Neural mechanisms of reward processing and emotion

National Institute Of Mental Health

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Abstract

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. As a step to develop a method to study affect and mood regulation, we measured heart rates of animals while they performed tasks in which different fluid reward amounts were cued. Heart rate was measured with a pulse oximetry sensor. Animals were trained on a choice task in which different visual cues signaled different magnitudes of fluid reward. A fixed set of 7 cues was associated with fixed amounts of fluid, ranging from 0.15 ml to 1.05 ml. A trial began when the subject pressed a central button for 1.5 s. Then two visual cues, pseudo-randomly selected from the set, were presented for 1.5 s, one on each side of the monitor. The animal could choose the cue on the left or right side of the screen by selecting and pressing either the left or right button, respectively, after which a 1.5-s waiting period ensued. At the end of the waiting period, the fluid reward amount associated with the chosen cue was delivered. The temporal separation of the cue period and reward delivery ensured that any change in heart rate during the cue period could not be attributed to breath holding or other reward consumption activities. We found that the heart rates increased as the reward amount became larger. The changes in the heart rate began to occur approximately 500 ms after the cue onset. The heart rates during the cue period were analyzed with a regression model which included variables such as the location of the larger reward, choice direction, reaction time and the amount of the larger reward. The heart rate during the cue period was significantly related to the amount of the larger reward (t-test; p < 0.01), but not to the reaction time (p > 0.05). Our results show that heart rate can be modulated fast enough to reflect trial-by-trial changes of attention, arousal or motivation.