and S. Hestrin
Burst Firing Induces a Rebound of Synaptic Strength at Unitary Neocortical Synapses
J Neurophysiol, January 1, 2000; 83(1): 621 - 624.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
C. Chen and W. G. Regehr
Contributions of Residual Calcium to Fast Synaptic Transmission
J. Neurosci., August 1, 1999; 19(15): 6257 - 6266.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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): 6309 - 6317.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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; 82(1): 42 - 49.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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): 5265 - 5274.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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; 19(11): 4293 - 4304.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
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; 275(44): 34393 - 34398.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
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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J. Physiol.Home page
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]



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