Activity-dependent depression of mechanosensory discharge in Aplysia

Abstract

1. Inhibition of action potential discharge in Aplysia mechanosensory neurons after noxious stimulation has not been described previously. The present studies investigated depressive effects of prolonged noxious stimulation and repetitive intracellular activation on the number and latency of action potentials evoked by test stimuli applied to the tail or the nerve innervating the tail. Action potential discharge was monitored in the somata of mechanonociceptors in the pleural ganglia. 2. Repeated brief pinches delivered at 5-s intervals to a sensory neuron's receptive field on the tail initially caused intense activation (10-25 spikes recorded in the soma) followed by a progressive decrease or "wind-down" of spike number during subsequent pinches. 3. Repeated application to the tail of noxious shock that caused intense activation of sensory neurons (10-22 spikes during the initial shock) produced progressive wind-down of discharge similar to that produced by repeated tail pinch. However, sensory neurons that showed lower activation (1-9 spikes) to the same shock displayed wind-up of discharge during the 10 shocks. These results suggested that prolonged, intense activation depresses subsequent action potential discharge. 4. Changes in the time required for spikes evoked in the tail to reach the central soma were used as an indicator of changes in the excitability and/or conduction velocity of peripheral branches. Repeated pinch within a sensory neuron's receptive field caused an increase in the latency of discharge elicited by test shocks within the receptive field that lasted > or = 10 min. Repetitive intracellular stimulation of the sensory neuron soma caused a similar increase in latency. 5. Repetitive soma activation decreased the number of spikes evoked 10 s later by a test shock in the sensory neuron's receptive field, indicating that spike activity depresses the initiation and/or conduction of spikes in peripheral branches. Surprisingly, repeated pinch to the receptive field caused no significant change in the number of spikes evoked by the same test shock. This difference suggests that tail pinch produces concomitant facilitatory effects that oppose the depressive effects of intense spike activity. 6. Depressive effects of repeated pinch and repetitive soma activation were expressed in the axon between the receptive field and the CNS. Spikes evoked by brief test shocks delivered to the nerve containing the axon of the recorded sensory neuron showed a transient increase in latency (perhaps due to a decrease in conduction velocity) after either procedure. Repeated pinch, but not repetitive soma activation, also caused an increase in spike threshold in the nerve.(ABSTRACT TRUNCATED AT 400 WORDS)

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

“…(2) The sensory neurons that we recorded from, which respond to the tail stimuli, also generate progressively fewer action potentials, and they respond with increasing latency to each stimulus. A similar decrease in spike number and increase in response latency in tail sensory neurons has been observed after noxious, repetitive tail stimulation (Clatworthy and Walters, 1993). These authors refer to the action potential number and latency changes collectively as response "wind-down."…”

“…5A,C2). These results reveal that at least two forms of plasticity occur at the level of the primary sensory neuron response to habituating stimuli: (1) reduction of spike number and (2) increase in spike latency (Clatworthy and Walters, 1993) (also see Discussion). Both of these forms of plasticity seem consistent with the overall response decrement observed behaviorally and at the level of the complex EPSP in tail and siphon motor neurons.…”

Memory-Like Alterations inAplysiaAxons after Nerve Injury or Localized Depolarization

“…2 A). In addition, hyperpolarizing responses to p9 shock, which can block conduction of sensory neuron spikes (Clatworthy and Walters, 1993b), were completely blocked by low-Ca saline in every sensory neuron tested (n ϭ 6) ( Fig. 2 B).…”

“…1). However, nerve shock can evoke contractile responses of the nerve (Umitsu et al, 1987) that might change effective test current density, and it can alter the number of action potentials conducted to the central soma by causing the release of neuromodulators in the CNS (Clatworthy and Walters, 1993b) and perhaps the nerve. Because contraction of smooth muscle cells and exocytosis of neuroactive substances are often highly dependent on extracellular Ca 2ϩ , we attempted to minimize these complications by delivering nerve test stimuli in low-Ca saline containing 1% normal extracellular [Ca 2ϩ ].…”

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

“…Evidence for an axon was usually the elicitation of overshooting action potentials, but all-ornone blocked spikes were occasionally elicited (see Fig. 9D; see also Clatworthy and Walters, 1993a). Because spikes are not evoked by synaptic inputs to VC cells, most of the receptive field mapping of this cluster was performed in ASW, although a few receptive fields of VC cluster and S cluster neurons were tested with the periphery bathed in 1% [Ca 2ϩ ] solution in order to block peripheral synaptic transmission.…”