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The Journal of Neuroscience, December 15, 2004, 24(50):11391-11403; doi:10.1523/JNEUROSCI.2756-04.2004

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Cellular/Molecular
Augmentation Increases Vesicular Release Probability in the Presence of Masking Depression at the Frog Neuromuscular Junction

Jonathan M. Kalkstein and Karl L. Magleby

Department of Physiology and Biophysics and Neuroscience Program, University of Miami School of Medicine, Miami, Florida 33136

Synaptic augmentation is a short-term component of synaptic plasticity that increases transmitter release during repetitive stimulation and decays thereafter with a time constant of 7 sec. Augmentation has typically been observed under conditions where there is little or no depression because of depletion of synaptic vesicles from the readily releasable pool (RRP) of transmitter. We now study augmentation under conditions of pronounced depression at the frog neuromuscular junction to gain additional insight into mechanism. If augmentation reflects an increase in the size of the RRP of transmitter, then augmentation should not be present with depression. Our findings using four different experimental approaches suggested that augmentation was still present in the presence of pronounced depression: mathematical extraction of augmentation from the changes in transmitter release after repetitive stimulation, identification of augmentation with Ba²⁺, correction of the data for the measured depletion of the RRP, and identification of an augmentation component of residual Ca²⁺. We conclude that the augmentation machinery still acts to increase transmitter release when depression reduces the RRP sufficiently to mask obvious augmentation. The masked augmentation was found to increase transmitter release by increasing the probability of releasing individual vesicles from the depressed RRP, countering the effects of depression. Because augmentation and depression have similar time courses, either process can mask the other, depending on their relative magnitudes. Consequently, the apparent absence of one of the processes does not exclude that it is still contributing to short-term synaptic plasticity.

Key words: synaptic augmentation; synaptic depression; synaptic transmission; readily releasable pool; synaptic plasticity; Ca²⁺ imaging

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Received April 19, 2004; revised November 2, 2004; accepted November 3, 2004.

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