Neuronal Encoding of Emotional Valence and Intensity in the Monkey Amygdala

Abstract

Neuropsychological and neuroimaging studies have suggested that the primate amygdala plays an essential role in processing the emotional valence and intensity of visual stimuli, which is necessary for determining whether to approach or avoid a stimulus. However, the neuronal mechanisms underlying the evaluation of emotional value remain unknown. In the present study, we trained male macaque monkeys to perform an operant conditioning task in which fractal visual patterns were associated with three different amounts of air puff delivered to the cheek (negative) or liquid reward (positive). After confirming that the monkeys successfully differentiated the emotional valence and intensity of the visual stimuli, we analyzed neuronal responses to the stimuli in the amygdala. Most amygdala neurons conveyed information concerning the emotional valence and/or intensity of the visual stimuli, and the majority of those conveying information about emotional valence responded optimally to negative stimuli. Further, some amygdala neurons conveyed information related to both emotional valence and intensity, whereas a small portion conveyed information related to emotional intensity alone. These results indicate that the primate amygdala encodes both emotional valence and intensity, highlighting its important role in the avoidance of dangerous stimuli and animal survival.SIGNIFICANCE STATEMENT Evaluating the emotional value of visual stimuli is essential for animal survival, especially in primates. Emotional value is estimated from the emotional valence and intensity of stimuli, and evidence indicates that the amygdala is likely to play a major role in processing these types of information. To our knowledge, the current study is the first to examine the responses of neurons in the monkey amygdala to visual stimuli that differ in emotional valence and intensity simultaneously. Our data suggest that the amygdala plays an important role in the evaluation of emotional stimuli and in the decision to escape negative and harmful stimuli.

Keywords: amygdala; emotion; intensity; primates; single-unit recording; valence.