Organization of neural systems for aversive information processing: pain, error, and punishment

The avoidance of aversive events is critically important for the survival of organisms. It has been proposed that the medial pain system, including the amygdala, periaqueductal gray (PAG), and anterior cingulate cortex (ACC), contains the neural circuitry that signals pain affect and negative value. This system appears to have multiple defense mechanisms, such as rapid stereotyped escape, aversive association learning, and cognitive adaptation. These defense mechanisms vary in speed and flexibility, reflecting different strategies of self-protection. Over the course of evolution, the medial pain system appears to have developed primitive, associative, and cognitive solutions for aversive avoidance. There may be a functional grading along the caudal-rostral axis, such that the amygdala-PAG system underlies automatic and autonomic responses, the amygdala-orbitofrontal system contributes to associative learning, and the ACC controls cognitive processes in cooperation with the lateral prefrontal cortex. A review of behavioral and physiological studies on the aversive system is presented, and a conceptual framework for understanding the neural organization of the aversive avoidance system is proposed.