Abstract

There is growing evidence from both behavioral and neurophysiological approaches that primates are able to rapidly discriminate visually between snakes and innocuous stimuli. Recent behavioral evidence suggests that primates are also able to discriminate the level of threat posed by snakes, by responding more intensely to a snake model poised to strike than to snake models in coiled or sinusoidal postures (Etting and Isbell 2014). In the present study, we examine the potential for an underlying neurological basis for this ability. Previous research indicated that the pulvinar is highly sensitive to snake images. We thus recorded pulvinar neurons in Japanese macaques (Macaca fuscata) while they viewed photos of snakes in striking and non-striking postures in a delayed non-matching to sample (DNMS) task. Of 821 neurons recorded, 78 visually responsive neurons were tested with the all snake images. We found that pulvinar neurons in the medial and dorsolateral pulvinar responded more strongly to snakes in threat displays poised to strike than snakes in non-threat-displaying postures with no significant difference in response latencies. A multidimensional scaling analysis of the 78 visually responsive neurons indicated that threat-displaying and non-threat-displaying snakes were separated into two different clusters in the first epoch of 50 ms after stimulus onset, suggesting bottom-up visual information processing. These results indicate that pulvinar neurons in primates discriminate between poised to strike from those in non-threat-displaying postures. This neuronal ability likely facilitates behavioral discrimination and has clear adaptive value. Our results are thus consistent with the Snake Detection Theory, which posits that snakes were instrumental in the evolution of primate visual systems.

Highlights

  • Threatening stimuli are known to elicit fast and vigorous reactions from most animals, including freezing, darting, rapid retreat, alarm calls, and defensive attacks

  • Children with no experience with snakes visually detected photos of snakes in threat posture faster than those of snakes not poised to strike [29]. These findings suggest that primates are sensitive to variation in the level of threat revealed by snakes in different positions, with elongated or sinusoidal snakes being least threatening, coiled snakes intermediate, and snakes poised to strike most threatening

  • 78 neurons were tested with all stimuli in this experiment. From this 78neuron subset, 45 neurons responded more strongly to snakes in threat display (t-test, P,0.05), 24 neurons responded more strongly to snakes in non-threat-displaying postures (t-test, P,0.05), and 9 neurons showed no difference between these two kinds of the stimuli (t-test, P.0.05)

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Summary

Introduction

Threatening stimuli are known to elicit fast and vigorous reactions from most animals, including freezing, darting, rapid retreat, alarm calls, and defensive attacks. Such responses were likely selected for over evolutionary time because animals that behaved in ways that helped them avoid threatening stimuli would have survived longer than those that did not. Before these reactions occur, the threatening stimuli must be detected, and this can be achieved through one or more of the senses. Primate visual systems are wellsuited for clearly seeing objects in the lower visual field within peripersonal space, where the risk from snakes is usually greatest [4, 5]

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