A persistent cellular change in a single modulatory neuron contributes to associative long-term memory.
Most neuronal models of learning assume that changes in synaptic strength are the main mechanism underlying long-term memory (LTM) formation. However, we show here that a persistent depolarization of membrane potential, a type of cellular change that increases neuronal responsiveness, contributes significantly to a long-lasting associative memory trace. The use of a model invertebrate network with identified neurons and known synaptic connectivity had the advantage that the contribution of this cellular change to memory could be evaluated in a neuron with a known function in the learning circuit. Specifically, we used the well-understood motor circuit underlying molluscan feeding and showed that a key modulatory neuron involved in the initiation of feeding ingestive movements underwent a long-term depolarization following behavioral associative conditioning. This depolarization led to an enhanced single cell and network responsiveness to a previously neutral tactile conditioned stimulus, and the persistence of both matched the time course of behavioral associative memory. The change in the membrane potential of a key modulatory neuron is both sufficient and necessary to initiate a conditioned response in a reduced preparation and underscores its importance for associative LTM.
Jones
Nicholas G
NG
Sussex Centre for Neuroscience, School of Biological Sciences, University of Sussex, Falmer, Brighton BN1 9QG, United Kingdom.
Kemenes
Ildikó
I
Kemenes
György
G
Benjamin
Paul R
PR
D000818:Animals; D001245:Association Learning / Q000502:physiology*; D004594:Electrophysiology; D005247:Feeding Behavior / Q000502:physiology; D008195:Lymnaea / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology*; D008568:Memory / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology*; D016571:Neural Networks, Computer; D013997:Time Factors