No abstract

The amygdala is a small subcortical structure located bilaterally in medial temporal lobes. It is a key region for emotional processes and some forms of associative learning. In particular, the role of the amygdala in processing of negative emotions and aversive learning has been shown in numerous studies. However, involvement of this structure in processing of positive affect and appetitive learning is not fully understood. Previous experiments in animals are not consistent. While some authors implicate only the centromedial part of the amygdala in appetitive learning, the others suggest contribution of both centromedial and basolateral subregions. Although from the evolutionary perspective appetitive learning is equally important as aversive learning, research on the role of the human amygdala and its subregions in appetitive learning is undertaken relatively rarely and the results are not conclusive. Therefore, the aim of this review is twofold: to summarize the current knowledge in this field and to indicate and discuss the factors, which might affect the observed level of the amygdala activity during appetitive learning in humans.

Prediction error (PE) is the mismatch between a prior expectation and reality, and it lies at the core of associative learning about aversive and appetitive stimuli. Human studies on fear learning have linked the amygdala to aversive PEs. In contrast, the relationship between the amygdala and PE in appetitive settings and stimuli unlike those that induce fear has received less research attention. Animal studies show that the amygdala is a functionally heterogeneous structure. Nevertheless, the role of the amygdala's nuclei in PE signaling remains unknown in humans. To clarify the role of two subdivisions of the human amygdala, the centromedial (CMA) and basolateral (BLA), in appetitive and aversive PE signaling, we employed gustatory Pavlovian learning involving eating-related naturalistic outcomes. Thirty-eight right-handed individuals (19 females) participated in the study. We found that surprise with neutral feedback when a reward is expected triggers activity within the left and right CMA. When an aversive outcome is expected, surprise with neutral feedback triggers activity only within the left CMA. Notably, the BLA was not activated by those conditions. Thus, the CMA engages in negative PE signaling during appetitive and aversive gustatory Pavlovian learning, while the BLA is not critical for this process. In addition, PE-related activity within the left CMA during aversive learning is negatively correlated with neuroticism and positively correlated with extraversion. The findings indicate the importance of the CMA in gustatory learning when the value of outcomes changes and have implications for understanding psychological conditions that manifest perturbed processing of negative PEs.SIGNIFICANCE STATEMENT:A discrepancy between a prediction and an actual outcome (prediction error, PE) plays a crucial role in learning. Learning improves when an outcome is more significant than expected (positive PE) and worsens when it is smaller than expected (negative PE). We found that the negative PE during appetitive and aversive taste learning is associated with increased activity of the centromedial amygdala (CMA), which suggests that the CMA controls taste learning. Our findings may have implications for understanding psychological states associated with deficient learning from negative PEs, such as obesity and addictive behaviors.