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)

Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin‐A mRNA in Aplysia californica

“…Possible sensory functions of these newly discovered cells remain to be tested. On the other hand, extensive investigations of the LE clusters (Byrne et al, 1974(Byrne et al, , 1978aDubuc and Castellucci, 1991;Illich and Walters, 1997) and VC clusters (this paper; see also Walters et al, 1983;Walters, 1987;Billy and Walters, 1989a,b;Clatworthy and Walters, 1993b) indicate strongly that all of the cells in the LE and VC clusters have peripheral mechanosensory fields.…”

Non-Associative Learning and Serotonin Induce Similar Bi-Directional Changes in Excitability of a Neuron Critical for Learning in the Medicinal Leech

“…Changes in neuronal excitability during learning have been observed in other animals, including rabbit hippocampal neurons Thompson et al, 1996), rat cerebellar neurons (Armano et al, 2000), Hermissenda sensory neurons (Crow and Alkon, 1980;Frysztak and Crow, 1993), Helix interneurons (Gainutdinov et al, 1998), and Aplysia sensory neurons after delivery of a noxious stimulus (Clatworthy and Walters, 1993). In addition, serotonin enhances excitability in neurons known to contribute to learning and memory in both vertebrates and invertebrates (Klein et al, 1986;Andrade and Nicoll, 1987;Araneda and Andrade, 1991;Liao et al, 1999).…”

Localization of the myomodulin-like immunoreactivity in the leech CNS

“…Based on the anatomical distribution of the myomodulinlike immunoreactivity of the individual cells composing the touch-elicited shortening circuit, it appears that myomodulin could potentially mediate both intrinsic and extrinsic modulation of the reflex and the modulatory changes could occur at many levels ranging from the molecular to the cellular to the network. Recent work on Aplysia and the leech indicates neuromodulators could have a dramatic effect on behavior via the alteration of the number of action potentials that invade a neuron's synaptic terminals (Baylor and Nicholls, 1969;Clatworthy and Walters, 1993;Mar and Drapeau, 1993;Gu, 199 l ;Macagno et al, 1986). This raises interesting possibilities for the role of myomodulin in the neural modulation underlying learning in the leech.…”