Adaptive emotional behavior requires subjects to generate responses to innately rewarding or aversive stimuli as well as to conditioned stimuli whose relationship to impending reinforcement often changes through learning or regulation. Evidence has accumulated implicating the amygdala as a critical structure in mediating these processes. We pursue a two-pronged approach for elucidating amygdalar mechanisms underlying innate, learned, and regulated emotional behavior. First, we use a genetic strategy to identify representations of innately rewarding and aversive stimuli (unconditioned stimuli, USs) in the basolateral amygdala (BLA) and examine their role in innate and learned responses. Activation of an ensemble of US-responsive cells in the BLA elicits innate physiological and behavioral responses of different valence. Activation of this US ensemble can also reinforce appetitive and aversive learning when paired with differing neutral stimuli. Moreover, activation of US-responsive cells in the BLA is necessary for the expression of a conditioned response. Neural representations of conditioned and unconditioned stimuli must therefore ultimately connect to US-responsive cells in the BLA to elicit both innate and learned responses. Second, we examine the neurophysiological mechanisms that may mediate how representations of emotional significance in the amygdala may be regulated. Subjects perform a task in which reinforcement prediction required identifying a stimulus, knowing the context in which the stimulus appeared, and understanding context-dependent reinforcement contingencies. It is commonly assumed that processing in the prefrontal cortex (PFC) helps confer emotional flexibility on this type of task since PFC neurons encode rules, goals and other abstract information. Surprisingly, we discovered that neurons in the amygdala also represents abstract cognitive information. Disappearance of this abstract representation in the amygdala predicts errors in reward anticipation, a finding not observed for PFC. These data emphasize the potential importance of maintaining abstract cognitive information in the amygdala to support the flexible regulation of emotion.