Neural mechanisms of reward processing and emotion

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Neurons in both the orbitofrontal cortex (OFC) and medial frontal cortex (MFC) encode the sensory properties, magnitude and subjective value of expected and received rewarding outcomes. In addition, the activity of neurons in these regions reflects anticipatory arousal, as measured by pupil diameter. Decision-making and representations of arousal are intimately linked. How these processes interact at the level of single neurons as well as neural circuits are unknown. To understand how OFC and MFC influence arousal and decision making, we recorded neural activity from both regions while animals made reward-guided decisions. Heart rate (HR) was recorded as a proxy for arousal. In intact animals we found that higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and MFC selectively encoded trial-by-trial variations in HR independent of reward magnitude. After amygdala lesions, HR generally increased and the relationship between HR and RTs was reversed. Concurrent with this change, there was an increase in the proportion of MFC neurons encoding HR. At the population level, the balance of encoding in MFC shifted towards signaling HR, suggesting a specific mechanism through which arousal influences decision-making. The amygdala, along with the orbitofrontal cortex (OFC), has been implicated in stimulus-reward learning, affect, and modulation of autonomic arousal. For example, as noted above, the amygdala contributes to the development of neural activity in OFC related to stimulus-reward processing, and removal of the amygdala causes a reduction in both expected and received reward-value coding by OFC neurons. In animals, amygdala lesions have been reported to disrupt autonomic responses to the sight of highly palatable foods but not autonomic responses that accompany consumption of that food. In a Pavlovian conditioning task, humans with amygdala damage were found deficient in their autonomic responses to visual stimuli that predicted aversive outcomes and after receipt of those outcomes. It is not known, however, how selective amygdala removal affects autonomic responses during comparable stimulus-reward learning in animals. To investigate this issue, we tested animals with bilateral excitotoxic lesions of the amygdala and unoperated controls on an appetitive Pavlovian task, using conditioned autonomic responses (pupil size change) as our measure of learning. We examined how many sessions the monkeys needed to show pupil responses that differed significantly between CS+ and CS-, and whether the conditioned pupil responses were maintained across 4 consecutive sessions. We found no group differences in either the development of conditioned pupil responses or the ability to maintain those responses across days. Our results indicate that the amygdala is not necessary for the generation of sympathetic autonomic arousal in anticipation of fluid reward, at least as determined by a change in pupil responses. These results argue against the idea that the amygdala is essential for generating anticipatory autonomic responses to guide decision making.