Abstract

Appropriate processing of others’ facial emotions is a fundamental ability of primates in social situations. Several moods and anxiety disorders such as depression cause a negative bias in the perception of facial emotions. Depressive patients show abnormalities of activity and gray matter volume in the perigenual portion of the anterior cingulate cortex (ACC) and an increase of activation in the amygdala. However, it is not known whether neurons in the ACC have a function in the processing of facial emotions. Furthermore, detecting predators quickly and taking avoidance behavior are important functions in a matter of life and death for wild monkeys. the existence of predators in their vicinity is life-and-death information for monkeys. In the present study, we recorded the activity of single neurons from the monkey ACC and examined the responsiveness of the ACC neurons to various visual stimuli including monkey faces, snakes, foods, and artificial objects. About one-fourth of the recorded neurons showed a significant change in activity in response to the stimuli. The ACC neurons exhibited high selectivity to certain stimuli, and more neurons exhibited the maximal response to monkey faces and snakes than to foods and objects. The responses to monkey faces and snakes were faster and stronger compared to those to foods and objects. Almost all of the neurons that responded to video stimuli responded strongly to negative facial stimuli, threats, and scream. Most of the responsive neurons were located in the cingulate gyrus or the ventral bank of the cingulate sulcus just above or anterior to the genu of the corpus callosum, that is, the perigenual portion of the ACC, which has a strong mutual connection with the amygdala. These results suggest that the perigenual portion of the ACC in addition to the amygdala processes emotional information, especially negative life-and-death information such as conspecifics’ faces and snakes.

Highlights

  • The limbic system including the amygdala, cingulate cortex, and pulvinar in collaboration with the frontal cortex has been implicated in the regulation of emotional behavior (Cardinal et al, 2002; Etkin et al, 2011)

  • These findings suggest that the anterior cingulate cortex (ACC) functions in the processing of facial information, and that malfunction leads to the negative bias of the emotion of others in depressive patients

  • We examined the neuronal responsiveness to complex visual stimuli in the anterior cingulate cortex (ACC) of macaque monkeys

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Summary

INTRODUCTION

The limbic system including the amygdala, cingulate cortex, and pulvinar in collaboration with the frontal cortex has been implicated in the regulation of emotional behavior (Cardinal et al, 2002; Etkin et al, 2011). Several neuroimaging studies have reported that perception of negative facial expressions modulates the neuronal activity in the ACC (Blair et al, 1999) and amygdala (Blair et al, 1999) in humans. The modulation of ACC activity by negative facial expressions was more prominent in depressive patients (Gotlib et al, 2005; Chen et al, 2006). To understand the function of the ACC in the regulation of emotional behavior, we recorded the neuronal activity from the perigenual ACC (area 24) and examined their response to various visual stimuli including conspecifics’ faces and snakes

MATERIALS AND METHODS
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