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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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J. Neurosci., January 15, 2002; 22(2): 584 - 591.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
G. Fuhrmann, I. Segev, H. Markram, and M. Tsodyks
Coding of Temporal Information by Activity-Dependent Synapses
J Neurophysiol, January 1, 2002; 87(1): 140 - 148.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. R. Muller, A. B. Metha, J. Krauskopf, and P. Lennie
Information Conveyed by Onset Transients in Responses of Striate Cortical Neurons
J. Neurosci., September 1, 2001; 21(17): 6978 - 6990.
[Abstract] [Full Text] [PDF]


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


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J. Neurophysiol.Home page
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]


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


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


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J. Neurophysiol.Home page
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]


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J. Neurosci.Home page
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
J. Neurosci., April 1, 2001; 21(7): 2308 - 2319.
[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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J. Neurosci.Home page
E. S. Fortune and G. J. Rose
Short-Term Synaptic Plasticity Contributes to the Temporal Filtering of Electrosensory Information
J. Neurosci., September 15, 2000; 20(18): 7122 - 7130.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
W. M. Usrey, J.-M. Alonso, and R. C. Reid
Synaptic Interactions between Thalamic Inputs to Simple Cells in Cat Visual Cortex
J. Neurosci., July 15, 2000; 20(14): 5461 - 5467.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
M. V. Sanchez-Vives, L. G. Nowak, and D. A. McCormick
Membrane Mechanisms Underlying Contrast Adaptation in Cat Area 17 In Vivo
J. Neurosci., June 1, 2000; 20(11): 4267 - 4285.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
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
J Neurophysiol, May 1, 2000; 83(5): 3031 - 3041.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
D. L. Brody and D. T. Yue
Release-Independent Short-Term Synaptic Depression in Cultured Hippocampal Neurons
J. Neurosci., April 1, 2000; 20(7): 2480 - 2494.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
D. Parker
Activity and Calcium-Dependent Mechanisms Maintain Reliable Interneuron Synaptic Transmission in a Rhythmic Neural Network
J. Neurosci., March 1, 2000; 20(5): 1754 - 1766.
[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
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]


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J. Neurophysiol.Home page
A. V. Galazyuk, D. Llano, and A. S. Feng
Temporal Dynamics of Acoustic Stimuli Enhance Amplitude Tuning of Inferior Colliculus Neurons
J Neurophysiol, January 1, 2000; 83(1): 128 - 138.
[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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