 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 16, Number 18, Issue of September 15, 1996 pp. 5661-5671
Copyright ©1996 Society for NeuroscienceDeterminants of the Time Course of Facilitation at the Granule Cell to Purkinje Cell Synapse
Received May 10, 1996; revised July 2, 1996; accepted July 3, 1996.
Pradeep P. Atluri and Wade G. Regehr Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115
Short-term facilitation is a widely observed form of synaptic enhancement that is not well understood. Although presynaptic calcium has long been implicated in this process, its role is unclear, particularly at synapses in the mammalian brain. We tested the role of presynaptic residual free calcium ([Ca]res) in facilitation of synapses between granule cells and Purkinje cells in rat cerebellar slices. Paired-pulse facilitation of synaptic currents resulted in an approximately 2.5-fold enhancement that decayed with a time constant of ~200 msec, as assessed by voltage-clamp recordings. Measurements of [Ca]res using fluorescent calcium-sensitive indicators revealed that [Ca]res decayed more rapidly than did facilitation. Manipulation of [Ca]res dynamics by introducing EGTA into presynaptic terminals sped the decays of [Ca]res and facilitation in a dose-dependent manner. When [Ca]res was reduced to a brief impulse lasting several milliseconds, facilitation was still present, although reduced in amplitude and duration. Facilitation decayed with an intrinsic time constant of ~40 msec. These results suggest that facilitation at this synapse is produced by a calcium-driven process with a high affinity and a slow effective off-rate. A combination of [Ca]res dynamics and the properties of a calcium-driven reaction determine the time course and amplitude of facilitation.
Key words: synaptic transmission; parallel fiber; presynaptic terminal; short-term enhancement; calcium; magnesium green; cerebellum
This article has been cited by other articles:
F. Crepel
Role of Presynaptic Kainate Receptors at Parallel Fiber-Purkinje Cell Synapses in Induction of Cerebellar LTD: Interplay With Climbing Fiber Input
J Neurophysiol, August 1, 2009; 102(2): 965 - 973.
[Abstract] [Full Text] [PDF]
J. A. Goldberg, M. A. Teagarden, R. C. Foehring, and C. J. Wilson
Nonequilibrium Calcium Dynamics Regulate the Autonomous Firing Pattern of Rat Striatal Cholinergic Interneurons
J. Neurosci., July 1, 2009; 29(26): 8396 - 8407.
[Abstract] [Full Text] [PDF]
T. Hori and T. Takahashi
Mechanisms underlying short-term modulation of transmitter release by presynaptic depolarization
J. Physiol., June 15, 2009; 587(12): 2987 - 3000.
[Abstract] [Full Text] [PDF]
M. Galante, H. Jani, L. Vanes, H. Daniel, E. M.C. Fisher, V. L.J. Tybulewicz, T. V.P. Bliss, and E. Morice
Impairments in motor coordination without major changes in cerebellar plasticity in the Tc1 mouse model of Down syndrome
Hum. Mol. Genet., April 15, 2009; 18(8): 1449 - 1463.
[Abstract] [Full Text] [PDF]
Y. Etzion, A. Mor, and Y. Grossman
Differential modulation of cerebellar climbing fiber and parallel fiber synaptic responses at high pressure
J Appl Physiol, February 1, 2009; 106(2): 729 - 736.
[Abstract] [Full Text] [PDF]
M. Muller, F. Felmy, and R. Schneggenburger
A limited contribution of Ca2+ current facilitation to paired-pulse facilitation of transmitter release at the rat calyx of Held
J. Physiol., November 15, 2008; 586(22): 5503 - 5520.
[Abstract] [Full Text] [PDF]
J. Balaji, M. Armbruster, and T. A. Ryan
Calcium Control of Endocytic Capacity at a CNS Synapse
J. Neurosci., June 25, 2008; 28(26): 6742 - 6749.
[Abstract] [Full Text] [PDF]
H. Yang and M. A. Xu-Friedman
Relative Roles of Different Mechanisms of Depression at the Mouse Endbulb of Held
J Neurophysiol, May 1, 2008; 99(5): 2510 - 2521.
[Abstract] [Full Text] [PDF]
E. Neher
Details of Ca2+ dynamics matter
J. Physiol., April 15, 2008; 586(8): 2031 - 2031.
[Full Text] [PDF]
S. Curti, L. Gomez, R. Budelli, and A. E. Pereda
Subthreshold Sodium Current Underlies Essential Functional Specializations at Primary Auditory Afferents
J Neurophysiol, April 1, 2008; 99(4): 1683 - 1699.
[Abstract] [Full Text] [PDF]
S. R. Williams and S. E. Atkinson
Pathway-specific use-dependent dynamics of excitatory synaptic transmission in rat intracortical circuits
J. Physiol., December 15, 2007; 585(3): 759 - 777.
[Abstract] [Full Text] [PDF]
C. J. Edwards, C. J. Leary, and G. J. Rose
Counting on Inhibition and Rate-Dependent Excitation in the Auditory System
J. Neurosci., December 5, 2007; 27(49): 13384 - 13392.
[Abstract] [Full Text] [PDF]
F. Crepel and H. Daniel
Developmental Changes in Agonist-Induced Retrograde Signaling at Parallel Fiber Purkinje Cell Synapses: Role of Calcium-Induced Calcium Release
J Neurophysiol, November 1, 2007; 98(5): 2550 - 2565.
[Abstract] [Full Text] [PDF]
S. D. Brenowitz and W. G. Regehr
Reliability and Heterogeneity of Calcium Signaling at Single Presynaptic Boutons of Cerebellar Granule Cells
J. Neurosci., July 25, 2007; 27(30): 7888 - 7898.
[Abstract] [Full Text] [PDF]
M. J. Wall, A. Atterbury, and N. Dale
Control of basal extracellular adenosine concentration in rat cerebellum
J. Physiol., July 1, 2007; 582(1): 137 - 151.
[Abstract] [Full Text] [PDF]
K. J. Iremonger and J. S. Bains
Integration of Asynchronously Released Quanta Prolongs the Postsynaptic Spike Window
J. Neurosci., June 20, 2007; 27(25): 6684 - 6691.
[Abstract] [Full Text] [PDF]
R. M. Empson, M. L. Garside, and T. Knopfel
Plasma Membrane Ca2+ ATPase 2 Contributes to Short-Term Synapse Plasticity at the Parallel Fiber to Purkinje Neuron Synapse
J. Neurosci., April 4, 2007; 27(14): 3753 - 3758.
[Abstract] [Full Text] [PDF]
K. M. MacLeod, T. K. Horiuchi, and C. E. Carr
A Role for Short-Term Synaptic Facilitation and Depression in the Processing of Intensity Information in the Auditory Brain Stem
J Neurophysiol, April 1, 2007; 97(4): 2863 - 2874.
[Abstract] [Full Text] [PDF]
G. Akopian and J. P. Walsh
Reliable long-lasting depression interacts with variable short-term facilitation to determine corticostriatal paired-pulse plasticity in young rats
J. Physiol., April 1, 2007; 580(1): 225 - 240.
[Abstract] [Full Text] [PDF]
M. Muller, F. Felmy, B. Schwaller, and R. Schneggenburger
Parvalbumin Is a Mobile Presynaptic Ca2+ Buffer in the Calyx of Held that Accelerates the Decay of Ca2+ and Short-Term Facilitation
J. Neurosci., February 28, 2007; 27(9): 2261 - 2271.
[Abstract] [Full Text] [PDF]
F. Crepel
Developmental Changes in Retrograde Messengers Involved in Depolarization-Induced Suppression of Excitation at Parallel Fiber-Purkinje Cell Synapses in Rodents
J Neurophysiol, January 1, 2007; 97(1): 824 - 836.
[Abstract] [Full Text] [PDF]
V. Matveev, R. Bertram, and A. Sherman
Residual Bound Ca2+ Can Account for the Effects of Ca2+ Buffers on Synaptic Facilitation
J Neurophysiol, December 1, 2006; 96(6): 3389 - 3397.
[Abstract] [Full Text] [PDF]
G. A. Lnenicka, J. Grizzaffi, B. Lee, and N. Rumpal
Ca2+ Dynamics along Identified Synaptic Terminals in Drosophila Larvae.
J. Neurosci., November 22, 2006; 26(47): 12283 - 12293.
[Abstract] [Full Text] [PDF]
A. R. B. Schiess, C. S. Scullin, and L. D. Partridge
Neurosteroid-induced enhancement of short-term facilitation involves a component downstream from presynaptic calcium in hippocampal slices
J. Physiol., November 1, 2006; 576(3): 833 - 847.
[Abstract] [Full Text] [PDF]
F. Ricci-Tersenghi, F. Minneci, E. Sola, E. Cherubini, and L. Maggi
Multivesicular Release at Developing Schaffer Collateral-CA1 Synapses: An Analytic Approach to Describe Experimental Data
J Neurophysiol, July 1, 2006; 96(1): 15 - 26.
[Abstract] [Full Text] [PDF]
M. Beierlein and W. G. Regehr
Brief bursts of parallel fiber activity trigger calcium signals in bergmann glia.
J. Neurosci., June 28, 2006; 26(26): 6958 - 6967.
[Abstract] [Full Text] [PDF]
B. L. Moss, A. D. Fuller, C. L. Sahley, and B. D. Burrell
Serotonin Modulates Axo-Axonal Coupling Between Neurons Critical for Learning in the Leech
J Neurophysiol, October 1, 2005; 94(4): 2575 - 2589.
[Abstract] [Full Text] [PDF]
F. Saitow, H. Suzuki, and S. Konishi
{beta}-Adrenoceptor-mediated long-term up-regulation of the release machinery at rat cerebellar GABAergic synapses
J. Physiol., June 1, 2005; 565(2): 487 - 502.
[Abstract] [Full Text] [PDF]
K. Matsui and C. E. Jahr
Differential Control of Synaptic and Ectopic Vesicular Release of Glutamate
J. Neurosci., October 13, 2004; 24(41): 8932 - 8939.
[Abstract] [Full Text] [PDF]
T. N. Allana and J.-W. Lin
Relative Distribution of Ca2+ Channels at the Crayfish Inhibitory Neuromuscular Junction
J Neurophysiol, September 1, 2004; 92(3): 1491 - 1500.
[Abstract] [Full Text] [PDF]
M. Beierlein, K. R. Gee, V. V. Martin, and W. G. Regehr
Presynaptic Calcium Measurements at Physiological Temperatures Using a New Class of Dextran-Conjugated Indicators
J Neurophysiol, July 1, 2004; 92(1): 591 - 599.
[Abstract] [Full Text] [PDF]
B. D. Burrell and C. L. Sahley
Multiple Forms of Long-Term Potentiation and Long-Term Depression Converge on a Single Interneuron in the Leech CNS
J. Neurosci., April 21, 2004; 24(16): 4011 - 4019.
[Abstract] [Full Text] [PDF]
C. Thaler, A. C. Gray, and D. Lipscombe
Cumulative inactivation of N-type CaV2.2 calcium channels modified by alternative splicing
PNAS, April 13, 2004; 101(15): 5675 - 5679.
[Abstract] [Full Text] [PDF]
B. Granseth
Dynamic properties of corticogeniculate excitatory transmission in the rat dorsal lateral geniculate nucleus in vitro
J. Physiol., April 1, 2004; 556(1): 135 - 146.
[Abstract] [Full Text] [PDF]
P. Isope, R. Franconville, B. Barbour, and P. Ascher
Repetitive firing of rat cerebellar parallel fibres after a single stimulation
J. Physiol., February 1, 2004; 554(3): 829 - 839.
[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]
M. A. XU-FRIEDMAN and W. G. REGEHR
Structural Contributions to Short-Term Synaptic Plasticity
Physiol Rev, January 1, 2004; 84(1): 69 - 85.
[Abstract] [Full Text] [PDF]
F. Mori-Kawakami, K. Kobayashi, and T. Takahashi
Developmental decrease in synaptic facilitation at the mouse hippocampal mossy fibre synapse
J. Physiol., November 15, 2003; 553(1): 37 - 48.
[Abstract] [Full Text] [PDF]
M. Beierlein, J. R. Gibson, and B. W. Connors
Two Dynamically Distinct Inhibitory Networks in Layer 4 of the Neocortex
J Neurophysiol, November 1, 2003; 90(5): 2987 - 3000.
[Abstract] [Full Text] [PDF]
S. D. Brenowitz and W. G. Regehr
Calcium Dependence of Retrograde Inhibition by Endocannabinoids at Synapses onto Purkinje Cells
J. Neurosci., July 16, 2003; 23(15): 6373 - 6384.
[Abstract] [Full Text] [PDF]
B. Granseth and S. Lindstrom
Unitary EPSCs of Corticogeniculate Fibers in the Rat Dorsal Lateral Geniculate Nucleus In Vitro
J Neurophysiol, June 1, 2003; 89(6): 2952 - 2960.
[Abstract] [Full Text] [PDF]
Y. D. Zhou, T. J Turner, and K. Dunlap
Enhanced G protein-dependent modulation of excitatory synaptic transmission in the cerebellum of the Ca2+ channel-mutant mouse, tottering
J. Physiol., March 1, 2003; 547(2): 497 - 507.
[Abstract] [Full Text] [PDF]
A. I. Ivanov and R. L. Calabrese
Modulation of Spike-Mediated Synaptic Transmission by Presynaptic Background Ca2+ in Leech Heart Interneurons
J. Neurosci., February 15, 2003; 23(4): 1206 - 1218.
[Abstract] [Full Text] [PDF]
Y. Li and R. E. Burke
Developmental Changes in Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord
J Neurophysiol, December 1, 2002; 88(6): 3218 - 3231.
[Abstract] [Full Text] [PDF]
H. Kamiya, S. Ozawa, and T. Manabe
Kainate Receptor-Dependent Short-Term Plasticity of Presynaptic Ca2+ Influx at the Hippocampal Mossy Fiber Synapses
J. Neurosci., November 1, 2002; 22(21): 9237 - 9243.
[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]
B. Granseth, E. Ahlstrand, and S. Lindstrom
Paired pulse facilitation of corticogeniculate EPSCs in the dorsal lateral geniculate nucleus of the rat investigated in vitro
J. Physiol., October 15, 2002; 544(2): 477 - 486.
[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]
D. H Brager, M. Capogna, and S. M Thompson
Short-term synaptic plasticity, simulation of nerve terminal dynamics, and the effects of protein kinase C activation in rat hippocampus
J. Physiol., June 1, 2002; 541(2): 545 - 559.
[Abstract] [Full Text] [PDF]
A. G. Carter, K. E. Vogt, K. A. Foster, and W. G. Regehr
Assessing the Role of Calcium-Induced Calcium Release in Short-Term Presynaptic Plasticity at Excitatory Central Synapses
J. Neurosci., January 1, 2002; 22(1): 21 - 28.
[Abstract] [Full Text] [PDF]
C. Levenes, H. Daniel, and F. Crepel
Retrograde modulation of transmitter release by postsynaptic subtype 1 metabotropic glutamate receptors in the rat cerebellum
J. Physiol., November 15, 2001; 537(1): 125 - 140.
[Abstract] [Full Text] [PDF]
S. Jacoby, R. E Sims, and N. A Hartell
Nitric oxide is required for the induction and heterosynaptic spread of long-term potentiation in rat cerebellar slices
J. Physiol., September 15, 2001; 535(3): 825 - 839.
[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]
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] [Full Text] [PDF]
A Rozov, N Burnashev, B Sakmann, and E Neher
Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics
J. Physiol., March 15, 2001; 531(3): 807 - 826.
[Abstract] [Full Text] [PDF]
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]
S. Charpak, J. Mertz, E. Beaurepaire, L. Moreaux, and K. Delaney
Odor-evoked calcium signals in dendrites of rat mitral cells
PNAS, January 10, 2001; (2001) 21422798.
[Abstract] [Full Text]
J. S. Isaacson
Mechanisms governing dendritic gamma -aminobutyric acid (GABA) release in the rat olfactory bulb
PNAS, December 14, 2000; (2000) 21445798.
[Abstract] [Full Text]
O. Caillard, H. Moreno, B. Schwaller, I. Llano, M. R. Celio, and A. Marty
Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity
PNAS, November 2, 2000; (2000) 230362997.
[Abstract] [Full Text]
M. Casado, S. Dieudonné, and P. Ascher
Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse
PNAS, September 29, 2000; (2000) 200354297.
[Abstract] [Full Text]
M. A. Xu-Friedman and W. G. Regehr
Probing Fundamental Aspects of Synaptic Transmission with Strontium
J. Neurosci., June 15, 2000; 20(12): 4414 - 4422.
[Abstract] [Full Text] [PDF]
A. G. Carter and W. G. Regehr
Prolonged Synaptic Currents and Glutamate Spillover at the Parallel Fiber to Stellate Cell Synapse
J. Neurosci., June 15, 2000; 20(12): 4423 - 4434.
[Abstract] [Full Text] [PDF]
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]
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]
D. L. Brody and D. T. Yue
Relief of G-Protein Inhibition of Calcium Channels and Short-Term Synaptic Facilitation in Cultured Hippocampal Neurons
J. Neurosci., February 1, 2000; 20(3): 889 - 898.
[Abstract] [Full Text] [PDF]
D. A. DiGregorio, A. Peskoff, and J. L. Vergara
Measurement of Action Potential-Induced Presynaptic Calcium Domains at a Cultured Neuromuscular Junction
J. Neurosci., September 15, 1999; 19(18): 7846 - 7859.
[Abstract] [Full Text] [PDF]
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]
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]
P. Pavlidis and D. V. Madison
Synaptic Transmission in Pair Recordings From CA3 Pyramidal Cells in Organotypic Culture
J Neurophysiol, June 1, 1999; 81(6): 2787 - 2797.
[Abstract] [Full Text] [PDF]
S. N. Schiffmann, G. Cheron, A. Lohof, P. d'Alcantara, M. Meyer, M. Parmentier, and S. Schurmans
Impaired motor coordination and Purkinje cell excitability in mice lacking calretinin
PNAS, April 27, 1999; 96(9): 5257 - 5262.
[Abstract] [Full Text] [PDF]
P. P. Atluri and W. G. Regehr
Delayed Release of Neurotransmitter from Cerebellar Granule Cells
J. Neurosci., October 15, 1998; 18(20): 8214 - 8227.
[Abstract] [Full Text] [PDF]
J. S. Dittman and W. G. Regehr
Calcium Dependence and Recovery Kinetics of Presynaptic Depression at the Climbing Fiber to Purkinje Cell Synapse
J. Neurosci., August 15, 1998; 18(16): 6147 - 6162.
[Abstract] [Full Text] [PDF]
C. Chen and W. G. Regehr
The Mechanism of cAMP-Mediated Enhancement at a Cerebellar Synapse
J. Neurosci., November 15, 1997; 17(22): 8687 - 8694.
[Abstract] [Full Text] [PDF]
H. von Gersdorff, R. Schneggenburger, S. Weis, and E. Neher
Presynaptic Depression at a Calyx Synapse: The Small Contribution of Metabotropic Glutamate Receptors
J. Neurosci., November 1, 1997; 17(21): 8137 - 8146.
[Abstract] [Full Text] [PDF]
T. M. Fischer, R. S. Zucker, and T. J. Carew
Activity-Dependent Potentiation of Synaptic Transmission From L30 Inhibitory Interneurons of Aplysia Depends on Residual Presynaptic Ca2+ But Not on Postsynaptic Ca2+
J Neurophysiol, October 1, 1997; 78(4): 2061 - 2071.
[Abstract] [Full Text] [PDF]
B. L. Sabatini and W. G. Regehr
Control of Neurotransmitter Release by Presynaptic Waveform at the Granule Cell to Purkinje Cell Synapse
J. Neurosci., May 15, 1997; 17(10): 3425 - 3435.
[Abstract] [Full Text] [PDF]
H. von Gersdorff and G. Matthews
Depletion and Replenishment of Vesicle Pools at a Ribbon-Type Synaptic Terminal
J. Neurosci., March 15, 1997; 17(6): 1919 - 1927.
[Abstract] [Full Text] [PDF]
S. Charpak, J. Mertz, E. Beaurepaire, L. Moreaux, and K. Delaney
Odor-evoked calcium signals in dendrites of rat mitral cells
PNAS, January 30, 2001; 98(3): 1230 - 1234.
[Abstract] [Full Text] [PDF]
J. S. Isaacson
Mechanisms governing dendritic gamma -aminobutyric acid (GABA) release in the rat olfactory bulb
PNAS, January 2, 2001; 98(1): 337 - 342.
[Abstract] [Full Text] [PDF]
M. Casado, S. Dieudonne, and P. Ascher
Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse
PNAS, October 10, 2000; 97(21): 11593 - 11597.
[Abstract] [Full Text] [PDF]
O. Caillard, H. Moreno, B. Schwaller, I. Llano, M. R. Celio, and A. Marty
Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity
PNAS, November 21, 2000; 97(24): 13372 - 13377.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|