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.(ABSTRACT TRUNCATED AT 250 WORDS)

Control of Neurotransmitter Release by Presynaptic Waveform at the Granule Cell to Purkinje Cell Synapse

“…The waveform of the depolarization dictates the calcium signal available to trigger vesicle fusion by controlling the opening of voltage-gated calcium channels and the driving force for calcium influx. Altering the presynaptic waveform has been shown to affect neurotransmitter release in many systems (Klein and Kandel, 1980;Llinas et al, 1981;Coates and Bulloch, 1985;Gainer et al, 1986;Spencer et al, 1989;Augustine, 1990;Delaney et al, 1991;Wheeler et al, 1996). For example, in Aplysia serotonin modulates presynaptic potassium channels, thereby broadening the action potential.…”

Heterologous Expression of the Kv3.1 Potassium Channel Eliminates Spike Broadening and the Induction of a Depolarizing Afterpotential in the Peptidergic Bag Cell Neurons

“…The duration of individual spikes often increases during a train of action potentials (Aldrich et al, 1979;Coates and Bulloch, 1985;Jackson et al, 1991). This progressive spike broadening can enhance transmitter release, probably by regulating the calcium signal that triggers secretion (Jackson et al, 1991).…”

Stimulus History Reliably Shapes Action Potential Waveforms of Cortical Neurons

“…Even injecting a steady current step produces several action potentials of different shapes, with a correlation between spike frequency and spike broadening (Kandel and Spencer, 1961;Aldrich et al, 1979;Fox and Ranck, 1981). Sodium and potassium channels are responsible for activitydependent spike amplitude reduction and broadening (Grossman et al, 1979;Coates and Bullock, 1985;Gillette et al, 1980;Jackson et al, 1991;Wang and Kaczmarek, 1998;Geiger and Jonas, 2000).…”