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The Journal of Neuroscience, April 15, 2003, 23(8):3186
Independent Sources of Quantal Variability at Single
Glutamatergic Synapses
Kevin M.
Franks1, 2, 4,
Charles F.
Stevens1, 3, and
Terrence J.
Sejnowski1, 2, 4
1 Howard Hughes Medical Institute,
2 Computational and 3 Molecular Neurobiology
Laboratories, The Salk Institute for Biological Studies, La Jolla,
California 92037, and 4 Division of Biology, University of
California, San Diego, La Jolla, California 92093
Variability in the size of single postsynaptic responses is a
feature of most central neurons, although the source of this variability is not completely understood. The dominant source of
variability could be either intersynaptic or intrasynaptic. To
quantitatively examine this question, a biophysically realistic model
of an idealized central axospinous synapse was used to assess mechanisms underlying synaptic variability measurements. Three independent sources of variability were considered: stochasticity of
postsynaptic receptors ("channel noise"), variations of
glutamate concentration in the synaptic cleft ( q),
and differences in the potency of vesicles released from different
locations on the active zone [release-location dependence
(RLD)]. As expected, channel noise was small (8% of the total
variance) and q was the dominant source of
variability (58% of total variance). Surprisingly, RLD accounted for a
significant amount of variability (36%). Our simulations show that
potency of release sites decreased with a length constant of ~100 nm,
and that receptors were not activated by release events >300 nm away,
which is consistent with the observation that single active zones are
rarely >300 nm. RLD also predicts that the manner in which receptors
are added or removed from synapses can dramatically affect the nature
of the synaptic response, with increasing receptor density being more
efficient than merely increasing synaptic area. Saturation levels and
synaptic geometry were also important in determining the size and shape
of the distribution of amplitudes recorded at different synapses.
Key words:
synaptic variability; glutamate concentration; saturation; synaptic geometry; computational model; Monte Carlo
methods
Copyright © 2003 Society for Neuroscience 0270-6474/03/2383186-10$05.00/0
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