Presynaptic long-term facilitation at the crayfish neuromuscular junction: voltage-dependent and ion-dependent phases

Abstract

Long-term facilitation (LTF) of synaptic transmission was investigated in the crayfish opener muscle to determine the factors necessary for its induction and expression. LTF was induced without action potentials by intracellular depolarization of presynaptic nerve terminals. Following induction, the synaptic transmission was enhanced by about 80% for a period of several hours. Intracellular recordings from pre- and postsynaptic cells, combined with ionic and pharmacological tests, permitted dissection of LTF into 2 phases: an initial tetanic phase that depended on the presence of both sodium and calcium ions and a subsequent long-lasting phase. This latter long-lasting enhancement of synaptic transmission was induced by repeated depolarizations of synaptic terminals but did not depend on the influx of sodium or calcium ions or on intracellular release of calcium ions. Both tetanic and long-lasting phases of LTF are attributable to activity of a single neuron, i.e., they are homosynaptic phenomena. Furthermore, LTF is associated with an increase of quantal release, whereas the size of quanta remains unchanged. During the long-lasting phase of LTF, the nerve terminal releases more transmitter for a given depolarization than before induction of LTF. Thus, the locus of LTF is presynaptic. Our findings suggest the presence of a voltage-dependent mechanism in the presynaptic membrane different from voltage-gating of Na or Ca channels. Such a mechanism may be important in the establishment of long-lasting synaptic changes at the crayfish neuromuscular junction and perhaps in other neural systems.