A simplified preparation for relating cellular events to behavior: Mechanisms contributing to habituation, dishabituation, and sensitization of the Aplysia gill-withdrawal reflex

Abstract

To relate cellular events to behavior in a more rigorous fashion, we have developed a simplified preparation for studying the gill-withdrawal reflex of Aplysia, in which it is relatively easy to record the activity of individual neurons during simple forms of learning. Approximately 84% of the reflex in this preparation is mediated through the single motor neuron LDG1, so that changes in the firing of LDG1 can account for most of the changes in behavior. We have used this preparation to investigate cellular mechanisms contributing to habituation, dishabituation, and sensitization by recording evoked firing, the complex postsynaptic potential (PSP), and the monosynaptic component of the complex PSP in LDG1. Our results suggest that habituation is largely attributable to depression at sensory neuron synapses. By contrast, dishabituation and sensitization involve several mechanisms at different loci, including facilitation at sensory neuron synapses, enhancement in the periphery (perhaps attributable to post-tetanic potentiation at the neuromuscular junction), and both facilitation and inhibition of excitatory and inhibitory interneurons. Moreover, these different mechanisms contribute preferentially at different times after training, so that information processing in the neuronal circuit for the reflex is distributed not only in space but also in time. Nonetheless, our results also suggest that the neuronal circuit is not a highly distributed neural network. Rather, plasticity of the reflex can evidently be accounted for by several specific mechanisms and loci of plasticity in a defined neural circuit, including a limited number of neurons, some of which make a large contribution to the behavior.