#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Gaze and body cues interplay during interactive requests


Autoři: Sonia Betti aff001;  Umberto Castiello aff001;  Silvia Guerra aff001;  Umberto Granziol aff001;  Giovanni Zani aff001;  Luisa Sartori aff001
Působiště autorů: Department of General Psychology, University of Padua, Padua, Italy aff001;  Padova Neuroscience Center, University of Padua, Padua, Italy aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223591

Souhrn

Although observing other’s gaze and body movements provides a crucial source of information to successfully interact with other people, it remains unclear whether observers weigh differently these cues and whether the convergence of gaze and body’s directions determines facilitation effects. Here we aim to shed more light on this issue by testing the reliance upon these cues from both a behavioral and a neurophysiological perspective in a social interactive context. In Experiment 1, we manipulated the convergence between the direction of an actor’s upper limb movement and gaze direction while he attempts to socially interact with the participants observing the scene. We determined the direction of gaze as well as the duration of participants’ ocular fixations during the observation of the scene. In Experiment 2, we measured and correlated the effect of the body/gaze manipulation on corticospinal excitability and on the readiness to interact—a disposition to engage in social situations. Eye-tracking data revealed that participants fixated chiefly the actor’s head when his hand and gaze directions were divergent. Possibly a strategy to disambiguate the scene. Whereas participants mainly fixated the actor’s hand when he performed an interactive request toward the participants. From a neurophysiological point of view, the more participants felt involved in the interaction, the lower was motor preparation in the muscle potentially needed to fulfill the actor’s request. We contend that social contexts are more likely to elicit motor preparation compared to non-social ones, and that muscular inhibition is a necessary mechanism in order to prevent unwanted overt reactions during action observation tasks.

Klíčová slova:

Attention – Body limbs – Electromyography – Eye movements – Motor system – Neurophysiology – Questionnaires


Zdroje

1. Emery NJ. The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev. 2000;24: 581–604. doi: 10.1016/S0149-7634(00)00025-7 10940436

2. Porciello G, Crostella F, Liuzza MT, Valentini E, Aglioti SM. rTMS-induced virtual lesion of the posterior parietal cortex (PPC) alters the control of reflexive shifts of social attention triggered by pointing hands. Neuropsychologia. 2014;59: 148–156. doi: 10.1016/j.neuropsychologia.2014.04.017 24813151

3. Conty L, Tijus C, Hugueville L, Coelho E, George N. Searching for asymmetries in the detection of gaze contact versus averted gaze under different head views: a behavioural study. Spat Vis. 2006;19: 529–545. doi: 10.1163/156856806779194026 17278526

4. Farroni T, Csibra G, Simion F, Johnson MH. Eye contact detection in humans from birth. Proc Natl Acad Sci. 2002;99: 9602–9605. doi: 10.1073/pnas.152159999 12082186

5. Langton SRH, Watt RJ, Bruce V. Do the eyes have it? Cues to the direction of social attention. Trends Cogn Sci. 2000;4: 50–59. doi: 10.1016/S1364-6613(99)01436-9 10652522

6. Maurer D, Salapatek P. Developmental changes in the scanning of faces by young infants. Child Dev. 1976;47: 523–527. 1269319

7. Driver JI, Davis G, Ricciardelli P, Kidd P, Maxwell E, Baron-Cohen S. Gaze Perception Triggers Reflexive Visuospatial Orienting. Vis Cogn. 1999;6: 509–540. doi: 10.1080/135062899394920

8. Friesen CK, Kingstone A. The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychon Bull Rev. 1998;5: 490–495. doi: 10.3758/BF03208827

9. Langton SRH, Bruce V. Reflexive Visual Orienting in Response to the Social Attention of Others. Vis Cogn. 1999;6: 541–567. doi: 10.1080/135062899394939

10. Bukowski H, Hietanen JK, Samson D. From gaze cueing to perspective taking: Revisiting the claim that we automatically compute where or what other people are looking at. Vis Cogn. 2015;23: 1020–1042. doi: 10.1080/13506285.2015.1132804 26924936

11. Butterworth G. The ontogeny and phylogeny of joint visual attention. Natural theories of mind: Evolution, development and simulation of everyday mindreading. Cambridge, MA, US: Basil Blackwell; 1991. pp. 223–232.

12. Atkinson MA, Simpson AA, Cole GG. Visual attention and action: How cueing, direct mapping, and social interactions drive orienting. Psychon Bull Rev. 2017; 1–21. doi: 10.3758/s13423-016-1113-7

13. Frischen A, Bayliss AP, Tipper SP. Gaze cueing of attention: Visual attention, social cognition, and individual differences. Psychol Bull. 2007;133: 694–724. doi: 10.1037/0033-2909.133.4.694 17592962

14. Becchio C, Bertone C, Castiello U. How the gaze of others influences object processing. Trends Cogn Sci. 2008;12: 254–258. doi: 10.1016/j.tics.2008.04.005 18555735

15. Sartori L, Becchio C, Castiello U. Cues to intention: The role of movement information. Cognition. 2011;119: 242–252. doi: 10.1016/j.cognition.2011.01.014 21349505

16. Castiello U. Understanding other people’s actions: Intention and attention. J Exp Psychol Hum Percept Perform. 2003;29: 416–430. doi: 10.1037/0096-1523.29.2.416 12760625

17. Pierno AC, Becchio C, Wall MB, Smith AT, Turella L, Castiello U. When gaze turns into grasp. J Cogn Neurosci. 2006;18: 2130–2137. doi: 10.1162/jocn.2006.18.12.2130 17129195

18. Ramsey R, Cross ES, Hamilton AF de C. Predicting others’ actions via grasp and gaze: evidence for distinct brain networks. Psychol Res. 2012;76: 494–502. doi: 10.1007/s00426-011-0393-9 22120203

19. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G. Understanding motor events: a neurophysiological study. Exp Brain Res. 1992;91: 176–180. doi: 10.1007/bf00230027 1301372

20. Coudé G, Festante F, Cilia A, Loiacono V, Bimbi M, Fogassi L, et al. Mirror Neurons of Ventral Premotor Cortex Are Modulated by Social Cues Provided by Others’ Gaze. J Neurosci. 2016;36: 3145–3156. doi: 10.1523/JNEUROSCI.3220-15.2016 26985026

21. Jellema T, Baker CI, Wicker B, Perrett DI. Neural representation for the perception of the intentionality of actions. Brain Cogn. 2000;44: 280–302. doi: 10.1006/brcg.2000.1231 11041992

22. Letesson C, Grade S, Edwards MG. Different but complementary roles of action and gaze in action observation priming: Insights from eye- and motion-tracking measures. Front Psychol. 2015;6. doi: 10.3389/fpsyg.2015.00006

23. Prinsen J, Bernaerts S, Wang Y, de Beukelaar TT, Cuypers K, Swinnen SP, et al. Direct eye contact enhances mirroring of others’ movements: A transcranial magnetic stimulation study. Neuropsychologia. 2017;95: 111–118. doi: 10.1016/j.neuropsychologia.2016.12.011 27939365

24. Innocenti A, Stefani ED, Bernardi NF, Campione GC, Gentilucci M. Gaze Direction and Request Gesture in Social Interactions. PLOS ONE. 2012;7: e36390. doi: 10.1371/journal.pone.0036390 22693550

25. Di Paolo E, De Jaegher H. The interactive brain hypothesis. Front Hum Neurosci. 2012;6. doi: 10.3389/fnhum.2012.00006

26. Sartori L, Betti S. Complementary actions. Front Psychol. 2015;6: 557. doi: 10.3389/fpsyg.2015.00557 25983717

27. Betti S, Zani G, Granziol U, Guerra S, Castiello U, Sartori L. Look At Me: Early Gaze Engagement Enhances Corticospinal Excitability During Action Observation. Front Psychol. 2018;9. doi: 10.3389/fpsyg.2018.00009

28. Pinheiro J, Bates D, Debroy S, Sarkar D, R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3. 1–128. 2016; Available: http://CRAN.R-project.org/package=nlme

29. Nakagawa S, Schielzeth H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol. 2013; 133–142. doi: 10.1111/j.2041-210x.2012.00261.x

30. Bartoń K. MuMIn: Multi-Model Inference. 2018; Available: https://CRAN.R-project.org/package=MuMIn

31. Lenth RV. Least-Squares Means: The R Package lsmeans. J Stat Softw. 2016;69: 1–33.

32. Gaylor DW, Hopper FN. Estimating the Degrees of Freedom for Linear Combinations of Mean Squares by Satterthwaite’s Formula. Technometrics. 1969;11: 691–706. doi: 10.1080/00401706.1969.10490732

33. Westfall J, Kenny DA, Judd CM. Statistical power and optimal design in experiments in which samples of participants respond to samples of stimuli. J Exp Psychol Gen. 2014;143: 2020–2045. doi: 10.1037/xge0000014 25111580

34. Becchio C, Koul A, Ansuini C, Bertone C, Cavallo A. Seeing mental states: An experimental strategy for measuring the observability of other minds. Phys Life Rev. 2018;24: 67–80. doi: 10.1016/j.plrev.2017.10.002 29066076

35. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol Potentials Sect. 1998;108: 1–16. doi: 10.1016/S0168-5597(97)00096-8

36. Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009;120: 2008–2039. doi: 10.1016/j.clinph.2009.08.016 19833552

37. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M. Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity. J Clin Neurophysiol. 1992;9: 132. 1552001

38. Mills KR, Boniface SJ, Schubert M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol Potentials Sect. 1992;85: 17–21. doi: 10.1016/0168-5597(92)90096-T

39. Betti S, Zani G, Guerra S, Castiello U, Sartori L. Reach-To-Grasp Movements: A Multimodal Techniques Study. Front Psychol. 2018;9. doi: 10.3389/fpsyg.2018.00009

40. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 1994;91: 79–92. doi: 10.1016/0013-4694(94)90029-9 7519144

41. Betti S, Castiello U, Guerra S, Sartori L. Overt orienting of spatial attention and corticospinal excitability during action observation are unrelated. PLOS ONE. 2017;12: e0173114. doi: 10.1371/journal.pone.0173114 28319191

42. D’Innocenzo G, Gonzalez CC, Nowicky AV, Williams AM, Bishop DT. Motor resonance during action observation is gaze-contingent: A TMS study. Neuropsychologia. 2017;103: 77–86. doi: 10.1016/j.neuropsychologia.2017.07.017 28720525

43. Wright DJ, Wood G, Franklin ZC, Marshall B, Riach M, Holmes PS. Directing visual attention during action observation modulates corticospinal excitability. PLOS ONE. 2018;13: e0190165. doi: 10.1371/journal.pone.0190165 29304044

44. Naish KR, Houston-Price C, Bremner AJ, Holmes NP. Effects of action observation on corticospinal excitability: Muscle specificity, direction, and timing of the mirror response. Neuropsychologia. 2014;64: 331–348. doi: 10.1016/j.neuropsychologia.2014.09.034 25281883

45. Sartori L, Becchio C, Bulgheroni M, Castiello U. Modulation of the action control system by social intention: unexpected social requests override preplanned action. J Exp Psychol Hum Percept Perform. 2009;35: 1490–1500. doi: 10.1037/a0015777 19803652

46. Salmelin R, Hámáaláinen M, Kajola M, Hari R. Functional Segregation of Movement-Related Rhythmic Activity in the Human Brain. NeuroImage. 1995;2: 237–243. doi: 10.1006/nimg.1995.1031 9343608

47. Jurkiewicz MT, Gaetz WC, Bostan AC, Cheyne D. Post-movement beta rebound is generated in motor cortex: Evidence from neuromagnetic recordings. NeuroImage. 2006;32: 1281–1289. doi: 10.1016/j.neuroimage.2006.06.005 16863693

48. Schuch S, Bayliss AP, Klein C, Tipper SP. Attention modulates motor system activation during action observation: evidence for inhibitory rebound. Exp Brain Res. 2010;205: 235–249. doi: 10.1007/s00221-010-2358-4 20644919

49. Hummel F, Andres F, Altenmüller E, Dichgans J, Gerloff C. Inhibitory control of acquired motor programmes in the human brain. Brain. 2002;125: 404–420. doi: 10.1093/brain/awf030 11844740

50. Zarkowski P, Shin CJ, Dang T, Russo J, Avery D. EEG and the variance of motor evoked potential amplitude. Clin EEG Neurosci. 2006;37: 247–251. doi: 10.1177/155005940603700316 16929713

51. Sauseng P, Klimesch W, Gerloff C, Hummel FC. Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex. Neuropsychologia. 2009;47: 284–288. doi: 10.1016/j.neuropsychologia.2008.07.021 18722393

52. Naish KR, Obhi SS. Self-selected conscious strategies do not modulate motor cortical output during action observation. J Neurophysiol. 2015;114: 2278–2284. doi: 10.1152/jn.00518.2015 26311182

53. Baldissera F, Cavallari P, Craighero L, Fadiga L. Modulation of spinal excitability during observation of hand actions in humans. Eur J Neurosci. 2001;13: 190–194. doi: 10.1046/j.0953-816x.2000.01368.x 11135017

54. Mukamel R, Ekstrom AD, Kaplan J, Iacoboni M, Fried I. Single-Neuron Responses in Humans during Execution and Observation of Actions. Curr Biol. 2010;20: 750–756. doi: 10.1016/j.cub.2010.02.045 20381353

55. Stamos AV, Savaki HE, Raos V. The Spinal Substrate of the Suppression of Action during Action Observation. J Neurosci. 2010;30: 11605–11611. doi: 10.1523/JNEUROSCI.2067-10.2010 20810881

56. Vigneswaran G, Philipp R, Lemon RN, Kraskov A. M1 Corticospinal Mirror Neurons and Their Role in Movement Suppression during Action Observation. Curr Biol. 2013;23: 236–243. doi: 10.1016/j.cub.2012.12.006 23290556

57. Hardwick RM, McAllister CJ, Holmes PS, Edwards MG. Transcranial magnetic stimulation reveals modulation of corticospinal excitability when observing actions with the intention to imitate: Intention to imitate modulates action observation. Eur J Neurosci. 2012;35: 1475–1480. doi: 10.1111/j.1460-9568.2012.08046.x 22519854

58. Tipper SP. From observation to action simulation: The role of attention, eye-gaze, emotion, and body state. Q J Exp Psychol. 2010;63: 2081–2105. doi: 10.1080/17470211003624002 20721814

59. Bach P, Peatfield NA, Tipper SP. Focusing on body sites: the role of spatial attention in action perception. Exp Brain Res. 2007;178: 509–517. doi: 10.1007/s00221-006-0756-4 17091293

60. Chong TT-J, Williams MA, Cunnington R, Mattingley JB. Selective attention modulates inferior frontal gyrus activity during action observation. NeuroImage. 2008;40: 298–307. doi: 10.1016/j.neuroimage.2007.11.030 18178107

61. Chong TT-J, Cunnington R, Williams MA, Mattingley JB. The role of selective attention in matching observed and executed actions. Neuropsychologia. 2009;47: 786–795. doi: 10.1016/j.neuropsychologia.2008.12.008 19124033

62. Sartori L, Cavallo A, Bucchioni G, Castiello U. Corticospinal excitability is specifically modulated by the social dimension of observed actions. Exp Brain Res. 2011;211: 557. doi: 10.1007/s00221-011-2650-y 21472443

63. Flach R, Press C, Badets A, Heyes C. Shaking hands: Priming by social action effects. Br J Psychol. 2010;101: 739–749. doi: 10.1348/000712609X484595 20100397

64. Bunday KL, Lemon RN, Kilner JM, Davare M, Orban GA. Grasp-specific motor resonance is influenced by the visibility of the observed actor. Cortex. 2016;84: 43–54. doi: 10.1016/j.cortex.2016.09.002 27697663

65. Cole GG, Skarratt PA, Kuhn G. Real Person Interaction in Visual Attention Research. Eur Psychol. 2016;21: 141–149. doi: 10.1027/1016-9040/a000243

66. Chemero A. An Outline of a Theory of Affordances. Ecol Psychol. 2003;15: 181–195. doi: 10.1207/S15326969ECO1502_5

67. Gibson JJ. The Ecological Approach to Visual Perception. Boston: Houghton Mifflin; 1979.

68. Tipper SP, Paul MA, Hayes AE. Vision-for-action: The effects of object property discrimination and action state on affordance compatibility effects. Psychon Bull Rev. 2006;13: 493–498. doi: 10.3758/BF03193875 17048736

69. Borghi AM, Flumini A, Natraj N, Wheaton LA. One hand, two objects: Emergence of affordance in contexts. Brain Cogn. 2012;80: 64–73. doi: 10.1016/j.bandc.2012.04.007 22634033

70. Scorolli C, Miatton M, Wheaton LA, Borghi AM. I give you a cup, I get a cup: A kinematic study on social intention. Neuropsychologia. 2014;57: 196–204. doi: 10.1016/j.neuropsychologia.2014.03.006 24680723

71. Borghi AM. Affordances, context and sociality. Synthese. 2018; doi: 10.1007/s11229-018-02044-1

72. Dezecache G, Conty L, Grèzes J. Social affordances: Is the mirror neuron system involved? Behav Brain Sci. 2013;36: 417–418. doi: 10.1017/S0140525X12001872 23883746

73. Gallagher HL, Frith CD. Dissociable neural pathways for the perception and recognition of expressive and instrumental gestures. Neuropsychologia. 2004;42: 1725–1736. doi: 10.1016/j.neuropsychologia.2004.05.006 15351623

74. Sartori L. Complementary Actions. In: Obhi SS, Cross ES, editors. Shared Representations. Cambridge: Cambridge University Press; 2016. pp. 392–416. doi: 10.1017/CBO9781107279353.020

75. Sartori L, Bucchioni G, Castiello U. When emulation becomes reciprocity. Soc Cogn Affect Neurosci. 2013;8: 662–669. doi: 10.1093/scan/nss044 22490925

76. Sebanz N, Shiffrar M. Detecting deception in a bluffing body: The role of expertise. Psychon Bull Rev. 2009;16: 170–175. doi: 10.3758/PBR.16.1.170 19145029

77. Finisguerra A, Amoruso L, Makris S, Urgesi C. Dissociated Representations of Deceptive Intentions and Kinematic Adaptations in the Observer’s Motor System. Cereb Cortex. 2018;28: 33–47. doi: 10.1093/cercor/bhw346 29253254

78. Wokke ME, Knot SL, Fouad A, Richard Ridderinkhof K. Conflict in the kitchen: Contextual modulation of responsiveness to affordances. Conscious Cogn. 2016;40: 141–146. doi: 10.1016/j.concog.2016.01.007 26821243

79. Reader AT, Holmes NP. Examining ecological validity in social interaction: problems of visual fidelity, gaze, and social potential. Cult Brain. 2016;4: 134–146. doi: 10.1007/s40167-016-0041-8 27867831

80. Kingstone A, Smilek D, Ristic J, Kelland Friesen C, Eastwood JD. Attention, Researchers! It Is Time to Take a Look at the Real World. Curr Dir Psychol Sci. 2003;12: 176–180. doi: 10.1111/1467-8721.01255


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#