 |
 Previous Article | Next Article 
Volume 17, Number 21,
Issue of November 1, 1997
pp. 8137-8146
Copyright ©1997 Society for Neuroscience
Presynaptic Depression at a Calyx Synapse: The Small Contribution
of Metabotropic Glutamate Receptors
Received June 26, 1997; revised Aug. 8, 1997; accepted Aug. 12, 1997.
Henrique von Gersdorff,
Ralf Schneggenburger,
Sibylle Weis, and
Erwin Neher
Department of Membrane Biophysics, Max Planck Institute for
Biophysical Chemistry, D-37077 Göttingen, Germany
Synaptic depression of evoked EPSCs was quantified with stimulation
frequencies ranging from 0.2 to 100 Hz at the single CNS synapse formed
by the calyx of Held in the rat brainstem. Half-maximal depression
occurred at  1 Hz, with 10 and 100 Hz stimulation frequencies reducing EPSC amplitudes to 30% and 10% of their initial
magnitude, respectively. The time constant of recovery from depression
elicited by 10 Hz afferent fiber stimulation was 4.2 sec. AMPA and NMDA receptor-mediated EPSCs depressed in parallel at 1-5 Hz stimulation frequencies, suggesting that depression was induced by presynaptic mechanism(s) that reduced glutamate release. To determine the contribution of autoreceptors to depression, we studied the inhibitory effects of the metabotropic glutamate receptor (mGluR) agonists (1S, 3S)-ACPD and L-AP4 and
found them to be reversed in a dose-dependent manner by
(RS)- -cyclopropyl-4-phosphonophenylglycine (CPPG), a
novel and potent competitive antagonist of mGluRs. At 300 µM, CPPG completely reversed the effects of
L-AP4 and (1S, 3S)-ACPD, but
reduced 5-10 Hz elicited depression by only 6%. CPPG-sensitive mGluRs, presumably activated by glutamate spillover during
physiological synaptic transmission, thus contribute on the order of
only 10% to short-term synaptic depression. We therefore suggest that
the main mechanism contributing to the robust depression elicited by
5-10 Hz afferent fiber stimulation of the calyx of Held synapse is
synaptic vesicle pool depletion.
Key words:
EPSCs;
NMDA;
AMPA;
competitive antagonist;
synaptic
transmission;
auditory brainstem slices;
secretion;
short-term
plasticity
This article has been cited by other articles:
|
|
|
|
 
G. Srinivasan, J. H. Kim, and H. von Gersdorff
The Pool of Fast Releasing Vesicles Is Augmented by Myosin Light Chain Kinase Inhibition at the Calyx of Held Synapse
J Neurophysiol,
April 1, 2008;
99(4):
1810 - 1824.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Innocenti and R. Heidelberger
Mechanisms Contributing to Tonic Release at the Cone Photoreceptor Ribbon Synapse
J Neurophysiol,
January 1, 2008;
99(1):
25 - 36.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Hosoi, T. Sakaba, and E. Neher
Quantitative Analysis of Calcium-Dependent Vesicle Recruitment and Its Functional Role at the Calyx of Held Synapse
J. Neurosci.,
December 26, 2007;
27(52):
14286 - 14298.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Heidelberger
Mechanisms of tonic, graded release: lessons from the vertebrate photoreceptor
J. Physiol.,
December 15, 2007;
585(3):
663 - 667.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Renden and H. von Gersdorff
Synaptic Vesicle Endocytosis at a CNS Nerve Terminal: Faster Kinetics at Physiological Temperatures and Increased Endocytotic Capacity During Maturation
J Neurophysiol,
December 1, 2007;
98(6):
3349 - 3359.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Scheuss, H. Taschenberger, and E. Neher
Kinetics of both synchronous and asynchronous quantal release during trains of action potential-evoked EPSCs at the rat calyx of Held
J. Physiol.,
December 1, 2007;
585(2):
361 - 381.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. G. Inchauspe, I. D. Forsythe, and O. D. Uchitel
Changes in synaptic transmission properties due to the expression of N-type calcium channels at the calyx of Held synapse of mice lacking P/Q-type calcium channels
J. Physiol.,
November 1, 2007;
584(3):
835 - 851.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Hermann, M. Pecka, H. von Gersdorff, B. Grothe, and A. Klug
Synaptic Transmission at the Calyx of Held Under In Vivo Like Activity Levels
J Neurophysiol,
August 1, 2007;
98(2):
807 - 820.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. L. P. Habets and J. G. G. Borst
An Increase in Calcium Influx Contributes to Post-Tetanic Potentiation at the Rat Calyx of Held Synapse
J Neurophysiol,
December 1, 2006;
96(6):
2868 - 2876.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z.-Y. Zhou, Q.-F. Wan, P. Thakur, and R. Heidelberger
Capacitance Measurements in the Mouse Rod Bipolar Cell Identify a Pool of Releasable Synaptic Vesicles
J Neurophysiol,
November 1, 2006;
96(5):
2539 - 2548.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. X. Gittelman and B. L Tempel
Kv1.1-Containing Channels Are Critical for Temporal Precision During Spike Initiation
J Neurophysiol,
September 1, 2006;
96(3):
1203 - 1214.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Y. C. Wong, B. Billups, J. Johnston, R. J. Evans, and I. D. Forsythe
Endogenous Activation of Adenosine A1 Receptors, but Not P2X Receptors, During High-Frequency Synaptic Transmission at the Calyx of Held
J Neurophysiol,
June 1, 2006;
95(6):
3336 - 3342.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Kittel, C. Wichmann, T. M. Rasse, W. Fouquet, M. Schmidt, A. Schmid, D. A. Wagh, C. Pawlu, R. R. Kellner, K. I. Willig, et al.
Bruchpilot Promotes Active Zone Assembly, Ca2+ Channel Clustering, and Vesicle Release
Science,
May 19, 2006;
312(5776):
1051 - 1054.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Sun, P. Bronk, X. Liu, W. Han, and T. C. Sudhof
Synapsins regulate use-dependent synaptic plasticity in the calyx of Held by a Ca2+/calmodulin-dependent pathway
PNAS,
February 21, 2006;
103(8):
2880 - 2885.
[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]
|
|
|
|
|
|
|
C. Kushmerick, R. Renden, and H. von Gersdorff
Physiological Temperatures Reduce the Rate of Vesicle Pool Depletion and Short-Term Depression via an Acceleration of Vesicle Recruitment
J. Neurosci.,
February 1, 2006;
26(5):
1366 - 1377.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. M. Schluter, J. Basu, T. C. Sudhof, and C. Rosenmund
Rab3 Superprimes Synaptic Vesicles for Release: Implications for Short-Term Synaptic Plasticity
J. Neurosci.,
January 25, 2006;
26(4):
1239 - 1246.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Abrahamsson, B. Gustafsson, and E. Hanse
Synaptic fatigue at the naive perforant path-dentate granule cell synapse in the rat
J. Physiol.,
December 15, 2005;
569(3):
737 - 750.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Shtrahman, C. Yeung, D. W. Nauen, G.-q. Bi, and X.-l. Wu
Probing Vesicle Dynamics in Single Hippocampal Synapses
Biophys. J.,
November 1, 2005;
89(5):
3615 - 3627.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Taschenberger, V. Scheuss, and E. Neher
Release kinetics, quantal parameters and their modulation during short-term depression at a developing synapse in the rat CNS
J. Physiol.,
October 15, 2005;
568(2):
513 - 537.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Ishikawa, M. Kaneko, H.-S. Shin, and T. Takahashi
Presynaptic N-type and P/Q-type Ca2+ channels mediating synaptic transmission at the calyx of Held of mice
J. Physiol.,
October 1, 2005;
568(1):
199 - 209.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Renden, H. Taschenberger, N. Puente, D. A. Rusakov, R. Duvoisin, L.-Y. Wang, K. P. Lehre, and H. von Gersdorff
Glutamate Transporter Studies Reveal the Pruning of Metabotropic Glutamate Receptors and Absence of AMPA Receptor Desensitization at Mature Calyx of Held Synapses
J. Neurosci.,
September 14, 2005;
25(37):
8482 - 8497.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Billups, B. P Graham, A. Y. C Wong, and I. D Forsythe
Unmasking group III metabotropic glutamate autoreceptor function at excitatory synapses in the rat CNS
J. Physiol.,
June 15, 2005;
565(3):
885 - 896.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Korogod, X. Lou, and R. Schneggenburger
Presynaptic Ca2+ Requirements and Developmental Regulation of Posttetanic Potentiation at the Calyx of Held
J. Neurosci.,
May 25, 2005;
25(21):
5127 - 5137.
[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]
|
|
|
|
|
|
|
N. Hosoi, I. Arai, and M. Tachibana
Group III Metabotropic Glutamate Receptors and Exocytosed Protons Inhibit L-Type Calcium Currents in Cones But Not in Rods
J. Neurosci.,
April 20, 2005;
25(16):
4062 - 4072.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. Leao, C. Kushmerick, R. Pinaud, R. Renden, G.-L. Li, H. Taschenberger, G. Spirou, S. R. Levinson, and H. von Gersdorff
Presynaptic Na+ Channels: Locus, Development, and Recovery from Inactivation at a High-Fidelity Synapse
J. Neurosci.,
April 6, 2005;
25(14):
3724 - 3738.
[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]
|
|
|
|
|
|
|
J. B. Bergsman, P. De Camilli, and D. A. McCormick
Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body
J Neurophysiol,
July 1, 2004;
92(1):
545 - 552.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Kushmerick, G. D. Price, H. Taschenberger, N. Puente, R. Renden, J. I. Wadiche, R. M. Duvoisin, P. Grandes, and H. von Gersdorff
Retroinhibition of Presynaptic Ca2+ Currents by Endocannabinoids Released via Postsynaptic mGluR Activation at a Calyx Synapse
J. Neurosci.,
June 30, 2004;
24(26):
5955 - 5965.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. D. Eisen, M. Spassova, and T. D. Parsons
Large Releasable Pool of Synaptic Vesicles in Chick Cochlear Hair Cells
J Neurophysiol,
June 1, 2004;
91(6):
2422 - 2428.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. H. Wu, C. L. Ma, and J. B. Kelly
Contribution of AMPA, NMDA, and GABAA Receptors to Temporal Pattern of Postsynaptic Responses in the Inferior Colliculus of the Rat
J. Neurosci.,
May 12, 2004;
24(19):
4625 - 4634.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. B. Awatramani, R. Turecek, and L. O. Trussell
Inhibitory Control at a Synaptic Relay
J. Neurosci.,
March 17, 2004;
24(11):
2643 - 2647.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Joshi, S. Shokralla, P. Titis, and L.-Y. Wang
The Role of AMPA Receptor Gating in the Development of High-Fidelity Neurotransmission at the Calyx of Held Synapse
J. Neurosci.,
January 7, 2004;
24(1):
183 - 196.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. P. J. de Lange, A. D. G. de Roos, and J. G. G. Borst
Two Modes of Vesicle Recycling in the Rat Calyx of Held
J. Neurosci.,
November 5, 2003;
23(31):
10164 - 10173.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Losonczy, P. Somogyi, and Z. Nusser
Reduction of Excitatory Postsynaptic Responses by Persistently Active Metabotropic Glutamate Receptors in the Hippocampus
J Neurophysiol,
April 1, 2003;
89(4):
1910 - 1919.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Trommershauser, R. Schneggenburger, A. Zippelius, and E. Neher
Heterogeneous Presynaptic Release Probabilities: Functional Relevance for Short-Term Plasticity
Biophys. J.,
March 1, 2003;
84(3):
1563 - 1579.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Chacron, K. Pakdaman, and A. Longtin
Interspike Interval Correlations, Memory, Adaptation, and Refractoriness in a Leaky Integrate-and-Fire Model with Threshold Fatigue
Neural Comput.,
February 1, 2003;
15(2):
253 - 278.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. H. Brager and S. M. Thompson
Activity-Dependent Release of Adenosine Contributes to Short-Term Depression at CA3-CA1 Synapses in Rat Hippocampus
J Neurophysiol,
January 1, 2003;
89(1):
22 - 26.
[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]
|
|
|
|
|
|
|
A. G. Millar, H. Bradacs, M. P. Charlton, and H. L. Atwood
Inverse Relationship between Release Probability and Readily Releasable Vesicles in Depressing and Facilitating Synapses
J. Neurosci.,
November 15, 2002;
22(22):
9661 - 9667.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Billups and I. D. Forsythe
Presynaptic Mitochondrial Calcium Sequestration Influences Transmission at Mammalian Central Synapses
J. Neurosci.,
July 15, 2002;
22(14):
5840 - 5847.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. Leao and H. Von Gersdorff
Noradrenaline Increases High-Frequency Firing at the Calyx of Held Synapse During Development by Inhibiting Glutamate Release
J Neurophysiol,
May 1, 2002;
87(5):
2297 - 2306.
[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]
|
|
|
|
|
|
|
M. G. Mozhayeva, Y. Sara, X. Liu, and E. T. Kavalali
Development of Vesicle Pools during Maturation of Hippocampal Synapses
J. Neurosci.,
February 1, 2002;
22(3):
654 - 665.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Scheuss, R. Schneggenburger, and E. Neher
Separation of Presynaptic and Postsynaptic Contributions to Depression by Covariance Analysis of Successive EPSCs at the Calyx of Held Synapse
J. Neurosci.,
February 1, 2002;
22(3):
728 - 739.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. W. Keefer, A. Gramowski, and G. W. Gross
NMDA Receptor-Dependent Periodic Oscillations in Cultured Spinal Cord Networks
J Neurophysiol,
December 1, 2001;
86(6):
3030 - 3042.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. C. Meyer, E. Neher, and R. Schneggenburger
Estimation of Quantal Size and Number of Functional Active Zones at the Calyx of Held Synapse by Nonstationary EPSC Variance Analysis
J. Neurosci.,
October 15, 2001;
21(20):
7889 - 7900.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Chacron, A. Longtin, and L. Maler
Negative Interspike Interval Correlations Increase the Neuronal Capacity for Encoding Time-Dependent Stimuli
J. Neurosci.,
July 15, 2001;
21(14):
5328 - 5343.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Futai, M. Okada, K. Matsuyama, and T. Takahashi
High-Fidelity Transmission Acquired via a Developmental Decrease in NMDA Receptor Expression at an Auditory Synapse
J. Neurosci.,
May 15, 2001;
21(10):
3342 - 3349.
[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]
|
|
|
|
|
|
|
M. W. Doyle and M. C. Andresen
Reliability of Monosynaptic Sensory Transmission in Brain Stem Neurons In Vitro
J Neurophysiol,
May 1, 2001;
85(5):
2213 - 2223.
[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]
|
|
|
|
|
|
|
T. Sakaba and E. Neher
Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held
PNAS,
December 22, 2000;
(2000)
21541098.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
H. Taschenberger and H. von Gersdorff
Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity
J. Neurosci.,
December 15, 2000;
20(24):
9162 - 9173.
[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 2, 2000;
(2000)
230362997.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
G. B. Awatramani and M. M. Slaughter
Origin of Transient and Sustained Responses in Ganglion Cells of the Retina
J. Neurosci.,
September 15, 2000;
20(18):
7087 - 7095.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. H. Bollmann, B. Sakmann, and J. G. G. Borst
Calcium Sensitivity of Glutamate Release in a Calyx-Type Terminal
Science,
August 11, 2000;
289(5481):
953 - 957.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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]
|
|
|
|
