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Open Access 01-07-2016 | Research Article

Approaching threat modulates visuotactile interactions in peripersonal space

Authors: Alyanne M. de Haan, Miranda Smit, Stefan Van der Stigchel, H. Chris Dijkerman

Published in: Experimental Brain Research | Issue 7/2016

Abstract

The region surrounding our body (i.e. peripersonal space) is coded in a multimodal representation by fronto-parietal bimodal neurons integrating tactile stimuli on the body with nearby visual stimuli. This has often been suggested to serve a defensive purpose, which we propose could be mediated through visuotactile predictions. An approaching threat would then be of particular interest to peripersonal space processing. To investigate this, we asked participants to respond as fast as possible to a tactile stimulus on the hand, while looking at an animation of an approaching or receding spider or butterfly. Tactile stimulation was applied at one of 25 possible time points during the animation. Tactile reaction times were faster when an approaching stimulus was closer to the hand at the time of tactile presentation. Critically, this effect of distance on reaction times was larger when participants saw an approaching spider compared to an approaching butterfly, but only for participants who were afraid of spiders. This finding demonstrates that the perceived threat of an approaching stimulus modulates visuotactile interactions in peripersonal space and is consistent with the idea that visuotactile predictions are important for defensive purposes and maintaining bodily integrity.

Alais D, Burr D (2004) The ventriloquist effect results from near-optimal bimodal integration. Curr Biol 14:257–262. doi:10.1016/j.cub.2004.01.029 CrossRefPubMed

Anelli F, Nicoletti R, Bolzani R, Borghi AM (2013) Keep away from danger: dangerous objects in dynamic and static situations. Front Hum Neurosci 7:344. doi:10.3389/fnhum.2013.00344 CrossRefPubMedPubMedCentral

Bassolino M, Serino A, Ubaldi S, Làdavas E (2010) Everyday use of the computer mouse extends peripersonal space representation. Neuropsychologia 48:803–811. doi:10.1016/j.neuropsychologia.2009.11.009 CrossRefPubMed

Belopolsky AV, Devue C, Theeuwes J (2011) Angry faces hold the eyes. Vis Cogn 19:27–36. doi:10.1080/13506285.2010.536186 CrossRef

Bowen AL, Ramachandran R, Muday JA, Schirillo JA (2011) Visual signals bias auditory targets in azimuth and depth. Exp Brain Res 214:403–414. doi:10.1007/s00221-011-2838-1 CrossRefPubMed

Brendel E, Hecht H, DeLucia PR, Gamer M (2014) Emotional effects on time-to-contact judgments: arousal, threat, and fear of spiders modulate the effect of pictorial content. Exp Brain Res 232:2337–2347. doi:10.1007/s00221-014-3930-0 CrossRefPubMed

Brown C, El-Deredy W, Blanchette I (2010) Attentional modulation of visual-evoked potentials by threat: investigating the effect of evolutionary relevance. Brain Cogn 74:281–287. doi:10.1016/j.bandc.2010.08.008 CrossRefPubMed

Canzoneri E, Magosso E, Serino A (2012) Dynamic sounds capture the boundaries of peripersonal space representation in humans. PLoS ONE 7:e44306. doi:10.1371/journal.pone.0044306 CrossRefPubMedPubMedCentral

Carretié L, Hinojosa JA, López-Martín S, Albert J, Tapia M, Pozo MA (2009) Danger is worse when it moves: neural and behavioral indices of enhanced attentional capture by dynamic threatening stimuli. Neuropsychologia 47:364–369. doi:10.1016/j.neuropsychologia.2008.09.007 CrossRefPubMed

Cléry J, Guipponi O, Odouard S, Wardak C, Ben Hamed S (2015) Impact prediction by looming visual stimuli enhances tactile detection. J Neurosci 35:4179–4189. doi:10.1523/JNEUROSCI.3031-14.2015 CrossRefPubMed

Cochrane A, Barnes-Holmes D, Barnes-Holmes Y (2008) The Perceived-Threat Behavioral Approach Test (PT-BAT): measuring avoidance in high-, mid-, and low-spider-fearful participants. Psychol Rec 58:585–596

Coello Y, Bourgeois J, Iachini T (2012) Embodied perception of reachable space: How do we manage threatening objects? Cogn Process 13:S131–S135. doi:10.1007/s10339-012-0470-z CrossRefPubMed

Cooke DF, Graziano MSA (2003) Defensive movements evoked by air puff in monkeys. J Neurophysiol 90:3317–3329. doi:10.1152/jn.00513.2003 CrossRefPubMed

De Vignemont F, Iannetti GD (2015) How many peripersonal spaces? Neuropsychologia 70:327-334. doi:10.1016/j.neuropsychologia.2014.11.018 CrossRefPubMed

Farnè A, Làdavas E (2000) Dynamic size-change of hand peripersonal space following tool use. NeuroReport 11:1645–1649CrossRefPubMed

Farnè A, Pavani F, Meneghello F, Làdavas E (2000) Left tactile extinction following visual stimulation of a rubber hand. Brain 123(Pt 1):2350–2360CrossRefPubMed

Ferri F, Tajadura-Jiménez A, Väljamäe A, Vastano R, Costantini M (2015) Emotion-inducing approaching sounds shape the boundaries of multisensory peripersonal space. Neuropsychologia 70:468–475. doi:10.1016/j.neuropsychologia.2015.03.001 CrossRefPubMed

Fox E, Russo R, Bowles R, Dutton K (2001) Do threatening stimuli draw or hold visual attention in subclinical anxiety? J Exp Psychol Gen 130:681–700. doi:10.1037/0096-3445.130.4.681 CrossRefPubMedPubMedCentral

Frens MA, Van Opstal AJ, Van der Willigen RF (1995) Spatial and temporal factors determine auditory-visual interactions in human saccadic eye movements. Percept Psychophys 57:802–816CrossRefPubMed

Gray R, Tan HZ (2002) Dynamic and predictive links between touch and vision. Exp Brain Res 145:50–55. doi:10.1007/s00221-002-1085-x CrossRefPubMed

Graziano MSA, Cooke DF (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44:845–859. doi:10.1016/j.neuropsychologia.2005.09.009 CrossRefPubMed

Holmes NP (2012) Does tool use extend peripersonal space? A review and re-analysis. Exp Brain Res 218:273–282. doi:10.1007/s00221-012-3042-7 CrossRefPubMed

Holmes NP, Calvert GA, Spence C (2004) Extending or projecting peripersonal space with tools? Multisensory interactions highlight only the distal and proximal ends of tools. Neurosci Lett 372:62–67. doi:10.1016/j.neulet.2004.09.024 CrossRefPubMed

Huang R-S, Chen C-F, Tran AT, Holstein KL, Sereno MI (2012) Mapping multisensory parietal face and body areas in humans. Proc Natl Acad Sci USA 109:18114–18119. doi:10.1073/pnas.1207946109 CrossRefPubMedPubMedCentral

Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurones. NeuroReport 7:2325–2330CrossRefPubMed

Kandula M, Hofman D, Dijkerman HC (2015) Visuo-tactile interactions are dependent on the predictive value of the visual stimulus. Neuropsychologia 70:358-366. doi:10.1016/j.neuropsychologia.2014.12.008 CrossRefPubMed

Koster EHW, Crombez G, Verschuere B, De Houwer J (2004) Selective attention to threat in the dot probe paradigm: differentiating vigilance and difficulty to disengage. Behav Res Ther 42:1183–1192. doi:10.1016/j.brat.2003.08.001 CrossRefPubMed

Ladavas E, Serino A (2008) Action-dependent plasticity in peripersonal space representations. Cogn Neuropsychol 25:1099–1113. doi:10.1080/02643290802359113 CrossRef

Leys C, Ley C, Klein O, Bernard P, Licata L (2013) Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J Exp Soc Psychol 49:764–766. doi:10.1016/j.jesp.2013.03.013 CrossRef

Lipp OV, Derakshan N (2005) Attentional bias to pictures of fear-relevant animals in a dot probe task. Emotion 5:365–369. doi:10.1037/1528-3542.5.3.365 CrossRefPubMed

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. doi:10.1037/1528-3542.7.1.192 CrossRefPubMed

Maister L, Cardini F, Zamariola G, Serino A, Tsakiris M (2015) Your place or mine: shared sensory experiences elicit a remapping of peripersonal space. Neuropsychologia 70:455–461. doi:10.1016/j.neuropsychologia.2014.10.027 CrossRefPubMed

Maravita A, Spence C, Sergent C, Driver J (2002) Seeing your own touched hands in a mirror modulates cross-modal interactions. Psychol Sci 13:350–355. doi:10.1111/j.0956-7976.2002.00463.x CrossRefPubMed

Massar SAA, Mol NM, Kenemans JL, Baas JMP (2011) Attentional bias in high- and low-anxious individuals: evidence for threat-induced effects on engagement and disengagement. Cogn Emot 25:805–817. doi:10.1080/02699931.2010.515065 CrossRefPubMed

McGlynn FD, Wheeler SA, Wilamowska ZA, Katz JS (2008) Detection of change in threat-related and innocuous scenes among snake-fearful and snake-tolerant participants: data from the flicker task. J Anxiety Disord 22:515–523. doi:10.1016/j.janxdis.2007.05.002 CrossRefPubMed

Mulckhuyse M, Dalmaijer ES (2015) Distracted by danger: temporal and spatial dynamics of visual selection in the presence of threat. Cogn Affect Behav Neurosci. doi:10.3758/s13415-015-0391-2

Öhman A, Flykt A, Esteves F (2001) Emotion drives attention: detecting the snake in the grass. J Exp Psychol Gen 130:466–478CrossRefPubMed

Pavani F, Castiello U (2004) Binding personal and extrapersonal space through body shadows. Nat Neurosci 7:14–16. doi:10.1038/nn1167 CrossRefPubMed

Poliakoff E, Miles E, Li X, Blanchette I (2007) The effect of visual threat on spatial attention to touch. Cognition 102:405–414. doi:10.1016/j.cognition.2006.01.006 CrossRefPubMed

Previc FH (1998) The neuropsychology of 3-D space. Psychol Bull 124:123–164CrossRefPubMed

Reed CL, Grubb JD, Steele C (2006) Hands up: attentional prioritization of space near the hand. J Exp Psychol Hum Percept Perform 32:166–177. doi:10.1037/0096-1523.32.1.166 CrossRefPubMed

Requin J, Brener J, Ring C (1991) Preparation for action. In: Jennings JR, Coles MGH (eds) Handbook of cognitive psychophysiology: central and autonomic nervous system approaches. Wiley, New York, pp 357–448

Rizzolatti G, Scandolara C, Matelli M, Gentilucci M, Press B (1981) Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2:147–163CrossRefPubMed

Sagliano L, Cappuccio A, Trojano L, Conson M (2014) Approaching threats elicit a freeze-like response in humans. Neurosci Lett 561:35–40. doi:10.1016/j.neulet.2013.12.038 CrossRefPubMed

Sambo CF, Forster B (2011) When far is near: ERP correlates of crossmodal spatial interactions between tactile and mirror-reflected visual stimuli. Neurosci Lett 500:10–15. doi:10.1016/j.neulet.2011.05.233 CrossRefPubMed

Sambo CF, Iannetti GD (2013) Better safe than sorry? The safety margin surrounding the body is increased by anxiety. J Neurosci 33:14225–14230. doi:10.1523/JNEUROSCI.0706-13.2013 CrossRefPubMed

Sambo CF, Liang M, Cruccu G, Iannetti GD (2012) Defensive peripersonal space: the blink reflex evoked by hand stimulation is increased when the hand is near the face. J Neurophysiol 107:880–889. doi:10.1152/jn.00731.2011 CrossRefPubMed

Shi Z, Jia L, Müller HJ (2012) Modulation of tactile duration judgments by emotional pictures. Front Integr Neurosci 6:24. doi:10.3389/fnint.2012.00024 CrossRefPubMedPubMedCentral

Szymanski J, O’Donohue W (1995) Fear of spiders questionnaire. J Behav Ther Exp Psychiatry 26:31–34. doi:10.1016/0005-7916(94)00072-T CrossRefPubMed

Taffou M, Viaud-Delmon I (2014) Cynophobic fear adaptively extends peri-personal space. Front Psychiatry 5:3–9. doi:10.3389/fpsyt.2014.00122 CrossRef

Tseng P, Bridgeman B (2011) Improved change detection with nearby hands. Exp Brain Res 209:257–269. doi:10.1007/s00221-011-2544-z CrossRefPubMedPubMedCentral

Vagnoni E, Lourenco SF, Longo MR (2012) Threat modulates perception of looming visual stimuli. Curr Biol 22:R826–R827. doi:10.1016/j.cub.2012.07.053 CrossRefPubMed

Valdés-Conroy B, Román FJ, Hinojosa JA, Shorkey SP (2012) So far so good: emotion in the peripersonal/extrapersonal space. PLoS ONE 7:e49162. doi:10.1371/journal.pone.0049162 CrossRefPubMedPubMedCentral

Van Damme S, Crombez G, Eccleston C, Goubert L (2004) Impaired disengagement from threatening cues of impending pain in a crossmodal cueing paradigm. Eur J Pain 8:227–236. doi:10.1016/j.ejpain.2003.08.005 CrossRefPubMed

Van Damme S, Gallace A, Spence C, Crombez G, Moseley GL (2009) Does the sight of physical threat induce a tactile processing bias? Modality-specific attentional facilitation induced by viewing threatening pictures. Brain Res 1253:100–106. doi:10.1016/j.brainres.2008.11.072 CrossRefPubMed

Vrijsen JN, Fleurkens P, Nieuwboer W, Rinck M (2009) Attentional bias to moving spiders in spider fearful individuals. J Anxiety Disord 23:541–545. doi:10.1016/j.janxdis.2008.11.002 CrossRefPubMed

Vromen JMG, Lipp OV, Remington RW (2014) The spider does not always win the fight for attention: disengagement from threat is modulated by goal set. Cogn Emot 9931:1–12. doi:10.1080/02699931.2014.969198

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. doi:10.1016/j.brat.2007.11.002 CrossRefPubMed

Witt JK, Sugovic M (2013) Spiders appear to move faster than non-threatening objects regardless of one’s ability to block them. Acta Psychol (Amst) 143:284–291. doi:10.1016/j.actpsy.2013.04.011 CrossRef

Witt JK, Proffitt DR, Epstein W (2005) Tool use affects perceived distance, but only when you intend to use it. J Exp Psychol Hum Percept Perform 31:880–888. doi:10.1037/0096-1523.31.5.880 CrossRefPubMed

Yamaguchi M, Harwood SL (2015) Threat captures attention but does not affect learning of contextual regularities. Cogn Emot 9931:1–8. doi:10.1080/02699931.2015.1115752 CrossRef

Zopf R, Savage G, Williams MA (2010) Crossmodal congruency measures of lateral distance effects on the rubber hand illusion. Neuropsychologia 48:713–725. doi:10.1016/j.neuropsychologia.2009.10.028 CrossRefPubMed

Title: Approaching threat modulates visuotactile interactions in peripersonal space
Authors: Alyanne M. de Haan
Miranda Smit
Stefan Van der Stigchel
H. Chris Dijkerman
Publication date: 01-07-2016
Publisher: Springer Berlin Heidelberg
Published in: Experimental Brain Research / Issue 7/2016
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-016-4571-2

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Approaching threat modulates visuotactile interactions in peripersonal space

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