Classical conditioning in a simple withdrawal reflex in Aplysia californica.

The ability of Aplysia and other gastropod molluscs to exhibit complex behaviors that can be modified by associative learning has encouraged us to search for an elementary behavior controlled by a simple and well analyzed neural circuit that also can be modified by this type of learning. Toward that end, we have now produced classical conditioning in the defensive siphon and gill withdrawal reflex of Aplysia. We used as a conditioned stimulus (CS) a light tactile stimulus to the siphon, which produces weak siphon and gill withdrawal. As the unconditioned stimulus (US), we used a strong electric shock to the tail, which produces a massive withdrawal reflex. Specific temporal pairing of the CS and US endowed the CS with the ability of triggering enhanced withdrawal of both the siphon and the gill. Random or unpaired presentations of the CS and US, as well as presentations of the CS or US alone, produced either no enhancement or significantly less enhancement than paired presentations of the CS and US. The conditioning is acquired rapidly (within 15 trials) and is retained for several days. The conditioned response is abolished completely by removal of the abdominal ganglion and many of the neurons involved in the conditioning have been identified in this ganglion previously. These include the sensory neurons and several interneurons in the CS pathway and the siphon and gill motor neurons of the conditioned and unconditioned response pathways. Moreover, the sensory neurons of the US pathway have been identified in the pleural ganglia. As a result of its simplicity, it should be possible in this reflex to specify neurons that are causally related to the conditioned response. Since this reflex also exhibits nonassociative learning, it also may be possible to compare associative and nonassociative learning on a mechanistic level.