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The Journal of Neuroscience, February 15, 2000, 20(4):1374-1385
Interplay between Facilitation, Depression, and Residual Calcium
at Three Presynaptic Terminals
Jeremy S.
Dittman,
Anatol C.
Kreitzer, and
Wade G.
Regehr
Department of Neurobiology, Harvard Medical School, Boston,
Massachusetts 02115
Synapses display remarkable alterations in strength during
repetitive use. Different types of synapses exhibit distinctive synaptic plasticity, but the factors giving rise to such diversity are
not fully understood. To provide the experimental basis for a general
model of short-term plasticity, we studied three synapses in rat brain
slices at 34°C: the climbing fiber to Purkinje cell synapse, the
parallel fiber to Purkinje cell synapse, and the Schaffer collateral to
CA1 pyramidal cell synapse. These synapses exhibited a broad range of
responses to regular and Poisson stimulus trains. Depression dominated
at the climbing fiber synapse, facilitation was prominent at the
parallel fiber synapse, and both depression and facilitation were
apparent in the Schaffer collateral synapse. These synapses were
modeled by incorporating mechanisms of short-term plasticity that are
known to be driven by residual presynaptic calcium
(Cares). In our model, release is the product of two
factors: facilitation and refractory depression. Facilitation is caused by a calcium-dependent increase in the probability of release. Refractory depression is a consequence of release sites becoming transiently ineffective after release. These sites recover with a time
course that is accelerated by elevations of Cares.
Facilitation and refractory depression are coupled by their common
dependence on Cares and because increased transmitter
release leads to greater synaptic depression. This model captures the
behavior of three different synapses for various stimulus conditions.
The interplay of facilitation and depression dictates synaptic strength
and variability during repetitive activation. The resulting synaptic plasticity transforms the timing of presynaptic spikes into varying postsynaptic response amplitudes.
Key words:
short-term plasticity; residual calcium; cerebellar
granule cell; cerebellar Purkinje cell; climbing fiber; Schaffer
collateral; hippocampal CA1 pyramidal cell; synaptic model
Copyright © 2000 Society for Neuroscience 0270-6474/00/2041374-12$05.00/0
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|
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|
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|
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|
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|
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|
 |
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|
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|
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|
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|
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|
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|
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|
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[Full Text]
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|
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|
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|
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[Abstract]
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[PDF]
|
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|
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|

|
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|
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|
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|
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|
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|
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[PDF]
|
 |
|

|
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|
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[Full Text]
[PDF]
|
 |
|
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