Effects of amygdala lesions on overexpectation phenomena in food cup approach and autoshaping procedures

Prediction error (PE) plays a critical role in most modern theories of associative learning, by determining the effectiveness of conditioned stimuli (CS) or unconditioned stimuli (US). Here, we examined the effects of lesions of central (CeA) or basolateral (BLA) amygdala on performance in overexpectation tasks. In 2 experiments, after 2 CSs were separately paired with the US, they were combined and followed by the same US. In a subsequent test, we observed losses in strength of both CSs, as expected if the negative PE generated on reinforced compound trials encouraged inhibitory learning. CeA lesions, known to interfere with PE-induced enhancements in CS effectiveness, reduced those losses, suggesting that normally the negative PE also enhances cue associability in this task. BLA lesions had no effect. When a novel cue accompanied the reinforced compound, it acquired net conditioned inhibition, despite its consistent pairings with the US, consonant with US effectiveness models. That acquisition was unaffected by either CeA or BLA lesions, suggesting different rules for assignment of credit of changes in cue strength and cue associability. Finally, we examined a puzzling autoshaping phenomenon previously attributed to overexpectation effects. When a previously food-paired auditory cue was combined with the insertion of a lever and paired with the same food US, the auditory cue not only failed to block conditioning to the lever, but also lost strength, as in an overexpectation experiment. This effect was abolished by BLA lesions but unaffected by CeA lesions, suggesting it was unrelated to other overexpectation effects.