Role of Amygdala Central Nucleus in Aversive Learning Produced by Shock or by Unexpected Omission of Food

Many psychological learning theories have noted commonalities between aversive states produced by presentation of negative reinforcers, such as electric shock, and the omission of expected positive reinforcers, such as food. Here, three groups of rats received training with one auditory cue paired with shock and another with the omission of expected food, a shock-paired cue and a food-omission control cue, or a food-omission cue and a shock control cue. Food-omission cues were established by contrast with food delivery; after extensive light-food pairings, the light was followed by the food-omission cue instead of food. Aversiveness of the food-omission cue was assessed with a conditioned punishment procedure, in which presentation of that cue was made contingent on performance of one previously trained instrumental response, whereas a second response had no consequences. We found that rats with lesions of amygdala central nucleus (CeA) showed impaired acquisition of freezing to the cue paired with shock and no evidence for acquisition of aversive properties by the cue that accompanied the omission of expected food. Furthermore, analyses of Arc and Homer1a mRNAs after rats were exposed to a two-epoch test procedure that allowed assessment of gene expression produced by two different test stimuli showed that both food-omission and shock-paired cues generated more neuronal activity in CeA than appropriate control cues. However, the number of neurons that were activated by both shock and food-omission cues was not significantly greater than expected by chance. Thus, under these test conditions, different subsets of CeA neurons represented these two aversive states.