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Transcranial direct current stimulation (tDCS) of the inferior frontal cortex affects the “social scaling” of extrapersonal space depending on perspective-taking ability

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Abstract

When we have to judge the distance between another person and an object (social condition), we judge this distance as being smaller compared to judging the distance between two objects (nonsocial condition). It has been suggested that this compression is mediated by the attribution of a motor potential to the reference frame (other person vs. object). In order to explore the neural basis of this effect, we investigated whether the modulation of activity in the inferior frontal cortex (IFC) of the left hemisphere (recruited during visuospatial processes with a social component) changes the way we categorize space in a social compared with a nonsocial condition. We applied transcranial direct current stimulation to the left IFC, with different polarities (anodal, cathodal, and sham) while subjects performed an extrapersonal space categorization task. Interestingly, anodal stimulation of IFC induced an higher compression of space in the social compared to nonsocial condition. By contrast, cathodal stimulation induced the opposite effect. Furthermore, we found that this effect is modulated by interindividual differences in cognitive perspective taking. Our data support the idea that IFC is recruited during the social categorization of space.

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References

  • Abdullaev YG, Bechtereva NP (1993) Neuronal correlate of the higher-order semantic code in human prefrontal cortex in language tasks. Int J Psychophysiol 14(3):167–177

    Article  CAS  PubMed  Google Scholar 

  • Bloesch EK, Davoli CC, Roth N, Brockmole JR, Abrams RA (2012) Watch this! Observed tool use affects perceived distance. Psychon Bull Rev 19(2):177–183

    Article  PubMed  Google Scholar 

  • Cardellicchio P, Sinigaglia C, Costantini M (2011) The space of affordances: a TMS study. Neuropsychologia 49(5):1369–1372

    Article  PubMed  Google Scholar 

  • Cattaneo L, Caruana F, Jezzini A, Rizzolatti G (2009) Representation of goal and movements without overt motor behavior in the human motor cortex: a transcranial magnetic stimulation study. J Neurosci 29(36):11134–11138

    Article  CAS  PubMed  Google Scholar 

  • Coello Y, Delevoye-Turrell Y (2007) Embodiment, spatial categorisation and action. Conscious Cogn 16(3):667–683

    Article  PubMed  Google Scholar 

  • Costantini M, Ambrosini E, Sinigaglia C, Gallese V (2011) Tool-use observation makes far objects ready-to-hand. Neuropsychologia 49(9):2658–2663

    Article  PubMed  Google Scholar 

  • Creem-Regehr SH, Gagnon KT, Geuss MN, Stefanucci JK (2015) Relating spatial perspective taking to the perception of other’s affordances: providing a foundation for predicting the future behavior of others. Perspective taking: building a neurocognitive framework for integrating the “social” and the “spatial”

  • Davis MH (1983) Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 44(1):113

    Article  Google Scholar 

  • Enticott PG, Arnold SL, Fitzgibbon BM, Hoy KE, Susilo DA, Fitzgerald PB (2012) Transcranial direct current stimulation (tDCS) of the inferior frontal gyrus disrupts interpersonal motor resonance. Neuropsychologia 50(7):1628–1631

    Article  PubMed  Google Scholar 

  • Erle TM, Topolinski S (2015) Spatial and empathic perspective-taking Correlate on a dispositional level. Soc Cogn 33(3):187

    Article  Google Scholar 

  • Ferrucci R, Marceglia S, Vergari M, Cogiamanian F, Mrakic-Sposta S, Mameli FEEA, Priori A (2008) Cerebellar transcranial direct current stimulation impairs the practice-dependent proficiency increase in working memory. J Cogn Neurosci 20(9):1687–1697

    Article  CAS  PubMed  Google Scholar 

  • Fini C, Costantini M, Committeri G (2014) Sharing space: the presence of other bodies extends the space judged as near. PLoS ONE 9(12):e114719

    Article  PubMed  PubMed Central  Google Scholar 

  • Fini C, Brass M, Committeri G (2015a) Social scaling of extrapersonal space: target objects are judged as closer when the reference frame is a human agent with available movement potentialities. Cognition 134:50–56

    Article  CAS  PubMed  Google Scholar 

  • Fini C, Committeri G, Müller BC, Deschrijver E, Brass M (2015b) How watching Pinocchio movies changes our subjective experience of extrapersonal space. PLoS ONE 10(3):e0120306

    Article  PubMed  PubMed Central  Google Scholar 

  • Galea JM, Celnik P (2009) Brain polarization enhances the formation and retention of motor memories. J Neurophysiol 102(1):294–301

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallese V, Sinigaglia C (2011) What is so special about embodied simulation? Trends Cogn Sci 15(11):512–519

    Article  PubMed  Google Scholar 

  • Gazzola V, Aziz-Zadeh L, Keysers C (2006) Empathy and the somatotopic auditory mirror system in humans. Curr Biol 16(18):1824–1829

    Article  CAS  PubMed  Google Scholar 

  • Gazzola V, Rizzolatti G, Wicker B, Keysers C (2007) The anthropomorphic brain: the mirror neuron system responds to human and robotic actions. Neuroimage 35(4):1674–1684

    Article  CAS  PubMed  Google Scholar 

  • Holland R, Leff AP, Josephs O, Galea JM, Desikan M, Price CJ, Rothwell JC, Crinion J (2011) Speech facilitation by left inferior frontal cortex stimulation. Curr Biol 21:1403–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu TY, Tseng LY, Yu JX, Kuo WJ, Hung DL, Tzeng OJ, Juan CH (2011) Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. Neuroimage 56(4):2249–2257

    Article  PubMed  Google Scholar 

  • Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286(5449):2526–2528

    Article  CAS  PubMed  Google Scholar 

  • Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64(5):872–875

    Article  CAS  PubMed  Google Scholar 

  • Jang SH, Ahn SH, Byun WM, Kim CS, Lee MY, Kwon YH (2009) The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: an fMRI study. Neurosci Lett 460(2):117–120

    Article  CAS  PubMed  Google Scholar 

  • Marshall L, Mölle M, Siebner HR, Born J (2005) Bifrontal transcranial direct current stimulation slows reaction time in a working memory task. BMC Neurosci 6(1):1

    Article  Google Scholar 

  • Mazoyer BM, Tzourio N, Frak V, Syrota A, Murayama N, Levrier O, Mehler J (1993) The cortical representation of speech. J Cogn Neurosci 5(4):467–479

    Article  CAS  PubMed  Google Scholar 

  • Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(3):633–639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitsche MA, Doemkes S, Karakoese T, Antal A, Liebetanz D, Lang N, Paulus W (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97(4):3109–3117

    Article  CAS  PubMed  Google Scholar 

  • Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1(3):206–223

    Article  PubMed  Google Scholar 

  • Proffitt DR (2006) Embodied perception and the economy of action. Perspect Psychol Sci 1(2):110–122

    Article  PubMed  Google Scholar 

  • Proffitt DR, Stefanucci J, Banton T, Epstein W (2003) The role of effort in perceiving distance. Psychol Sci 14(2):106–112

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Sinigaglia C (2010) The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 11(4):264–274

    Article  CAS  PubMed  Google Scholar 

  • Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2(9):661–670

    Article  CAS  PubMed  Google Scholar 

  • Schnall S, Zadra JR, Proffitt DR (2010) Direct evidence for the economy of action: glucose and the perception of geographical slant. Perception 39(4):464–482

    Article  PubMed  PubMed Central  Google Scholar 

  • Stagg CJ, O’shea J, Kincses ZT, Woolrich M, Matthews PM, Johansen-Berg H (2009) Modulation of movement-associated cortical activation by transcranial direct current stimulation. Eur J Neurosci 30(7):1412–1423

    Article  CAS  PubMed  Google Scholar 

  • Stumpf H, Fay E (1983) Schlauchfiguren: ein Test zur Beurteilung des räumlichen Vorstellungsvermögens. Verlag für Psychologie, Hogrefe

    Google Scholar 

  • Sugovic M, Witt JK (2013) An older view on distance perception: older adults perceive walkable extents as farther. Exp Brain Res 226(3):383–391

    Article  PubMed  Google Scholar 

  • Thompson-Schill SL, D’Esposito M, Aguirre GK, Farah MJ (1997) Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc Natl Acad Sci 94(26):14792–14797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson-Schill SL, Kurtz KJ, Gabrieli JD (1998) Effects of semantic and associative relatedness on automatic priming. J Mem Lang 38(4):440–458

    Article  Google Scholar 

  • Tversky B, Hard BM (2009) Embodied and disembodied cognition: spatial perspective-taking. Cognition 110(1):124–129

    Article  PubMed  Google Scholar 

  • Uithol S, van Rooij I, Bekkering H, Haselager P (2011) Understanding motor resonance. Soc Neurosci 6(4):388–397

    Article  PubMed  Google Scholar 

  • Vogt S, Buccino G, Wohlschläger AM, Canessa N, Shah NJ, Zilles K, Fink GR (2007) Prefrontal involvement in imitation learning of hand actions: effects of practice and expertise. Neuroimage 37(4):1371–1383

    Article  PubMed  Google Scholar 

  • Wagner AD, Desmond JE, Demb JB, Glover GH, Gabrieli JD (1997) Semantic repetition priming for verbal and pictorial knowledge: a functional MRI study of left inferior prefrontal cortex. J Cognitive neurosci 9(6):714–726

    Article  CAS  Google Scholar 

  • Wagner AD, Paré-Blagoev EJ, Clark J, Poldrack RA (2001) Recovering meaning: left prefrontal cortex guides controlled semantic retrieval. Neuron 31(2):329–338

    Article  CAS  PubMed  Google Scholar 

  • Witt JK, Proffitt DR (2008) Action-specific influences on distance perception: a role for motor simulation. J Exp Psychol Hum Percept Perform 34(6):1479

    Article  PubMed  PubMed Central  Google Scholar 

  • Witt JK, Proffitt DR, Epstein W (2004) Perceiving distance: a role of effort and intent. Perception 33(5):577–590

    Article  PubMed  Google Scholar 

  • 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(5):880

    Article  PubMed  Google Scholar 

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Acknowledgements

This study has been supported by FWO Research Project G.0223.13.

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Correspondence to Chiara Fini.

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Fini, C., Bardi, L., Epifanio, A. et al. Transcranial direct current stimulation (tDCS) of the inferior frontal cortex affects the “social scaling” of extrapersonal space depending on perspective-taking ability. Exp Brain Res 235, 673–679 (2017). https://doi.org/10.1007/s00221-016-4817-z

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  • DOI: https://doi.org/10.1007/s00221-016-4817-z

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