Snakes elicit specific neural responses in the human infant brain.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
04 05 2020
04 05 2020
Historique:
received:
27
11
2019
accepted:
27
03
2020
entrez:
6
5
2020
pubmed:
6
5
2020
medline:
7
1
2021
Statut:
epublish
Résumé
Detecting predators is essential for survival. Given that snakes are the first of primates' major predators, natural selection may have fostered efficient snake detection mechanisms to allow for optimal defensive behavior. Here, we provide electrophysiological evidence for a brain-anchored evolved predisposition to rapidly detect snakes in humans, which does not depend on previous exposure or knowledge about snakes. To do so, we recorded scalp electrical brain activity in 7- to 10-month-old infants watching sequences of flickering animal pictures. All animals were presented in their natural background. We showed that glancing at snakes generates specific neural responses in the infant brain, that are higher in amplitude than those generated by frogs or caterpillars, especially in the occipital region of the brain. The temporal dynamics of these neural responses support that infants devote increased attention to snakes than to non-snake stimuli. These results therefore demonstrate that a single fixation at snakes is sufficient to generate a prompt and large selective response in the infant brain. They argue for the existence in humans of an inborn, brain-anchored mechanism to swiftly detect snakes based on their characteristic visual features.
Identifiants
pubmed: 32366886
doi: 10.1038/s41598-020-63619-y
pii: 10.1038/s41598-020-63619-y
pmc: PMC7198620
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7443Références
Isbell, L. A. Snakes as agents of evolutionary change in primate brains. J. Hum. Evol. 51, 1–35 (2006).
pubmed: 16545427
doi: 10.1016/j.jhevol.2005.12.012
pmcid: 16545427
Isbell, L. A. The Fruit, the Tree, and the Serpent. (Harvard University Press, 2009).
Öhman, A. & Mineka, S. The malicious serpent: Snakes as a prototypical stimulus for an evolved module of fear. Curr. Dir. Psychol. Sci. 12, 5–9 (2003).
doi: 10.1111/1467-8721.01211
Van Le, Q. et al. Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proc. Natl. Acad. Sci. 110, 19000–19005 (2013).
pubmed: 24167268
doi: 10.1073/pnas.1312531110
pmcid: 24167268
Soares, S. C., Lindström, B., Esteves, F. & Öhman, A. The hidden snake in the grass: Superior detection of snakes in challenging attentional conditions. Plos One 9, e114724 (2014).
pubmed: 25493937
pmcid: 4262429
doi: 10.1371/journal.pone.0114724
Lipp, O. V., Derakshan, N., Waters, A. M. & Logies, S. Snakes and cats in the flower bed: Fast detection is not specific to pictures of fear-relevant animals. Emotion 4, 233–250 (2004).
pubmed: 15456393
doi: 10.1037/1528-3542.4.3.233
pmcid: 15456393
LoBue, V. & Matthews, K. The snake in the grass revisited: An experimental comparison of threat detection paradigms. Cogn. Emot. 28, 22–35 (2014).
pubmed: 23668328
doi: 10.1080/02699931.2013.790783
pmcid: 23668328
LoBue, V., Matthews, K., Harvey, T. & Stark, S. L. What accounts for the rapid detection of threat? Evidence for an advantage in perceptual and behavioral responding from eye movements. Emotion 14, 816–823 (2014).
pubmed: 24749632
doi: 10.1037/a0035869
pmcid: 24749632
Ohman, A., Flykt, A. & Esteves, F. Emotion drives attention: Detecting the snake in the grass. J. Exp. Psychol. Gen. 130, 466–478 (2001).
pubmed: 11561921
doi: 10.1037/0096-3445.130.3.466
pmcid: 11561921
Penkunas, M. J. & Coss, R. G. Rapid detection of visually provocative animals by preschool children and adults. J. Exp. Child Psychol. 114, 522–536 (2013).
pubmed: 23218450
doi: 10.1016/j.jecp.2012.10.001
pmcid: 23218450
Penkunas, M. J. & Coss, R. G. A comparison of rural and urban Indian children’s visual detection of threatening and nonthreatening animals. Dev. Sci. 16, 463–475 (2013).
pubmed: 23587043
doi: 10.1111/desc.12043
pmcid: 23587043
Masataka, N., Hayakawa, S. & Kawai, N. Human young children as well as adults demonstrate ‘superior’ rapid snake detection when typical striking posture is displayed by the snake. Plos One 5, e15122 (2010).
pubmed: 21152050
pmcid: 2994910
doi: 10.1371/journal.pone.0015122
Hayakawa, S., Kawai, N. & Masataka, N. The influence of color on snake detection in visual search in human children. Sci. Rep. 1, 80 (2011).
pubmed: 22355599
pmcid: 3216567
doi: 10.1038/srep00080
Lobue, V. & Deloache, J. S. What’s so special about slithering serpents? Children and adults rapidly detect snakes based on their simple features. Vis. Cogn. 19, 129–143 (2011).
doi: 10.1080/13506285.2010.522216
LoBue, V. & DeLoache, J. S. Detecting the snake in the grass: Attention to fear-relevant stimuli by adults and young children. Psychol. Sci. 19, 284–289 (2008).
pubmed: 18315802
doi: 10.1111/j.1467-9280.2008.02081.x
pmcid: 18315802
Kawai, N. & Koda, H. Japanese monkeys (Macaca fuscata) quickly detect snakes but not spiders: Evolutionary origins of fear-relevant animals. J. Comp. Psychol. 130, 299–303 (2016).
pubmed: 27078076
doi: 10.1037/com0000032
pmcid: 27078076
Masataka, N., Koda, H., Atsumi, T., Satoh, M. & Lipp, O. V. Preferential attentional engagement drives attentional bias to snakes in Japanese macaques (Macaca fuscata) and humans (Homo sapiens). Sci. Rep. 8 (2018).
Shibasaki, M. & Kawai, N. Rapid detection of snakes by Japanese monkeys (Macaca fuscata): An evolutionarily predisposed visual system. J. Comp. Psychol. 123, 131–135 (2009).
pubmed: 19450020
doi: 10.1037/a0015095
pmcid: 19450020
Bertels, J., Bayard, C., Floccia, C. & Destrebecqz, A. Rapid detection of snakes modulates spatial orienting in infancy. Int. J. Behav. Dev. 42, 381–387 (2018).
doi: 10.1177/0165025417693955
DeLoache, J. S. & LoBue, V. The narrow fellow in the grass: Human infants associate snakes and fear. Dev. Sci. 12, 201–207 (2009).
pubmed: 19120429
doi: 10.1111/j.1467-7687.2008.00753.x
pmcid: 19120429
LoBue, V., Buss, K. A., Taber-Thomas, B. C. & Pérez-Edgar, K. Developmental differences in infants’ attention to social and nonsocial threats. Infancy 22, 403–415 (2017).
pubmed: 28936127
doi: 10.1111/infa.12167
pmcid: 28936127
LoBue, V. & DeLoache, J. S. Superior detection of threat-relevant stimuli in infancy: Threat detection in infancy. Dev. Sci. 13, 221–228 (2010).
pubmed: 20121878
doi: 10.1111/j.1467-7687.2009.00872.x
pmcid: 20121878
Rakison, D. H. Do 5-month-old infants possess an evolved detection mechanism for snakes, sharks, and rodents? J. Cogn. Dev. 19, 456–476 (2018).
pubmed: 30774559
pmcid: 6372989
doi: 10.1080/15248372.2018.1488717
Hoehl, S., Hellmer, K., Johansson, M. & Gredebäck, G. Itsy bitsy spider…: Infants react with increased arousal to spiders and snakes. Front. Psychol. 8 (2017).
Erlich, N., Lipp, O. V. & Slaughter, V. Of hissing snakes and angry voices: Human infants are differentially responsive to evolutionary fear-relevant sounds. Dev. Sci. 16, 894–904 (2013).
pubmed: 24118715
pmcid: 24118715
Thrasher, C. & LoBue, V. Do infants find snakes aversive? Infants’ physiological responses to “fear-relevant” stimuli. J. Exp. Child Psychol. 142, 382–390 (2016).
pubmed: 26483161
doi: 10.1016/j.jecp.2015.09.013
pmcid: 26483161
LoBue, V., Bloom Pickard, M., Sherman, K., Axford, C. & DeLoache, J. S. Young children’s interest in live animals. Br. J. Dev. Psychol. 31, 57–69 (2013).
pubmed: 23331106
doi: 10.1111/j.2044-835X.2012.02078.x
pmcid: 23331106
Mineka, S., Keir, R. & Price, V. Fear of snakes in wild- and laboratory-reared rhesus monkeys (Macaca mulatta). Anim. Learn. Behav. 8, 653–663 (1980).
doi: 10.3758/BF03197783
Seligman, M. E. P. Phobias and preparedness. Behav. Ther. 2, 307–320 (1971).
doi: 10.1016/S0005-7894(71)80064-3
LoBue, V. What are we so afraid of? How early attention shapes our most common fears. Child Dev. Perspect. 7, 38–42 (2013).
doi: 10.1111/cdep.12012
LoBue, V., Rakison, D. H. & DeLoache, J. S. Threat perception across the life span: Evidence for multiple converging pathways. Curr. Dir. Psychol. Sci. 19, 375–379 (2010).
doi: 10.1177/0963721410388801
LoBue, V. & Rakison, D. H. What we fear most: A developmental advantage for threat-relevant stimuli. Dev. Rev. 33, 285–303 (2013).
doi: 10.1016/j.dr.2013.07.005
Hoehl, S. & Pauen, S. Do infants associate spiders and snakes with fearful facial expressions? Evol. Hum. Behav. 38, 404–413 (2017).
doi: 10.1016/j.evolhumbehav.2016.12.001
Liu-Shuang, J., Norcia, A. M. & Rossion, B. An objective index of individual face discrimination in the right occipito-temporal cortex by means of fast periodic oddball stimulation. Neuropsychologia 52, 57–72 (2014).
pubmed: 24200921
doi: 10.1016/j.neuropsychologia.2013.10.022
Rossion, B. Understanding individual face discrimination by means of fast periodic visual stimulation. Exp. Brain Res. 232, 1599–1621 (2014).
pubmed: 24728131
doi: 10.1007/s00221-014-3934-9
Regan, D. Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine. (Elsevier, 1989).
Peykarjou, S., Hoehl, S., Pauen, S. & Rossion, B. Rapid categorization of human and ape faces in 9-month-old infants revealed by fast periodic visual stimulation. Sci. Rep. 7 (2017).
de Heering, A. & Rossion, B. Rapid categorization of natural face images in the infant right hemisphere. eLife 4 (2015).
Barry-Anwar, R., Hadley, H., Conte, S., Keil, A. & Scott, L. S. The developmental time course and topographic distribution of individual-level monkey face discrimination in the infant brain. Neuropsychologia 108, 25–31 (2018).
pubmed: 29157998
doi: 10.1016/j.neuropsychologia.2017.11.019
Peykarjou, S., Pauen, S. & Hoehl, S. How do 9-month-old infants categorize human and ape faces? A rapid repetition ERP study: Infants’ categorization of human and ape faces. Psychophysiology 51, 866–878 (2014).
pubmed: 24890394
doi: 10.1111/psyp.12238
pmcid: 24890394
de Haan, M., Johnson, M. H. & Halit, H. Development of face-sensitive event-related potentials during infancy: a review. Int. J. Psychophysiol. 51, 45–58 (2003).
pubmed: 14629922
doi: 10.1016/S0167-8760(03)00152-1
pmcid: 14629922
Jacques, C., Retter, T. L. & Rossion, B. A single glance at natural face images generate larger and qualitatively different category-selective spatio-temporal signatures than other ecologically-relevant categories in the human brain. NeuroImage 137, 21–33 (2016).
pubmed: 27138205
doi: 10.1016/j.neuroimage.2016.04.045
pmcid: 27138205
Soares, S. C., Maior, R. S., Isbell, L. A., Tomaz, C. & Nishijo, H. Fast detector/First responder: Interactions between the superior colliculus-pulvinar pathway and stimuli relevant to primates. Front. Neurosci. 11 (2017).
LoBue, V. Deconstructing the snake: The relative roles of perception, cognition, and emotion on threat detection. Emotion 14, 701–711 (2014).
pubmed: 24708497
doi: 10.1037/a0035898
pmcid: 24708497
Souchet, J. & Aubret, F. Revisiting the fear of snakes in children: the role of aposematic signalling. Sci. Rep. 6 (2016).
Rakison, D. H. & Derringer, J. Do infants possess an evolved spider-detection mechanism? Cognition 107, 381–393 (2008).
pubmed: 17825812
doi: 10.1016/j.cognition.2007.07.022
pmcid: 17825812
Van Strien, J. W. & Isbell, L. A. Snake scales, partial exposure, and the Snake Detection Theory: A human event-related potentials study. Sci. Rep. 7 (2017).
Isbell, L. A. & Etting, S. F. Scales drive detection, attention, and memory of snakes in wild vervet monkeys (Chlorocebus pygerythrus). Primates 58, 121–129 (2017).
pubmed: 27517268
doi: 10.1007/s10329-016-0562-y
pmcid: 27517268
Kawai, N. The fear of snakes: evolutionary and psychobiological perspectives on our innate fear. (2019).
Le, A. T. D., Cole, G. G. & Wilkins, A. J. Assessment of trypophobia and an analysis of its visual precipitation. Q. J. Exp. Psychol. 68, 2304–2322 (2015).
doi: 10.1080/17470218.2015.1013970
Luck, S. J. & Hillyard, S. A. The operation of selective attention at multiple stages of processing: Evidence from human and monkey electrophysiology. in The new cognitive neurosciences 687–700 (M. Gazzaniga, 2000).
Barry-Anwar, R., Hadley, H. & Scott, L. S. Differential neural responses to faces paired with labels versus faces paired with noise at 6- and at 9-months. Vision Res., https://doi.org/10.1016/j.visres.2018.03.002 (2018).
Guy, M. W., Zieber, N. & Richards, J. E. The cortical development of specialized face processing in infancy. Child Dev. 87, 1581–1600 (2016).
pubmed: 27246260
pmcid: 5042801
doi: 10.1111/cdev.12543
Leppänen, J. M., Moulson, M. C., Vogel-Farley, V. K. & Nelson, C. A. An ERP study of emotional face processing in the adult and infant brain. Child Dev. 78, 232–245 (2007).
pubmed: 17328702
pmcid: 2976653
doi: 10.1111/j.1467-8624.2007.00994.x
Buiatti, M. et al. Cortical route for facelike pattern processing in human newborns. Proc. Natl. Acad. Sci. 116, 4625–4630 (2019).
pubmed: 30755519
doi: 10.1073/pnas.1812419116
pmcid: 30755519
Reid, V. M. et al. The Human Fetus Preferentially Engages with Face-like Visual Stimuli. Curr. Biol. 27, 1825–1828.e3 (2017).
pubmed: 28602654
doi: 10.1016/j.cub.2017.05.044
pmcid: 28602654
Pessoa, L. & Adolphs, R. Emotion processing and the amygdala: from a ‘low road’ to ‘many roads’ of evaluating biological significance. Nat. Rev. Neurosci. 11, 773–782 (2010).
pubmed: 20959860
pmcid: 3025529
doi: 10.1038/nrn2920
Hébert, M., Versace, E. & Vallortigara, G. Inexperienced preys know when to flee or to freeze in front of a threat. Proc. Natl. Acad. Sci. 116, 22918–22920 (2019).
pubmed: 31659039
doi: 10.1073/pnas.1915504116
pmcid: 31659039
Nichols, T. E. & Holmes, A. P. Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum. Brain Mapp. 15, 1–25 (2002).
pubmed: 11747097
doi: 10.1002/hbm.1058
pmcid: 11747097
Sassenhagen, J. & Draschkow, D. Cluster-based permutation tests of MEG/EEG data do not establish significance of effect latency or location. Psychophysiology 56, e13335 (2019).
pubmed: 30657176
doi: 10.1111/psyp.13335
pmcid: 30657176
Heinrich, S. P. Some thoughts on the interpretation of steady-state evoked potentials. Doc. Ophthalmol. 120, 205–214 (2010).
pubmed: 20101435
doi: 10.1007/s10633-010-9212-7
pmcid: 20101435
Norcia, A. M., Appelbaum, L. G., Ales, J. M., Cottereau, B. R. & Rossion, B. The steady-state visual evoked potential in vision research: A review. J. Vis. 15, 4 (2015).
pubmed: 26024451
pmcid: 4581566
doi: 10.1167/15.6.4