Synaptic plasticity in the molluscan peripheral nervous system: physiology and role for peptides

Abstract

The plasticity of a synapse in the molluscan peripheral nervous system was examined under a variety of experimental, physiological, and pharmacological conditions. These studies employed the isolated salivary glands and attached buccal ganglia of the freshwater snail Helisoma. Action potentials evoked in buccal neuron 4 normally evoke a large excitatory postsynaptic potential (EPSP) which drives an action potential in gland secretory cells. In order to measure modulation of the EPSP, action potential generation in gland cells was prevented by bathing the preparation in low calcium, high magnesium salines. The relationship between the gland EPSP amplitude and specific physiological properties of neuron 4 was analyzed. In common with some central molluscan synapses, the EPSP was found to be strongly influenced by the membrane potential of neuron 4. Specifically, its amplitude was reduced by hyperpolarization of the neuron 4 soma. The relationship between EPSP amplitude and somatic potential of neuron 4 was linear in the range from resting potential (-47 .+-. 6mV) to-100 mV. Furthermore, the EPSP amplitude was directly proportional to the action potential half-width of neuron 4. In order to evaluate the possible physiological role of this action potential/EPSP relationship, we examined whether gland EPSPs are modulated during the spike broadening that occurs in both spontaneous burst activity and imposed impulse trains. The preceding action potential/EPSP relationship was maintained under both of these conditions, i.e., EPSP magnitude increased as spikes broadened during bursts or trains. The peptidergic modulation of neuroglandular transmission was also examined. The molluscan peptide SCPB was found to depolarize neuron 4 and an increase in EPSP amplitude was concomitantly observed. This increase in EPSP amplitude was attributed to the spike broadening accompanying depolarization of neuron 4. Accordingly, both EPSP and spike parameters were restored to control values by repolarization of neuron 4. In contrast, the molluscan tetrapeptide FMRF-amide was found to decrease EPSP amplitude by both hyperpolarizing neuron 4 and by direct hyperpolarization and conductance increase of gland cells. In this case, repolarization of neuron 4 restored the action potential but caused only partial restoration of the EPSP amplitude. We conclude that the neuroglandular synapse of Helisoma shows plasticity under a variety of physiological and pharmacological conditions which involve changes of presynaptic action potential parameters.