Rapid amplification and facilitation of mechanosensory discharge in Aplysia by noxious stimulation

Abstract

1. Little is known about modulation of action potential discharge in Aplysia mechanosensory neurons during defensive responses. The present studies examined rapid effects of noxious stimulation (occurring within 0.5-10 s) on the number of action potentials evoked by test stimuli delivered to the tail. Responses were monitored in the somata of mechanonociceptors in the pleural ganglion. A major hypothesis to be tested was that an important function of previously described alterations of membrane conductances in the sensory neuron soma is to generate an after-discharge that amplifies sensory signals during severe noxious stimulation of the cell's receptive field. 2. Discharge of spikes evoked by a moderate tap to one part of a sensory neuron's receptive field on the tail was enhanced by strong shock delivered 10 s earlier to another part of the field. Part of this enhancement appears to be due to a decrease in conduction block in central regions of the sensory neuron. 3. Repeated delivery of innocuous, moderately intense tail shock at 5-s intervals caused a progressive increase ("wind-up") of discharge, whereas repeated delivery of weak tail shock had no significant effect on discharge. In some cases the increase in action potential number involved a buildup of afterdischarge. 4. A single strong tail pinch sometimes induced an afterdischarge lasting < or = 2 s. Afterdischarge could also be induced in the isolated nervous system by intense electrical stimulation of the nerve containing the sensory neuron's main axon. 5. Several observations suggest that afterdischarge requires cooperative effects of a relatively large number of coactivated fibers in the test pathway. In contrast to pinching stimuli (which stimulated a larger part of the tail), intense, punctate stimulation with von Frey hairs failed to produce afterdischarge. Weaker tail or nerve stimulation failed to produce afterdischarge, even when short-latency, high-frequency discharge was evoked in the sensory neuron. 6. Cooperative effects on afterdischarge may differ from those involved in activity-dependent enhancement of presynaptic facilitation because simultaneous pairing of high-frequency activation of a single test sensory neuron with strong stimulation of a peripheral nerve lacking an axon of the tested sensory neuron was not sufficient to produce afterdischarge. The cooperative effects on afterdischarge may function to encode information about both the severity and spatial extensiveness of an injury. 7. Artificial hyperpolarization of the soma often reversibly reduced or abolished afterdischarge evoked by stimulating the nerve or tail. Thus the afterdischarge is often generated in or near the sensory neuron soma.(ABSTRACT TRUNCATED AT 400 WORDS)