Differential and temporally dynamic involvement of primate amygdala nuclei in face reality and reward information processing

Abstract

Decision-making is influenced by both expected rewards and social factors, such as who offers the outcomes. Therefore, although a reward might originally be independent of social factors, the two elements are closely related. However, whether and how they are processed separately or conjointly remains unclear. Here, we show that neurons in distinct sub-nuclei of the amygdala encode expected reward and face reality, a vital aspect of face perception. Although these encoding processes are distinct, they rely on partially shared neuronal circuits with characteristic temporal dynamics. Two male macaque monkeys made saccades under different social and reward contexts by viewing facial images with independent attributes: reality (a real monkey or a cartoon face) and associated reward (large or small). The stimulus image was presented twice per trial: during initial stimulus encoding (S1) and before saccades were made (S2). A longer gaze duration for the eye region of the monkeys compared to cartoons indicated more robust social engagement with realistic faces. During S1, a similar number of lateral nucleus neurons encoded either reality only, with a monkey-image preference; reward only, with a large-reward preference; or both. Conversely, neurons in the basal and central nuclei primarily encoded reward, preferring large- versus small-reward associated face images. Reward-dependent modulation continued after S1 but was more conspicuous during S1 in the basal nucleus and during both S1 and S2 in the central nucleus. This anatomically and temporally specific encoding in the amygdala may underlie the computation and integration of social and reward information.

Significance Statement Reward and social information are closely related but originally independent, as both influence our decision-making. The amygdala has been associated with both reward and social information coding. However, whether and how they are processed separately or conjointly by individual neurons in the amygdala remains unclear. We found that neurons in the lateral and basal nuclei encoded face reality, an important aspect of social information, and reward, respectively, during sensory processing. Neurons in the central nucleus encoded reward information during the execution phase. These findings provide new insight into mechanisms underlying separate or integrated social and reward information processing within the amygdala.