Advertisement

Experimental Brain Research

, Volume 236, Issue 5, pp 1409–1420 | Cite as

Emotional cues and social anxiety resolve ambiguous perception of biological motion

  • Hörmet Yiltiz
  • Lihan Chen
Research Article

Abstract

Perceptions of ambiguous biological motion are modulated by different individual cognitive abilities (such as inhibition and empathy) and emotional states (such as anxiety). This study explored facing-the-viewer bias (FTV) in perceiving ambiguous directions of biological motion, and investigated whether task-irrelevant simultaneous face emotional cues in the background and the individual social anxiety traits could affect FTV. We found that facial motion cues as background affect sociobiologically relevant scenarios, including biological motion, but not non-biological situations (conveyed through random dot motion). Individuals with high anxiety traits demonstrated a more dominant FTV bias than individuals with low anxiety traits. Ensemble coding-like processing of task-irrelevant multiple emotional cues could magnify the facing-the-viewer bias than did in the single emotional cue. Overall, those findings suggest a correlation between high-level emotional processing and high-level motion perception (subjective to attentional control) contributes to facing-the-viewer bias.

Keywords

Biological motion Emotion Social anxiety Ambiguity Visual perception Ensemble coding Facing-the-viewer bias 

Notes

Acknowledgements

This work is funded by the Natural Science Foundation of China (NSFC61527804, 81371206) and was partially funded by NSFC and the German Research Foundation (DFG) in Project Crossmodal Learning, NSFC 61621136008/DFG TRR-169.

References

  1. Aaen-Stockdale C, Thompson B, Hess RF, Troje NF (2008) Biological motion perception is cue-invariant. J Vis 8(8):6CrossRefPubMedGoogle Scholar
  2. Ahlström V, Blake R, Ahlström U (1997) Perception of biological motion. Perception 26(12):1539–1548CrossRefPubMedGoogle Scholar
  3. Alvarez GA (2011) Representing multiple objects as an ensemble enhances visual cognition. Trends Cogn Sci 15(3):122–131CrossRefPubMedGoogle Scholar
  4. Ariely D (2001) Seeing sets: representation by statistical properties. Psychol Sci 12(2):157–162CrossRefPubMedGoogle Scholar
  5. Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg MJ, van Ijzendoorn MH (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychol Bull 133(1):1–24.  https://doi.org/10.1037/0033-2909.133.1.1 CrossRefPubMedGoogle Scholar
  6. Battelli L, Cavanagh P, Thornton IM (2003) Perception of biological motion in parietal patients. Neuropsychologia 41(13):1808–1816CrossRefPubMedGoogle Scholar
  7. Beintema JA, Lappe M (2002) Perception of biological motion without local image motion. Proc Nat Acad Sci 99(8):5661–5663CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bertenthal BI, Pinto J (1994) Global processing of biological motions. Psychol Sci 5:221–225CrossRefGoogle Scholar
  9. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10(4):433–436CrossRefPubMedGoogle Scholar
  10. Bouma H (1970) Interaction effects in parafoveal letter recognition. Nature 226(5241):177–178CrossRefPubMedGoogle Scholar
  11. Brooks A, Schouten B, Troje NF, Verfaillie K, Blanke O, van der Zwan R (2008) Correlated changes in perceptions of the gender and orientation of ambiguous biological motion figures. Curr Biol 18(17):R728–R729.  https://doi.org/10.1016/j.cub.2008.06.054 CrossRefPubMedGoogle Scholar
  12. Cavanagh P, Alvarez GA (2005) Tracking multiple targets with multifocal attention. Trends Cogn Sci 9(7):349–354.  https://doi.org/10.1016/j.tics.2005.05.009 CrossRefPubMedGoogle Scholar
  13. Cavanagh P, Labianca AT, Thornton IM (2001) Attention-based visual routines: sprites. Cognition 80(1–2):47–60CrossRefPubMedGoogle Scholar
  14. Chong SC, Treisman A (2003) Representation of statistical properties. Vision Res 43(4):393–404CrossRefPubMedGoogle Scholar
  15. Clarke TJ, Bradshaw MF, Field DT, Hampson SE, Rose D (2005) The perception of emotion from body movement in point-light displays of interpersonal dialogue. Perception 34(10):1171–1180.  https://doi.org/10.1068/p5203 CrossRefPubMedGoogle Scholar
  16. Cutting JE, Kozlowski LT (1977) Recognition of friends by their walk: gait perception without familiarity cues. Bull Psychon Soc 9:353–356CrossRefGoogle Scholar
  17. Daniel PM, Whitteridge D (1961) The representation of the visual field on the cerebral cortex in monkeys. J Physiol 159(2):203–221CrossRefPubMedPubMedCentralGoogle Scholar
  18. de Lussanet MH, Lappe M (2012). Depth perception from point-light biological motion displays. J Vis 12(11). doi: 2.11.14[pii]10.1167/12.11.14Google Scholar
  19. de Gardelle V, Summerfield C (2011) Robust averaging during perceptual judgment. Proc Natl Acad Sci USA 108(32):13341–13346.  https://doi.org/10.1073/pnas.1104517108 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47CrossRefPubMedGoogle Scholar
  21. Fox E, Russo R, Dutton K (2002) Attentional bias for threat: evidence for delayed disengagement from emotional faces. Cogn Emot 16(3):355–379.  https://doi.org/10.1080/02699930143000527 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Giese MA, Poggio T (2003) Neural mechanisms for the recognition of biological movements. Nat Rev Neurosci 4(3):179–192CrossRefPubMedGoogle Scholar
  23. Gilboa-Schechtman E, Foa EB, Amir N (1999) Attentional biases for facial expressions in social phobia: the face-in-the-crowd paradigm. Cogn Emot 13(3):305–318CrossRefGoogle Scholar
  24. Gong X, Huang YX, Wang Y, Luo YJ (2011) The revision of chinese facial affective system. Chin Mental Health J 25(1):40–46Google Scholar
  25. Gray KL, Adams WJ, Garner M (2009) The influence of anxiety on the initial selection of emotional faces presented in binocular rivalry. Cognition 113(1):105–110.  https://doi.org/10.1016/j.cognition.2009.06.009 CrossRefPubMedGoogle Scholar
  26. Haberman J, Whitney D (2007) Rapid extraction of mean emotion and gender from sets of faces. Curr Biol 17(17):R751–753CrossRefPubMedGoogle Scholar
  27. Haberman J, Harp T, Whitney D (2009) Averaging facial expression over time. J Vis 9(11):1 1–13CrossRefGoogle Scholar
  28. Haselton MG, Bryant GA, Wilke A, Frederick DA, Galperin A, Frankenhuis WE, Moore T (2009) Adaptive rationality: an evolutionary perspective on cognitive bias. Soc Cogn 27(5):733–763CrossRefGoogle Scholar
  29. He Y, Zhang M (2004) Psychometric investigation of liebowitz social anxiety scale. J Diagn Concepts Pract 3:89–93Google Scholar
  30. Heenan A, Troje NF (2014) Both physical exercise and progressive muscle relaxation reduce the facing-the-viewer bias in biological motion perception. PLoS One 9(7):e99902.  https://doi.org/10.1371/journal.pone.0099902 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Heenan A, Troje NF (2015) The relationship between social anxiety and the perception of depth-ambiguous biological motion stimuli is mediated by inhibitory ability. Acta Psychol (Amst) 157:93–100.  https://doi.org/10.1016/j.actpsy.2015.02.012 CrossRefGoogle Scholar
  32. Hindi Attar C, Muller MM, Andersen SK, Buchel C, Rose M (2010) Emotional processing in a salient motion context: integration of motion and emotion in both V5/hMT + and the amygdala. J Neurosci 30(15):5204–5210. doi:30/15/5204 [pii]10.1523/JNEUROSCI.5029–09.2010CrossRefPubMedGoogle Scholar
  33. Holbrook C, Galperin A, Fessler DM, Johnson KL, Bryant GA, Haselton MG (2014) If looks could kill: anger attributions are intensified by affordances for doing harm. Emotion 14(3):455–461.  https://doi.org/10.1037/a0035826 CrossRefPubMedGoogle Scholar
  34. Hunt S, Low J, Burns KC (2008) Adaptive numerical competency in a food-hoarding songbird. Proc Biol Sci 275(1649):2373–2379.  https://doi.org/10.1098/rspb.2008.0702 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Iacoboni M, Molnar-Szakacs I, Gallese V, Buccino G, Mazziotta JC, Rizzolatti G (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3(3):e79.  https://doi.org/10.1371/journal.pbio.0030079 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Ikeda H, Blake R, Watanabe K (2005) Eccentric perception of biological motion is unscalably poor. Vision Res 45(15):1935–1943CrossRefPubMedGoogle Scholar
  37. Insch PM, Bull R, Phillips LH, Allen R, Slessor G (2012) Adult aging, processing style, and the perception of biological motion. Exp Aging Res 38(2):169–185.  https://doi.org/10.1080/0361073X.2012.660030 CrossRefPubMedGoogle Scholar
  38. Johansson G (1973) Visual perception of biological motion and a model for its analysis. Percept Psychophys 14:195–204CrossRefGoogle Scholar
  39. Levi DM, Klein SA, Aitsebaomo AP (1985) Vernier acuity, crowding and cortical magnification. Vision Res 25(7):963–977CrossRefPubMedGoogle Scholar
  40. Levi DM, McGraw PV, Klein SA (2000) Vernier and contrast discrimination in central and peripheral vision. Vision Res 40(8):973–988CrossRefPubMedGoogle Scholar
  41. MacLeod C, Mathews A, Tata P (1986) Attentional bias in emotional disorders. J Abnorm Psychol 95(1):15–20CrossRefPubMedGoogle Scholar
  42. Manera V, Schouten B, Becchio C, Bara BG, Verfaillie K (2010) Inferring intentions from biological motion: a stimulus set of point-light communicative interactions. Behav Res Methods 42(1):168–178.  https://doi.org/10.3758/BRM.42.1.168 CrossRefPubMedGoogle Scholar
  43. Mather G, Radford K, West S (1999). Low-level processing of biological motion. Proc Royal Soc London Ser B 249:149–155CrossRefGoogle Scholar
  44. Mathews A, MacLeod C (1985) Selective processing of threat cues in anxiety states. Behav Res Ther 23(5):563–569CrossRefPubMedGoogle Scholar
  45. McNair NA, Goodbourn PT, Shone LT, Harris IM (2017) Summary statistics in the attentional blink. Atten Percept Psychophys 79(1):100–116.  https://doi.org/10.3758/s13414-016-1216-2 CrossRefPubMedGoogle Scholar
  46. Miller JE, Carlson LA, McAuley JD (2013) When what you hear influences when you see: listening to an auditory rhythm influences the temporal allocation of visual attention. Psychol Sci 24(1):11–18CrossRefPubMedGoogle Scholar
  47. Neri P, Morrone MC, Burr DC (1998) Seeing biological motion. Nature 395(6705):894–896CrossRefPubMedGoogle Scholar
  48. Pan J, Zhang J, Ma P, Liang H, Wang H, Tao J, Wen S, Zhang J (2006) The utility of Liebowitz Social Anxiety Scale in the patients with social anxiety disorder in Chinese. Chin J Nerv Ment Dis 32(3):206–210Google Scholar
  49. Pavlova MA (2011) Biological motion processing as a hallmark of social cognition. Cereb Cortex 22(5):981–995 doi:bhr156[pii]10.1093/cercor/bhr156CrossRefPubMedGoogle Scholar
  50. Pavlova MA, Sokolov AN, Bidet-Ildei C (2014). Sex differences in the neuromagnetic cortical response to biological motion. Cereb Cortex. doi:bhu175[pii]10.1093/cercor/bhu175Google Scholar
  51. Pell DG, Cavanagh P, Desimone R, Tjan B, Treisman A (2007) Crowding: including illusory conjunctions, surround suppression, and attention. J Vis 7(2):1CrossRefPubMedGoogle Scholar
  52. Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10(4):437–442CrossRefPubMedGoogle Scholar
  53. Piazza EA, Sweeny TD, Wessel D, Silver MA, Whitney D (2013) Human use summary statistics to perceive auditory sequences. Psychol Sci 24(8):1389–1397CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pollick FE, Kay JW, Heim K, Stringer R (2005) Gender recognition from point-light walkers. J Exp Psychol Hum Percept Perform 31(6):1247–1265. doi:2005-15838-006[pii]10.1037/0096-1523.31.6.1247CrossRefPubMedGoogle Scholar
  55. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192.  https://doi.org/10.1146/annurev.neuro.27.070203.144230 CrossRefPubMedGoogle Scholar
  56. Rizzolatti G, Fabbri-Destro M (2010) Mirror neurons: from discovery to autism. Exp Brain Res 200(3–4):223–237.  https://doi.org/10.1007/s00221-009-2002-3 CrossRefPubMedGoogle Scholar
  57. Rytwinski NK, Fresco DM, Heimberg RG, Coles ME, Liebowitz MR, Cissell S, Hofmann SG (2009) Screening for social anxiety disorder with the self-report version of the Liebowitz Social Anxiety Scale. Depress Anxiety 26(1):34–38.  https://doi.org/10.1002/da.20503 CrossRefPubMedGoogle Scholar
  58. Safren SA, Heimberg RG, Horner KJ, Juster HR, Schneier FR, Liebowitz MR (1999) Factor structure of social fears: the Liebowitz Social Anxiety Scale. J Anxiety Disord 13(3):253–270CrossRefPubMedGoogle Scholar
  59. Schouten B, Troje NF, Brooks A, van der Zwan R, Verfaillie K (2010) The facing bias in biological motion perception: effects of stimulus gender and observer sex. Atten Percept Psychophys 72(5):1256–1260.  https://doi.org/10.3758/APP.72.5.1256 CrossRefPubMedGoogle Scholar
  60. Schouten B, Troje NF, Verfaillie K (2011) The facing bias in biological motion perception: structure, kinematics, and body parts. Atten Percept Psychophys 73(1):130–143.  https://doi.org/10.3758/s13414-010-0018-1 CrossRefPubMedGoogle Scholar
  61. Shim W, Alvarez G, Jiang Y (2008) Spatial separation between targets constraints maintenance of attention on multiple objects. Psychon Bull Rev 15(2):390–397CrossRefPubMedPubMedCentralGoogle Scholar
  62. Singer N, Eapen M, Grillon C, Ungerleider LG, Hendler T (2012) Through the eyes of anxiety: Dissecting threat bias via emotional-binocular rivalry. Emotion 12(5):960–969.  https://doi.org/10.1037/a0027070 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Thornton IM, Rensink RA, Shiffrar M (2002) Active versus passive processing of biological motion. Perception 31(7):837–853CrossRefPubMedGoogle Scholar
  64. Troje NF, Westhoff C (2006) The inversion effect in biological motion perception: evidence for a “life detector”? Curr Biol 16(8):821–824. doi:S0960-9822(06)01281-4[pii]10.1016/j.cub.2006.03.022CrossRefPubMedGoogle Scholar
  65. Van de Cruys S, Schouten B, Wagemans J (2013) An anxiety-induced bias in the perception of a bistable point-light walker. Acta Psychol (Amst) 144(3):548–553. doi:S0001-6918(13)00215-1[pii]10.1016/j.actpsy.2013.09.010CrossRefGoogle Scholar
  66. Vanrie J, Verfaillie K (2004) Perception of biological motion: a stimulus set of human point-light actions. Behav Res Methods Instrum Comput 36(4):625–629CrossRefPubMedGoogle Scholar
  67. Walker D, Vul E (2014) Hierarchical encoding makes individuals in a group seem more attractive. Psychol Sci 25(1):230–235CrossRefPubMedGoogle Scholar
  68. Weech S, McAdam M, Troje NF (2014) What causes the facing-the-viewer bias in biological motion? JVis 14:1–15Google Scholar
  69. Westheimer G (1982) The spatial grain of the perifoveal visual field. Vision Res 22(1):157–162CrossRefPubMedGoogle Scholar
  70. Whitney D, Levi DM (2011) Visual crowding: a fundamental limit on conscious perception and object recognition. Trends Cogn Sci 15(4):160–168.  https://doi.org/10.1016/j.tics.2011.02.005 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yiltiz H, Chen L (2015) Tactile input and empathy modulate the perception of ambiguous biological motion. Front Psychol 6:161.  https://doi.org/10.3389/fpsyg.2015.00161 PubMedPubMedCentralGoogle Scholar
  72. Ying HJ, Xu H (2017). Rapid sequential visual presentation and ensemble coding in facial expression adaptation. J Vi 17(15).  https://doi.org/10.1167/1117.1161.1115

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PsychologyNew York UniversityNew YorkUSA
  2. 2.School of Psychological and Cognitive Sciences and Beijing Key Laboratory of Behavior and Mental HealthPeking UniversityBeijingChina
  3. 3.Key Laboratory of Machine Perception (Ministry of Education)Peking UniversityBeijingChina

Personalised recommendations