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Journal of Neuroscience, Vol 9, 3558-3567, Copyright © 1989 by Society for Neuroscience
Calcium in motor nerve terminals associated with posttetanic potentiation
KR Delaney, RS Zucker and DW Tank
Department of Molecular and Cell Biology, University of California, Berkeley 94720.
We have used fura-2 fluorescence to study the effects of repetitive
stimulation producing posttetanic potentiation (PTP) at crayfish
neuromuscular junctions on presynaptic calcium concentration. Fura-2 was
injected into the preterminal axon of the excitor motor neuron to the claw
opener muscle of a walking leg. Pictures of presynaptic terminals on the
muscle surface were obtained with a charge-coupled device camera, ratioed,
and converted to spatial images of intracellular calcium concentration.
Stimulation of the motor nerve for 7-10 min at 20-33 Hz produced
potentiation during the tetanus and PTP following the tetanus. Presynaptic
calcium levels in terminal boutons and varicosities rose to about 2 microM
during the tetanus and decayed at first rapidly and then slowly back to
levels near the initial concentration of about 200 nM. The decay rate of
potentiated synaptic transmission was the same as the decay rate of the
elevated calcium concentration during the posttetanic period dominated by
PTP, when facilitation and augmentation had dissipated. A 13-fold
potentiation corresponded to a 500 nM elevation of calcium to about 700 nM.
The linear dependence we observed is not consistent with the power law
formulation of a residual calcium hypothesis for PTP. During the tetanus,
the enhancement of synaptic transmission due to facilitation, augmentation,
and potentiation exceeded that expected from the correspondence between PTP
and posttetanic calcium levels. This may occur because during the tetanus
there is insufficient time for calcium to equilibrate spatially between
action potentials, and the submembrane calcium will be higher than the
volume-average calcium levels that we detect. Following low-frequency
trains (typically 8 Hz for about 35 sec), enhanced synaptic transmission
and elevated presynaptic calcium decayed rapidly, within a few seconds.
Short high-frequency trains (50- 100 Hz for 1-2 min) elicited an additional
hours-long elevation of presynaptic calcium, corresponding to, and perhaps
responsible for, part of the long-term potentiation of transmission that
such stimulation produces at this synapse.
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