Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Abstract

Snakes and their relationships with humans and other primates have attracted broad attention from multiple fields of study, but not, surprisingly, from neuroscience, despite the involvement of the visual system and strong behavioral and physiological evidence that humans and other primates can detect snakes faster than innocuous objects. Here, we report the existence of neurons in the primate medial and dorsolateral pulvinar that respond selectively to visual images of snakes. Compared with three other categories of stimuli (monkey faces, monkey hands, and geometrical shapes), snakes elicited the strongest, fastest responses, and the responses were not reduced by low spatial filtering. These findings integrate neuroscience with evolutionary biology, anthropology, psychology, herpetology, and primatology by identifying a neurobiological basis for primates' heightened visual sensitivity to snakes, and adding a crucial component to the growing evolutionary perspective that snakes have long shaped our primate lineage.evolution | Snake Detection Theory | visual responses | low-pass filtered images S nakes have long been of interest to us above and beyond the attention we give to other wild animals. The attributes of snakes and our relationships with them have been topics of discussion in fields as disparate as religion, philosophy, anthropology, psychology, primatology, and herpetology (1, 2). Ochre and eggshells dated to as early as 75,000 y ago and found with cross-hatched and ladder-shaped lines (3, 4) resemble the dorsal and ventral scale patterns of snakes. As the only natural objects with those characteristics, snakes may have been among the first models used in representational imagery created by modern humans. Our interest in snakes may have originated much further back in time; our primate lineage has had a long and complex evolutionary history with snakes as competitors, predators, and prey (1). The position of primates as prey of snakes has, in fact, been argued to have constituted strong selection favoring the evolution of the ability to detect snakes quickly as a means of avoiding them, beginning with the earliest primates (2, 5). Across primate species, ages, and (human) cultures, snakes are indeed detected visually more quickly than innocuous stimuli, even in cluttered scenes (6-11). Physiological responses reveal that humans are also able to detect snakes visually even before becoming consciously aware of them (12). Although the visual system must be involved in the preferential ability to detect snakes rapidly and preconsciously or automatically, the neurological basis for this ability has not yet been elucidated, perhaps because an evolutionary perspective is rarely incorporated in neuroscientific studies. Our study helps to fill this interdisciplinary gap by investigating the responses of neurons to snakes and other natural stimuli that may have acted as selective pressures on primates in the past.Here, we identify a mechanism for the visual system's involvement in rapid snake detection by measurin...

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