Onset and offset of aversive events establish distinct memories requiring fear and reward networks

Abstract

Two things are worth remembering about an aversive event: What made it happen? What made it cease? If a stimulus precedes an aversive event, it becomes a signal for threat and will later elicit behavior indicating conditioned fear. However, if the stimulus is presented upon cessation of the aversive event, it elicits behavior indicating conditioned "relief." What are the neuronal bases for such learning? Using functional magnetic resonance imaging (fMRI) in humans we found that a fear-conditioned stimulus activates amygdala but not striatum, whereas a relief-conditioned stimulus activates striatum but not amygdala. Correspondingly, acute inactivation of amygdala or of ventral striatum in rats respectively abolished only conditioned fear or only conditioned relief. Thus, the behaviorally opponent memories supported by onset and offset of aversive events engage and require fear and reward networks, respectively. This may explain attraction to stimuli associated with the cessation of trauma or of panic attacks.