The Journal of Neuroscience, April 12, 2006, 26(15):4139-4146; doi:10.1523/JNEUROSCI.0489-06.2006
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Behavioral/Systems/Cognitive
Associative Memory Stored by Functional Novel Pathway rather than Modifications of Preexisting Neuronal Pathways
Volko A. Straub,
Ildiko Kemenes,
Michael OShea, and
Paul R. Benjamin
Sussex Centre for Neuroscience, School of Biology and Environmental Science, University of Sussex, Falmer, Brighton BN1 9QG, United Kingdom
Correspondence should be addressed to Volko A. Straub at his present address: Department of Cell Physiology and Pharmacology, University of Leicester, Maurice Shock Medical Sciences Building, P.O. Box 138, University Road, Leicester LE1 9HN, UK. Email: vs64{at}le.ac.uk
Associative conditioning involves changes in the processing pathways activated by sensory information to link the conditioned stimulus (CS) to the conditioned behavior. Thus, conditioning can recruit neuronal elements to form new pathways for the processing of the CS and/or can change the strength of existing pathways. Using a behavioral and systems level electrophysiological approach on a tractable invertebrate circuit generating feeding in the mollusk Lymnaea stagnalis, we identified three independent pathways for the processing of the CS amyl acetate used in appetitive conditioning. Two of these pathways, one suppressing and the other stimulating feeding, mediate responses to the CS in naive animals. The effects of these two pathways on feeding behavior are unaltered by conditioning. In contrast, the CS response of a third stimulatory pathway is significantly enhanced after conditioning, becoming an important contributor to the overall CS response. This is unusual because, in most of the previous examples in which naive animals already respond to the CS, memory formation results from changes in the strength of pathways that mediate the existing response. Here, we show that, in the molluscan feeding system, both modified and unmodified pathways are activated in parallel by the CS after conditioning, and it is their integration that results in the conditioned response.
Key words: learning; memory; conditioning; Lymnaea; chemosensory processing; sensory integration
Received Sept. 19, 2005;
revised March 6, 2006;
accepted March 11, 2006.
Correspondence should be addressed to Volko A. Straub at his present address: Department of Cell Physiology and Pharmacology, University of Leicester, Maurice Shock Medical Sciences Building, P.O. Box 138, University Road, Leicester LE1 9HN, UK. Email: vs64{at}le.ac.uk
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