Fast Detection of Snakes and Emotional Faces in the Macaque Amygdala.

Primate vision is reported to detect snakes and emotional faces faster than many other tested stimuli. Because the amygdala has been implicated in avoidance and emotional behaviors to biologically relevant stimuli and has neural connections with subcortical nuclei involved with vision, amygdalar neurons would be sensitive to snakes and emotional faces. 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. 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. 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.

Preferential Neuronal Responses to Snakes in the Monkey Medial Prefrontal Cortex Support an Evolutionary Origin for Ophidiophobia.

Ophidiophobia (snake phobia) is one of the most common specific phobias. It has been proposed that specific phobia may have an evolutionary origin, and that attentional bias to specific items may promote the onset of phobia. Noninvasive imaging studies of patients with specific phobia reported that the medial prefrontal cortex (mPFC), especially the rostral part of the anterior cingulate cortex (rACC), and amygdala are activated during the presentation of phobogenic stimuli. We propose that the mPFC-amygdala circuit may be involved in the pathogenesis of phobia. The mPFC receives inputs from the phylogenically old subcortical visual pathway including the superior colliculus, pulvinar, and amygdala, while mPFC neurons are highly sensitive to snakes that are the first modern predator of primates, and discriminate snakes with striking postures from those with non-striking postures. Furthermore, the mPFC has been implicated in the attentional allocation and promotes amygdala-dependent aversive conditioning. These findings suggest that the rACC focuses attention on snakes, and promotes aversive conditioning to snakes, which may lead to anxiety and ophidiophobia.

Superior Neuronal Detection of Snakes and Conspecific Faces in the Macaque Medial Prefrontal Cortex.

Snakes and conspecific faces are quickly and efficiently detected in primates. Because the medial prefrontal cortex (mPFC) has been implicated in attentional allocation to biologically relevant stimuli, we hypothesized that it might also be highly responsive to snakes and conspecific faces. In this study, neuronal responses in the monkey mPFC were recorded, while monkeys discriminated 8 categories of visual stimuli. Here, we show that the monkey mPFC neuronal responses to snakes and conspecific faces were unique. First, the ratios of the neurons that responded strongly to snakes and monkey faces were greater than those of the neurons that responded strongly to the other stimuli. Second, mPFC neurons responded stronger and faster to snakes and monkey faces than the other categories of stimuli. Third, neuronal responses to snakes were unaffected by low-pass filtering of the images. Finally, activity patterns of responsive mPFC neurons discriminated snakes from the other stimuli in the second 50 ms period and monkey faces in the third period after stimulus onset. These response features indicate that the mPFC processes fast and coarse visual information of snakes and monkey faces, and support the hypothesis that snakes and social environments have shaped the primate visual system over evolutionary time.