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Experimental extinction is the decline in the frequency or intensity of a conditioned behaviour resulting from repetitive performance of the behaviour in the absence of the unconditioned stimulus or reinforcer (Pavlov, 1927). Ample behavioural evidence indicates that experimental extinction does not reflect unlearning of the original trace, but rather a relearning process, in which the new association of the conditioned stimulus with the absence of the original reinforcer comes to control behaviour (Rescorla, 1996). If experimental extinction is indeed learning rather than forgetting, are the neuronal circuits that subserve learning and extinction identical? We address this question by double dissociation analysis of the role of the central (CeA) and the basolateral (BLA) nuclei of the rat's amygdala in the acquisition and extinction, respectively, of conditioned taste aversion (CTA). Whereas local blockade of protein synthesis or beta-adrenergic receptors in the CeA blocks acquisition but not extinction of CTA, a similar intervention in the BLA blocks extinction but not acquisition. Hence, the amygdalar circuit that acquires taste aversion memory differs functionally from the circuit that extinguishes it.

The study of experimental extinction and of the spontaneous recovery of the extinguished memory could cast light on neurobiological mechanisms by which internal representations compete to control behavior. In this work, we use a combination of behavioral and molecular methods to dissect subprocesses of experimental extinction of conditioned taste aversion (CTA). Extinction of CTA becomes apparent only 90 min after the extinction trial. This latency is insensitive to muscarinic and beta-adrenergic modulation and to protein synthesis inhibition in the insular cortex (IC). Immediately afterwards, however, the extinguishing trace becomes sensitive to beta-adrenergic blockade and protein synthesis inhibition. The subsequent kinetics and magnitude of extinction depend on whether a spaced or massed extinction protocol is used. A massed protocol is highly effective in the short run, but results in apparent stagnation of extinction in the long-run, which conceals fast spontaneous recovery of the preextinguished trace. This recovery can be truncated by a beta-adrenergic agonist or a cAMP analog in the insular cortex, suggesting that spontaneous overtaking of the behavioral control by the original association is regulated at least in part by beta-adrenergic input, probably operating via the cAMP cascade, long after the offset of the conditioned stimulus. Hence, the performance of the subject in experimental extinction is the sum total of multiple, sometimes conflicting, time-dependent processes.