Conditioned memory modulation, freezing, and avoidance as measures of amygdala-mediated conditioned fear

Abstract

Three conditioned aversive responses were used to infer the existence of an unobservable central state of "conditioned fear," and the roles of certain amygdala subregions in producing these responses were investigated. Rats received tone-shock pairings in one compartment of a shuttle box and no tones or shocks in the other, distinctive, compartment. They were then trained to find food in one arm of a Y-maze. After the final training trial they were exposed to different sets of stimuli in the shuttle box with no shock. Twenty-four hours later rats that had received immediate posttraining exposure to the conditioned stimuli (in the shock-paired compartment) made significantly more correct responses on the Y-maze than rats that had been exposed to the neutral stimuli (in the no-shock compartment) or rats that had received delayed posttraining exposure to the conditioned stimuli. This constitutes a demonstration of posttraining memory modulation by conditioned aversive stimuli. Freezing increased during posttraining exposure to the conditioned stimuli compared to the neutral stimuli. When subsequently allowed to move freely between the two compartments, the rats in all groups also showed significant conditioned avoidance of the compartment containing the conditioned stimuli. In a second experiment the effects of lesions confined to specific parts of the amygdala on the three conditioned responses (memory modulation, freezing, avoidance) were tested. Lesions of the central nucleus impaired all three conditioned responses; lesions of the medial nucleus impaired conditioned modulation and avoidance. These lesions had no effect on freezing during the training trials. Lesions of the lateral and basolateral nuclei attenuated freezing during both training and testing. The findings suggest that the central and medial nuclei of the amygdala may be important parts of neural circuits mediating conditioned responses that constitute conditioned aversive states, but that conditioned freezing may be mediated independently.