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Journal of Neuroscience, Vol 12, 4327-4336, Copyright © 1992 by Society for Neuroscience
Posttetanic potentiation at the crayfish neuromuscular junction is dependent on both intracellular calcium and sodium ion accumulation
RM Mulkey and RS Zucker
Department of Molecular and Cell Biology, University of California, Berkeley 94720.
The fluorescent indicator fura-2 was used to measure cytoplasmic calcium in
presynaptic terminals in the crayfish Procambarus clarkii under conditions
that raise intracellular sodium to examine whether sodium can elevate
intracellular calcium concentration ([Ca2+]i) or prolong its efflux and
thus influence the magnitude and duration of posttetanic potentiation
(PTP). Sodium was elevated in presynaptic terminals at rest by either (1)
injection of sodium into the excitatory axon, (2) application of
veratridine to open sodium channels, or (3) addition of ouabain to block
Na/K exchange, with [Ca2+]i increasing by either 430, 400, or 180 nM,
respectively. Intracellular calcium concentration increased only when
external calcium was present, indicating that calcium influx occurred
through Na/Ca exchange. Additionally, ouabain enhanced excitatory
junctional potentials (EJPs) eightfold. Elevation of sodium using a
high-frequency stimulation in zero-calcium Ringer's did not elevate [Ca2+]i
during the train or immediately afterward when calcium-containing Ringer's
was re- introduced. This indicates that a physiological sodium load does
not release calcium from internal stores or reverse Na/Ca exchange to
levels where [Ca2+]i accumulation is detectable. We examined the ability of
sodium to interfere with calcium efflux from presynaptic terminals by
loading boutons with both sodium and calcium or calcium alone using
high-potassium depolarization. Elevation of internal sodium slowed calcium
efflux from the terminal (12.3 min) compared to calcium removal without a
sodium load (4.0 min). When sodium loading was increased during a tetanus
by application of ouabain, the time constants for decay of EJP
potentiation, 17.3 min, and for [Ca2+]i, 35 min, were longer than control
values, 4.4 min and 5.8 min, respectively. In addition, using lithium to
inhibit the efflux of calcium by Na/Ca exchange following a PTP-inducing
train also lengthened the decay of [Ca2+]i to 15.7 min. Intracellular
sodium accumulation in presynaptic terminals slows the efflux of calcium
through Na/Ca exchange, and may therefore augment and prolong PTP.
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