Two-stage theory of conditioning: involvement of the cerebellum and the amygdala.

Classical conditioning is thought to proceed through two successive stages: fast rate emotional conditioning followed by slower motor conditioning. To verify the involvement of the amygdala and the cerebellum in these two stages of learning, rats were subjected to paired tone-airpuff (CS-US) trials. Lick suppression to CS was used as an index of conditioned emotional response (emotional CRs) and head movement was used as an index of motor CRs. The results showed that the fast acquisition of emotional CRs was dependent on the integrity of the amygdala and the slow acquisition of motor CRs was dependent on the integrity of the cerebellar interpositus nucleus. Cerebellar lesions had no effect on the acquisition of the emotional CRs but prevented the extinction of the emotional CRs seen in intact rats after massive conditioning. These findings suggest that the amygdala and the cerebellum provide the neuronal substrates of the fast and slow conditioning systems, respectively, and that conditioning-related cerebellar output interacts with the amygdala-based emotional conditioning.