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

Quan Van Le, Lynne A. Isbell, Jumpei Matsumoto, Minh Nguyen, Etsuro Hori, Rafael S. Maior, Carlos Tomaz, Anh Hai Tran, Taketoshi Ono, and Hisao Nishijo
PNAS first published October 28, 2013 https://doi.org/10.1073/pnas.1312648110

  1. Edited by David M. Hillis, University of Texas at Austin, Austin, TX, and approved October 1, 2013 (received for review July 4, 2013)

Significance

The present study shows preferential activity of neurons in the medial and dorsolateral pulvinar to images of snakes. Pulvinar neurons responded faster and stronger to snake stimuli than to monkey faces, monkey hands, and geometric shapes, and were sensitive to unmodified and low-pass filtered images but not to high-pass filtered images. These results identify a neurobiological substrate for rapid detection of threatening visual stimuli in primates. Our findings are unique in providing neuroscientific evidence in support of the Snake Detection Theory, which posits that the threat of snakes strongly influenced the evolution of the primate brain. This finding may have great impact on our understanding of the evolution of primates.

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.

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: laisbell{at}ucdavis.edu (for evolutionary/anthropological queries) and nishijo{at}med.u-toyama.ac.jp (for neurobiological queries).

  • Author contributions: L.A.I., C.T., and H.N. designed research; Q.V.L., J.M., M.N., E.H., and H.N. performed research; J.M., M.N., E.H., and A.H.T. contributed new reagents/analytic tools; Q.V.L., L.A.I., J.M., M.N., R.S.M., A.H.T., T.O., and H.N. analyzed data; and Q.V.L., L.A.I., R.S.M., C.T., T.O., and H.N. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1312648110/-/DCSupplemental.

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Responses to snakes in the primate pulvinar
Quan Van Le, Lynne A. Isbell, Jumpei Matsumoto, Minh Nguyen, Etsuro Hori, Rafael S. Maior, Carlos Tomaz, Anh Hai Tran, Taketoshi Ono, Hisao Nishijo
Proceedings of the National Academy of Sciences Oct 2013, 201312648; DOI: 10.1073/pnas.1312648110
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Proceedings of the National Academy of Sciences: 116 (16)
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