Abstract
In this chapter, I examined the possibility that quick detection of snakes is achieved not only by subcortical visual pathway but also by cortical processing such as V2 and V4. A larger EPN for snake pictures, which is considered to occur from visual cortical areas, emerges around 200 ms after the onset of the stimulus. It is thought to result from automatic selective visual attention to emotional stimuli, which may evoke priority processing because of their intrinsic affective significance, with the amygdala modulating activity in the visual cortex. Humans can identify one face among possible six faces, even if the stimuli were followed by a masking stimulus only 20–30 ms after the stimulus onset. Our recent study showed that macaques could select one target image among eight distractors, even when these images were followed by masking patterns after 50 ms. These suggest that visual information is processed by cortical areas as fast as subcortical areas at least for a single image. Early visual areas such as V2 and V4 play important role to discriminate textures. Snake skin (scale) constitutes a uniform texture. If snake scale is a critical feature to detect snakes for primates and humans, V2 and V4 may contribute to detect snakes quickly, which activations may be reflected as a larger EPN. I conclude this chapter with future directions for the better understanding of fear of snakes.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Almeida I, Soares SC, Castelo-Branco M (2015) The distinct role of the amygdala, superior colliculus and pulvinar in processing of central and peripheral snakes. PLoS One 10:e0129949. https://doi.org/10.1371/journal.pone.0129949
Anzai A, Peng X, Van Essen DC (2007) Neurons in monkey visual area V2 encode combinations of orientations. Nat Neurosci 10:1313–1321. https://doi.org/10.1038/nn1975
Aronoff J, Woike BA, Hyman LM (1992) Which are the stimuli in facial displays of anger and happiness? Configural bases of emotion recognition. J Pers Soc Psychol 62:1050–1066. https://doi.org/10.1037/0022-3514.62.6.1050
Benevento LA, Port D (1995) Single neurons with both form/color differential responses and saccade-related response in the non-retinotopic pulvinar of the behaving macaque monkey. Vis Neurosci 12:523–544. https://doi.org/10.1017/S0952523800008439
Boehnke SE, Munoz DP (2008) On the importance of the transient visual response in the superior colliculus. Curr Opin Neurobiol 18:544–551. https://doi.org/10.1016/j.conb.2008.11.004
Burghardt GM, Kawai N, Shibasaki M, Mori A, Masataka N (2011) Revisionary findings on primates and the fear of snakes. Paper presented at the international ethological conference/animal behavior society, Bloomington, IN
Capalbo M, Postma E, Goebel R (2008) Combining structural connectivity and response latencies to model the structure of the visual system. PLoS Comput Biol 4:e1000159. https://doi.org/10.1371/journal.pcbi.1000159
Casanova C, Savard T (1996) Motion sensitivity and stimulus interactions in the striate-recipient zone of the cat’s lateral posterior-pulvinar complex. Prog Brain Res 112:277–287. https://doi.org/10.1016/S0079-6123(08)63335-X
De Weerd P, Desimone R, Ungerleider LG (1996) Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques. Vis Neurosci 13:529–538. https://doi.org/10.1017/S0952523800008208
DeYoe EA, Van Essen DC (1985) Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317:58–61. https://doi.org/10.1038/317058a0
Dobkins KR (2000) Moving colors in the lime light. Neuron 25:15–18. https://doi.org/10.1016/S0896-6273(00)80867-3
El-Shamayleh Y, Movshon JA (2011) Neuronal responses to texture-defined form in macaque visual area V2. J Neurosci 31:8543–8555. https://doi.org/10.1523/JNEUROSCI.5974-10.2011
Flykt A, Caldara R (2006) Tracking fear in snake and spider fearful participants during visual search: a multi-response domain study. Cogn Emot 20:1075–1091. https://doi.org/10.1080/02699930500381405
Goodale MA, Westwood DA (2004) An evolving view of duplex vision: separate but interacting cortical pathways for perception and action. Curr Opin Neurobiol 14:203–211. https://doi.org/10.1016/j.conb.2004.03.002
Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG (2007) Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97:1671–1683. https://doi.org/10.1152/jn.00714.2006
Grassini S, Holm SK, Railo H, Koivisto M (2016) Who is afraid of the invisible snake? Subjective visual awareness modulates posterior brain activity for evolutionarily threatening stimuli. Biol Psychol 121:53–61. https://doi.org/10.1016/j.biopsycho.2016.10.007
Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, Egan MF, Weinberger DR (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403. https://doi.org/10.1126/science.1071829
Hariri AR, Drabant EM, Munox KE, Kolachana BS, Mattay VS, Egan MF, Weinberger DR (2005) A susceptibility gene for affective disorders and the response of the human amygdala. Arch Gen Psychiatry 62:146–152. https://doi.org/10.1001/archpsyc.62.2.146
Headland TH, Greene HW (2011) Hunter-gatherers and other primates as prey, predators, and competitors of snakes. Proc Natl Acad Sci 108:E1470–E1474. https://doi.org/10.1073/pnas.1115116108
Hegdé J, Van Essen DC (2000) Selectivity for complex shapes in primate visual area V2. J Neurosci 20:RC61. http://www.jneurosci.org/content/20/5/RC61
Hegdé J, Van Essen DC (2003) Strategies of shape representation in macaque visual area V2. Vis Neurosci 20:313–328. https://doi.org/10.1017/S0952523803203102
Hegdé J, Van Essen DC (2007) A comparative study of shape representation in macaque visual areas v2 and v4. Cereb Cortex 17:1100–1116. https://doi.org/10.1093/cercor/bhl020
Hendry SHC, Reid RC (2000) The koniocellular pathway in primate vision. Annu Rev Neurosci 23:127–153. https://doi.org/10.1146/annurev.neuro.23.1.127
Herrmann MJ, Huter T, Muller F, Muhlberger A, Pauli P, Reif A, Renner T, Canli T, Fallqatter AJ, Lesch KP (2006) Additive effects of serotonin transporter and tryptophan hydroxylase-2 gene variation on emotional processing. Cereb Cortex 17:1160–1163. https://doi.org/10.1093/cercor/bhl026
Hubel DH, Livingstone MS (1987) Segregation of form, color, and stereopsis in primate area 18. J Neurosci 7:3378–3415
Inoue-Murayama M, Weiss A, Morimura N, Tanaka M, Yamagiwa J, Idani G (2011) Molecular behavioral research in great apes. In: Inoue-Murayama M, Kawamura S, Weiss A (eds) From genes to animal behavior: social structures, personalities, communication by color. Springer, Tokyo, pp 239–253
Isbell LA (2006) Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1–35. https://doi.org/10.1016/j.jhevol.2005.12.012
Isbell LA (2009) The fruit, the tree, and the serpent. Why we see so well. Harvard University Press, Cambridge, MA
Ito M, Komatsu H (2004) Representation of angles embedded within contour stimuli in area V2 of macaque monkeys. J Neurosci 24:3313–3324. https://doi.org/10.1523/JNEUROSCI.4364-03.2004
Junghöfer M, Schupp HT, Stark R, Vaitl D (2005) Neuroimaging of emotion: empirical effects of proportional global signal scaling in fMRI data analysis. NeuroImage 25:520–526. https://doi.org/10.1016/j.neuroimage.2004.12.011
Junghöfer M, Sabatinelli D, Bradley MM, Schupp HT, Elbert TR, Lang PJ (2006) Fleeting images: rapid affect discrimination in the visual cortex. NeuroReport 17:225–229. https://doi.org/10.1097/01.wnr.0000198437.59883.bb
Kaas JH (2004) Early visual areas: V1, V2, V3, DM, DL, and MT. In: Kaas JH, Collins CE (eds) The primate visual system. CRC Press, Boca Raton, pp 136–160
Kaas JH, Huer MF (1988) The subcortical visual system of primates. In: Steklis HD, Erwin JA (eds) Comparative primate biology, vol 4. Neurosciences. Alan R. Liss, New York, pp 327–391
Kastner S, De Weerd P, Ungerleider LG (2000) Texture segregation in the human visual cortex: a functional MRI study. J Neurophysiol 83:2453–2457. https://doi.org/10.1152/jn.2000.83.4.2453
Kastner S, O’Connor DH, Fukui MM, Fehd HM, Herwig U, Pinsk MA (2004) Functional imaging of the human lateral geniculate nucleus and pulvinar. J Neurophysiol 91:438–448. https://doi.org/10.1152/jn.00553.2003
Kasturiratne A, Wickremasinghe AR, de Silva N, Gunawardena NK, Pathmeswaran A, Premaratna R, Savioli L, Lalloo DG, de Silva HJ (2008) The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Med 5:e218. https://doi.org/10.1371/journal.pmed.0050218
Kawai N, Koda H (2016) Japanese monkeys (Macaca fuscata) quickly detect snakes but not spiders: evolutionary origins of fear-relevant animals. J Comp Psychol 130:299–303. https://doi.org/10.1037/com0000032
Kawai N, Koda H (submitted) Rapid cortical processing by macaque monkeys with backward masking.
Klorman R, Weerts TC, Hastings JE, Melamed BG, Lang PJ (1974) Psychometric description of some specific-fear questionnaires. Behav Ther 5:401–409. https://doi.org/10.1016/S0005-7894(74)80008-0
Kobatake E, Tanaka K (1994) Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J Neurophysiol 71:856–867. https://doi.org/10.1152/jn.1994.71.3.856
Kovács G, Vogels R, Orban GA (1995) Cortical correlate of pattern backward masking. Proc Natl Acad Sci U S A 92:5587–5591. https://doi.org/10.1073/pnas.92.12.5587
Koyama T, Fujii H, Yonekawa F (1981) Comparative studies of gregariousness and social structure among seven feral Macaca fuscata groups. In: Chiarelli AB, Corruccine RS (eds) Primate behavior and sociobiology. Springer, Berlin, pp 52–63
Kravitz DJ, Saleem KS, Baker CI, Ungerleider LG, Mishukin M (2013) The ventral visual pathway: an expanded neural frame work for the processing of object quality. Trends Cogn Sci 17:26–49. https://doi.org/10.1016/j.tics.2012.10.011
Lamme VA, Roelfsema PR (2000) The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci 23:571–579. https://doi.org/10.1016/S0166-2236(00)01657-X
Lang PJ, Bradley MM, Cuthbert BN (1999) International affective picture system (IAPS): instruction manual and affective ratings, Technical Report A-4. The Center for Research in Psychophysiology, University of Florida, Gainesville
Larson CL, Aronoff J, Stearns J (2007) The shape of threat: simple geometric forms evoke rapid and sustained capture of attention. Emotion 7:526–534. https://doi.org/10.1037/1528-3542.7.3.526
Larson CL, Aronoff J, Sarinopoulos IC, Zhu DC (2009) Recognizing threat: a simple geometric shape activates neural circuitry for threat detection. J Cogn Neurosci 21:1523–1535. https://doi.org/10.1162/jocn.2009.21111
Larsson J, Landy MS, Heeger DJ (2006) Orientation-selective adaptation to first- and second-order patterns in human visual cortex. J Neurophysiol 95:862–881. https://doi.org/10.1152/jn.00668.2005
LeDoux JE (1996) The emotional brain: the mysterious underpinnings emotional life. Simon and Schuster, New York
Leonard CM, Rolls ET, Wilson FA, Baylis GC (1985) Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 15:159–176. https://doi.org/10.1016/0166-4328(85)90062-2
Lesch K-P, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J, Muller CR, Hamer DH, Murphy DL (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274:1527–1531. https://doi.org/10.1126/science.274.5292.1527
Liddell BJ, Brown KJ, Kemp AH, Barton MJ, Das P, Peduto A, Gordem E, Williams LM (2005) A direct brainstem-amygdala-cortical “alarm” system for subliminal signals of fear. NeuroImage 24:235–243. https://doi.org/10.1016/j.neuroimage.2004.08.016
Lipp OV, Waters AM (2007) When danger lurks in the background: attentional capture by animal fear-relevant distractors is specific and selectively enhanced by animal fear. Emotion 7:192–200. https://doi.org/10.1037/1528-3542.7.1.192
LoBue V, DeLoache JS (2011) What’s so special about slithering serpents? Children and adults rapidly detect snakes based on their simple features. Vis Cogn 19:129–143. https://doi.org/10.1080/13506285.2010.522216
LoBue V, Larson CL (2010) What makes angry faces look so…angry? Examining visual attention to the shape of threat in children and adults. Vis Cogn 18:1165–1178. https://doi.org/10.1080/13506281003783675
Lonsdorf TB, Weike AI, Nikamo P, Schalling M, Hamm AO, Öhman A (2009) Genetic gating of human fear learning and extinction: possible implications for gene-environment interaction in anxiety disorder. Psychol Sci 20:198–206. https://doi.org/10.1111/j.1467-9280.2009.02280.x
Macknik SL, Livingstone MS (1998) Neuronal correlates of visibility and invisibility in the primate visual system. Nat Neurosci 1:144–149. https://doi.org/10.1038/393
Marešová J, Landová E, Frynta D (2009) What makes some species of milk snakes more attractive to humans than others? Theor Biosci 128:227–235. https://doi.org/10.1007/s12064-009-0075-y
Maunsell JHR, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363–401. https://doi.org/10.1146/annurev.ne.10.030187.002051
Merigan WH (2000) Cortical area V4 is critical for certain texture discriminations, but this effect is not dependent on attention. Vis Neurosci 17:949–958. https://doi.org/10.1017/S095252380017614X
Merigan WH, Nealey TA, Maunsell JH (1993) Visual effects of lesions of cortical area V2 in macaques. J Neurosci 13:3180–3191. http://www.jneurosci.org/content/13/7/3180
Morris JS, Öhman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci U S A 96:1680–1685. https://doi.org/10.1073/pnas.96.4.1680
Nassi JJ, Callaway EM (2009) Parallel processing strategies of the primate visual system. Nat Rev Neurosci 10:360–372. https://doi.org/10.1038/nrn2619
Öhman A, Mineka S (2001) Fears, phobias, and preparedness: toward and evolved module of fear and fear learning. Psychol Rev 108:483–522. https://doi.org/10.1037//0033-295X.108.3.483
Öhman A, Flykt A, Esteves F (2001) Emotion drives attention: detecting the snake in the grass. J Exp Psychol Gen 130:466–478. https://doi.org/10.1037//0096-3445.130.3.466
Ono T, Nishijo H (1992) Neurophysiological basis of the Klüver-Bucy syndrome: responses of monkey amygdaloid neurons to biologically significant objects. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, pp 167–190
Ouellette BG, Casanova C (2006) Overlapping visual response latency distributions in visual cortices and LP-pulvinar complex of the cat. Exp Brain Res 175:332–341. https://doi.org/10.1007/s00221-006-0555-y
Oya H, Kawasaki H, Howard MA, Adolphs R (2002) Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 22:9502–9512. http://www.jneurosci.org/content/22/21/9502
Pessoa L, Adolphs R (2010) Emotion processing and the amygdala: from a ‘low road’ to ‘many roads’ of evaluating biological significance. Nat Rev Neurosci 11:773–783. https://doi.org/10.1038/nrn2920
Peterhans E (1997) Functional organization of area V2 in the awake monkey. In: Rockland KS, Kaas JH, Peters A (eds) Extrastriate cortex in primates. Cerebral cortex, vol 12. Springer, Boston, pp 335–357. https://doi.org/10.1007/978-1-4757-9625-4_8
Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, Egan MF, Mattay VS, Hariri AR, Weinberger DR (2005) 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8:828–834. https://doi.org/10.1038/nn1463
Rinck M, Becker ES (2006) Spider fearful individuals attend to threat, then quickly avoid it: evidence from eye movements. J Abnorm Psychol 115:231–238. https://doi.org/10.1037/0021-843X.115.2.231
Rinck M, Reinecke A, Ellwart T, Heuer K, Becker ES (2005) Speeded detection and increased distraction in fear of spiders: evidence from eye movements. J Abnorm Psychol 114:235–248. https://doi.org/10.1037/0021-843X.114.2.235
Rolls ET, Tovee MJ (1994) Processing speed in the cerebral cortex and the neurophysiology of visual masking. Proc R Soc B Biol Sci 257:9–15. https://doi.org/10.1098/rspb.1994.0087
Rolls ET, Tovée MJ, Panzeri S (1999) The neurophysiology of backward visual masking: information analysis. J Cogn Neurosci 11:300–311. https://doi.org/10.1162/089892999563409
Rousselet GA, Thorpe SJ, Fabre-Thorpe M (2004) How parallel is visual processing in the ventral pathway? Trends Cogn Sci 8:363–370. https://doi.org/10.1016/j.tics.2004.06.003
Schupp HT, Junghöfer M, Weike AI, Hamm AO (2003) Emotional facilitation of sensory processing in the visual cortex. Psychol Sci 14:7–13. https://doi.org/10.1111/1467-9280.01411
Shi C, Davis M (2001) Visual pathways involved in fear conditioning measured with fear-potentiated startle: behavioral and anatomic studies. J Neurosci 21:9844–9855. http://www.jneurosci.org/content/21/24/9844.short
Shibasaki M, Kawai N (2009) Rapid detection of snakes by Japanese monkeys (Macaca fuscata): an evolutionarily predisposed visual system. J Comp Psychol 123:131–135. https://doi.org/10.1037/a0015095
Sincich LC, Horton JG (2002) Divided by cytochrome oxidase: a map of the projections from V1 to V2 in macaques. Science 295:1734–1737. https://doi.org/10.1126/science.1067902
Soares SC, Esteves F, Flykt A (2009) Fear, but non fear-relevance, modulates reaction times in visual search with animal distracters. J Anxiety Disord 23:136–144. https://doi.org/10.1016/j.janxdis.2008.05.002
Soares SC, Lindström B, Esteves F, Öhman A (2014) The hidden snake in the grass: superior detection of snakes in challenging attentional conditions. PLoS One 9:e114724. https://doi.org/10.1371/journal.pone.0114724
Tamietto M, de Gelder B (2010) Neural bases of the non-conscious perception of emotional signals. Nat Rev Neurosci 11:697–709. https://doi.org/10.1038/nrn2889
Tamietto M, Pullens P, de Gelder B, Weiskrantz L, Goebel R (2012) Subcortical connections to human amygdala and their changes following destruction of the visual cortex. Curr Biol 22:1449–1455. https://doi.org/10.1016/j.cub.2012.06.006
Tanaka K, Saito H, Fukada Y, Moriya M (1991) Coding visual images of objects in the inferotemporal cortex of the macaque monkey. J Neurophysiol 66:170–189. https://doi.org/10.1152/jn.1991.66.1.170
Thompson KG, Schall JD (1999) The detection of visual signals by macaque frontal eye field during masking. Nat Neurosci 2:283–288. https://doi.org/10.1038/6398
Van Le Q, Isbell LA, Matsumoto J, Nguyen M, Hori E, Maior RS, Tomaz C, Tran AH, Ono T, Nishijo H (2013) Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proc Natl Acad Sci U S A 110:19000–19005. https://doi.org/10.1073/pnas.1312648110
Villeneuve MY, Kupers R, Gjedde A, Ptito M, Casanova C (2005) Pattern-motion selectivity in the human pulvinar. NeuroImage 28:474–480. https://doi.org/10.1016/j.neuroimage.2005.06.015
Vuilleumier P, Driver J (2007) Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions. Philos Trans R Soc B: Biol Sci 362:837–855. https://doi.org/10.1098/rstb.2007.2092
Waters AM, Lipp OV (2008) The influence of animal fear on attentional capture by fear-relevant animal stimuli in children. Behav Res Ther 46:114–121. https://doi.org/10.1016/j.brat.2007.11.002
Watson KK, Ghodasra JH, Platt ML (2009) Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS One 4:e4156. https://doi.org/10.1371/journal.pone.0004156
Wendland JR, Martin BJ, Kruse MR, Lesch K-P, Murphy DL (2006) Simultaneous genotyping of four functional loci of human SLC6A4, with a reappraisal of 5-HTTLPR and rs25531. Mol Psychiatry 11(3):224–226
Yamane Y, Carlson ET, Bowman KC, Wang Z, Connor CE (2008) A neural code for three-dimensional object shape in macaque inferotemporal cortex. Nat Neurosci 11:1352–1360. https://doi.org/10.1038/nn.2202
Zhao B, Chen H, Li B (2005) Pattern motion and component motion sensitivity in cat superior colliculus. NeuroReport 16:721–726
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Kawai, N. (2019). Issues That Remain Unanswered. In: The Fear of Snakes. The Science of the Mind. Springer, Singapore. https://doi.org/10.1007/978-981-13-7530-9_8
Download citation
DOI: https://doi.org/10.1007/978-981-13-7530-9_8
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-7529-3
Online ISBN: 978-981-13-7530-9
eBook Packages: Behavioral Science and PsychologyBehavioral Science and Psychology (R0)