Comparison of differential pavlovian conditioning in whole animals and physiological preparations ofPleurobranchaea: Implications of motor pattern variability

Abstract

The present study compares differential Pavlovian conditioning in whole animals with the behavior of the same animals during electrophysiological recording. Untrained specimens of the sea slug Pleurobranchaea did not discriminate between two appetitive stimuli, one derived from an extract of beer (S_br) and the other from a homogenate of squid muscle (S_sq). When animals received S_br as the CS⁺ and S_sq as the CS⁻ in a single day of five-trial, differential Pavlovian conditioning they learned to avoid selectively the S_br but continued to exhibit appetitive responses to S_sq. Quantitative measures show that there was over a 1000-fold increase in the thresholds of the proboscis extension and bite-strike responses, many animals ceased all feeding behavior, and exhibited withdrawal responses to S_br. We examined the behavior of the same trained animals immediately before preparing them for physiological recording and during the recording session. There was a close one-to-one relationship between these behavioral observations, showing that the qualitative and quantitative features of whole-animal Pavlovian conditioning persist into the physiological preparations. Unexpectedly, motor patterns from untrained preparations showed considerable variability both within the same preparation at different times and between preparations; conditioning appeared to increase such variability. Thus, it was not possible to state unequivocally the behavior of the animal by examining the electromyogram recording alone. Many of the trained preparations not only exhibited suppressed feeding behavior and withdrawal responses to S_br, but, as a consequence of the multifunctional nature of the Pleurobranchaea buccal-oral system, also regurgitated previously ingested S_sq or squid meat when they were stimulated with S_br. We discuss the findings with respect to self-organizing mechanisms that may establish motor patterns in multifunctional systems, and suggest that such mechanisms may lead to the generation of behaviors that are not specifically encoded by the conditioned cellular changes.