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Fast Detection of Snakes and Emotional Faces in the Macaque Amygdala

楊 梦 富山大学

2022.09.28

概要

〔目的〕
　Rapid defensive responses are often required to avoid predators. Neural systems for such behaviors have been argued to be controlled by an evolved subcortical “fear module” that in mammals includes the superior colliculus and pulvinar, two nuclei involved with vision, and the amygdala. Although the amygdala has been implicated in avoidance and emotional behaviors to biologically relevant stimuli and has neural connections with subcortical nuclei involved with vision, the responsiveness of amygdalar neurons to phylogenetically salient stimuli in primates, especially snakes and emotional faces, is currently unknown. In this study, neuronal activity in the amygdala was recorded from Japanese macaques (Macaca fuscata) during discrimination of eight categories of visual stimuli including snakes, monkey faces, human faces, carnivores, raptors, non-predators, monkey hands, and simple figures.

〔方法並びに成績〕
　Two adult monkeys were trained to perform a delayed non-matching to sample (DNMS) task and discriminate 8 categories of visual stimuli (snakes, monkey faces, human faces, raptors, carnivores, non-predators, monkey hands, and simple figures). While monkeys performed the DNMS task, a glass-insulated tungsten microelectrode was stereotaxically inserted into the amygdala to record neuronal activity. After recording, a tungsten marker was implanted near the target area, and the brains were perfused, removed from the skulls, and cut into 100-µm coronal sections. The sections were stained with Cresyl violet, and the location of each recording site was then determined by comparing the stereotaxic coordinates of recording sites with those of maker positions.
　Of 527 amygdalar neurons, 95 responded to one or more stimuli. Response characteristics of the amygdalar neurons indicated that they were more sensitive to the snakes and emotional faces than other stimuli. Response magnitudes and latencies of amygdalar neurons to snakes and monkey faces were stronger and faster than those to the other categories of stimuli, respectively. Furthermore, response magnitudes to the low pass-filtered snake images were larger than those to scrambled snake images. Finally, analyses of population activity of amygdalar neurons suggest that snakes and emotional faces were represented separately from the other stimuli during the 50–100 ms period from stimulus onset, and neutral faces during the 100–150 ms period.

〔総括〕
　These response characteristics indicate that the amygdala processes fast and coarse visual information from emotional faces and snakes (but not other predators of primates) among the eight categories of the visual stimuli, and suggest that, like anthropoid primate visual systems, the amygdala has been shaped over evolutionary time to detect appearance of potentially threatening stimuli including both emotional faces and snakes, the first of the modern predators of primates. These findings suggest that amygdalar neuronal responsiveness is similar to that in the pulvinar and medial prefrontal cortex in monkeys reported in previous studies. This specific pattern of responsiveness to snakes and emotional faces might be attributed to natural selection favoring rapid detection of snakes as well as emotional faces in primates via the “fear module”, which includes the superior colliculus, pulvinar, and amygdala.

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