Japanese monkeys (Macaca fuscata) quickly detect snakes but not spiders: Evolutionary origins of fear-relevant animals.

Abstract

Humans quickly detect the presence of evolutionary threats through visual perception. Many theorists have considered humans to be predisposed to respond to both snakes and spiders as evolutionarily fear-relevant stimuli. Evidence supports that human adults, children, and snake-naive monkeys all detect pictures of snakes among pictures of flowers more quickly than vice versa, but recent neurophysiological and behavioral studies suggest that spiders may, in fact, be processed similarly to nonthreat animals. The evidence of quick detection and rapid fear learning by primates is limited to snakes, and no such evidence exists for spiders, suggesting qualitative differences between fear of snakes and fear of spiders. Here, we show that snake-naive Japanese monkeys detect a single snake picture among 8 nonthreat animal pictures (koala) more quickly than vice versa; however, no such difference in detection was observed between spiders and pleasant animals. These robust differences between snakes and spiders are the most convincing evidence that the primate visual system is predisposed to pay attention to snakes but not spiders. These findings suggest that attentional bias toward snakes has an evolutionary basis but that bias toward spiders is more due to top-down, conceptually driven effects of emotion on attention capture. (PsycINFO Database Record

Breaking Snake Camouflage: Humans Detect Snakes More Accurately than Other Animals under Less Discernible Visual Conditions

“…Studies with visual search tasks have revealed a larger threat-detection advantage for snakes than for spiders [5, 18]. Our study with three Japanese monkeys show that the monkeys detect a single snake picture among eight non-threat animal pictures (koala) more quickly than vice versa, however no such difference in detection was observed for spiders and non-threat animals [11]. Electroencephalogram studies using early posterior negativity (EPN), which reflects the early selective visual processing of emotionally significant information, also suggest that the degree of EPN for spider pictures was smaller than that for snake pictures and not different from other non-fear-relevant animals [12].…”

“…Although many studies with human adults [4, 5], children [6, 8, 9], and macaque monkeys [10, 11] from our laboratory and others support the Snake Detection Theory by demonstrating that humans and primates have an attentional bias toward snakes, there are still criticisms that quick detection of snakes in the visual search tasks is ambiguous, specifically, that it may be explained by speeded detection of threat targets (engagement), by slowed disengagement from threat distractors, or both [25]. More importantly, using visual search often generates the possibility of low-level perceptual confounds [26].…”

“…Evidence for an evolutionary specialized attention to snakes comes from our studies with macaque monkeys [10, 11]. Kawai and Koda [11] compared reaction times for snake-naïve macaque monkeys ( Macaca fuscata ) to detect deviant pictures of snakes and spiders in the background of non-threatening animal pictures (koala) and found that quicker detection occurred for snake pictures but not for spider pictures.…”

“…Kawai and Koda [11] compared reaction times for snake-naïve macaque monkeys ( Macaca fuscata ) to detect deviant pictures of snakes and spiders in the background of non-threatening animal pictures (koala) and found that quicker detection occurred for snake pictures but not for spider pictures. Despite the fact that monkeys in these studies [10, 11] were reared in captivity and assumed not to have been exposed to real or toy snakes, they reacted to snake pictures quickly. These results with visual search tasks suggest that evolution equipped our primate ancestors with a visual system predisposed to respond to snakes [1, 2, 7, 10, 11, 12, 13], as Darwin pointed out [14].…”

Defensive Vocalizations and Motor Asymmetry Triggered by Disinhibition of the Periaqueductal Gray in Non-human Primates

“…These defensive reactions are manifest in species-typical ways; for example, rodents display freezing both to looming stimuli and to unconditioned fear-evoking stimuli, such as fox odor (Cattarelli and Chanel, 1979; Wallace and Rosen, 2000; Yilmaz and Meister, 2013; Shang et al, 2015; De Franceschi et al, 2016). By contrast, primates display alarm calls, avoidance and escape behaviors toward unconditioned fear-provoking stimuli, such as snakes (Izquierdo and Murray, 2004; Shibasaki et al, 2014; Weiss et al, 2015; Kawai and Koda, 2016). In humans, midbrain regions (encompassing the periaquaductal gray and the deep/intermediate layers of the superior colliculus) parametricaly encoded proximity of threating stimuli (Mobbs et al, 2010) and looming threats (Coker-Appiah et al, 2013).…”