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Volume 17, Number 20,
Issue of October 15, 1997
pp. 7926-7940
Copyright ©1997 Society for Neuroscience
A Quantitative Description of Short-Term Plasticity at Excitatory
Synapses in Layer 2/3 of Rat Primary Visual Cortex
Received June 20, 1997; revised July 22, 1997; accepted July 24, 1997.
Juan A. Varela,
Kamal Sen,
Jay Gibson,
Joshua Fost,
L. F. Abbott, and
Sacha B. Nelson
Department of Biology and Center for Complex Systems, Brandeis
University, Waltham, Massachusetts 02254
Cortical synapses exhibit several forms of short-term plasticity,
but the contribution of this plasticity to visual response dynamics is
unknown. In part, this is because the simple patterns of stimulation
used to probe plasticity in vitro do not correspond to
patterns of activity that occur in vivo. We have
developed a method of quantitatively characterizing short-term
plasticity at cortical synapses that permits prediction of responses to
arbitrary patterns of stimulation. Synaptic responses were recorded
intracellularly as EPSCs and extracellularly as local field potentials
in layer 2/3 of rat primary visual cortical slices during stimulation
of layer 4 with trains of electrical stimuli containing random mixtures of frequencies. Responses exhibited complex dynamics that were well
described by a simple three-component model consisting of facilitation
and two forms of depression, a stronger form that decayed exponentially
with a time constant of several hundred milliseconds and a weaker, but
more persistent, form that decayed with a time constant of several
seconds. Parameters obtained from fits to one train were used to
predict accurately responses to other random and constant frequency
trains. Control experiments revealed that depression was not caused by
a decrease in the effectiveness of extracellular stimulation or by a
buildup of inhibition. Pharmacological manipulations of transmitter
release and postsynaptic sensitivity suggested that both forms of
depression are mediated presynaptically. These results indicate that
firing evoked by visual stimuli is likely to cause significant
depression at cortical synapses. Hence synaptic depression may be an
important determinant of the temporal features of visual cortical
responses.
Key words:
facilitation;
depression;
temporal integration;
temporal
filtering;
contrast adaptation;
presynaptic;
neocortex;
nonlinearity;
EPSC;
field potential
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A. Losonczy, L. Zhang, R. Shigemoto, P. Somogyi, and Z. Nusser
Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones
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J. E. Hanson and D. Jaeger
Short-Term Plasticity Shapes the Response to Simulated Normal and Parkinsonian Input Patterns in the Globus Pallidus
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June 15, 2002;
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C. C. H. Petersen
Short-Term Dynamics of Synaptic Transmission Within the Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex
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June 1, 2002;
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A.-M. M. Oswald, J. E. Lewis, and L. Maler
Dynamically Interacting Processes Underlie Synaptic Plasticity in a Feedback Pathway
J Neurophysiol,
May 1, 2002;
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J. A Hirsch, L. M Martinez, J.-M. Alonso, K. Desai, C. Pillai, and C. Pierre
Synaptic physiology of the flow of information in the cat's visual cortex in vivo
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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;
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J. J. Renger, K. N. Hartman, Y. Tsuchimoto, M. Yokoi, S. Nakanishi, and T. K. Hensch
Experience-dependent plasticity without long-term depression by type 2 metabotropic glutamate receptors in developing visual cortex
PNAS,
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M. S. Goldman, P. Maldonado, and L. F. Abbott
Redundancy Reduction and Sustained Firing with Stochastic Depressing Synapses
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January 15, 2002;
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G. Fuhrmann, I. Segev, H. Markram, and M. Tsodyks
Coding of Temporal Information by Activity-Dependent Synapses
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January 1, 2002;
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J. R. Muller, A. B. Metha, J. Krauskopf, and P. Lennie
Information Conveyed by Onset Transients in Responses of Striate Cortical Neurons
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September 1, 2001;
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J. D. Hunter and J. G. Milton
Synaptic Heterogeneity and Stimulus-Induced Modulation of Depression in Central Synapses
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August 1, 2001;
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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
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June 1, 2001;
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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
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June 1, 2001;
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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;
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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;
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S. P. Perrett, S. M. Dudek, D. Eagleman, P. R. Montague, and M. J. Friedlander
LTD Induction in Adult Visual Cortex: Role of Stimulus Timing and Inhibition
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April 1, 2001;
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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?
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E. S. Fortune and G. J. Rose
Short-Term Synaptic Plasticity Contributes to the Temporal Filtering of Electrosensory Information
J. Neurosci.,
September 15, 2000;
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W. M. Usrey, J.-M. Alonso, and R. C. Reid
Synaptic Interactions between Thalamic Inputs to Simple Cells in Cat Visual Cortex
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M. V. Sanchez-Vives, L. G. Nowak, and D. A. McCormick
Membrane Mechanisms Underlying Contrast Adaptation in Cat Area 17 In Vivo
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C. M. Hempel, K. H. Hartman, X.-J. Wang, G. G. Turrigiano, and S. B. Nelson
Multiple Forms of Short-Term Plasticity at Excitatory Synapses in Rat Medial Prefrontal Cortex
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May 1, 2000;
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D. L. Brody and D. T. Yue
Release-Independent Short-Term Synaptic Depression in Cultured Hippocampal Neurons
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April 1, 2000;
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D. Parker
Activity and Calcium-Dependent Mechanisms Maintain Reliable Interneuron Synaptic Transmission in a Rhythmic Neural Network
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A. C. Kreitzer and W. G. Regehr
Modulation of Transmission during Trains at a Cerebellar Synapse
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February 15, 2000;
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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;
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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
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February 15, 2000;
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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;
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A. V. Galazyuk, D. Llano, and A. S. Feng
Temporal Dynamics of Acoustic Stimuli Enhance Amplitude Tuning of Inferior Colliculus Neurons
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January 1, 2000;
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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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K. Tarczy-Hornoch, K.A.C. Martin, K.J. Stratford, and J.J.B. Jack
Intracortical Excitation of Spiny Neurons in Layer 4 of Cat Striate Cortex In Vitro
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