Evidence for a role of synchrony but not common fate in the perception of biological group movements.

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  • Author(s): Cracco E;Cracco E; Papeo L; Papeo L; Wiersema JR; Wiersema JR
  • Source:
    The European journal of neuroscience [Eur J Neurosci] 2024 Jul; Vol. 60 (1), pp. 3557-3571. Date of Electronic Publication: 2024 May 06.
  • Publication Type:
    Journal Article
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Wiley-Blackwell Country of Publication: France NLM ID: 8918110 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1460-9568 (Electronic) Linking ISSN: 0953816X NLM ISO Abbreviation: Eur J Neurosci Subsets: MEDLINE
    • Publication Information:
      Publication: : Oxford : Wiley-Blackwell
      Original Publication: Oxford, UK : Published on behalf of the European Neuroscience Association by Oxford University Press, c1989-
    • Subject Terms:
    • Abstract:
      Extensive research has shown that observers are able to efficiently extract summary information from groups of people. However, little is known about the cues that determine whether multiple people are represented as a social group or as independent individuals. Initial research on this topic has primarily focused on the role of static cues. Here, we instead investigate the role of dynamic cues. In two experiments with male and female human participants, we use EEG frequency tagging to investigate the influence of two fundamental Gestalt principles - synchrony and common fate - on the grouping of biological movements. In Experiment 1, we find that brain responses coupled to four point-light figures walking together are enhanced when they move in sync vs. out of sync, but only when they are presented upright. In contrast, we found no effect of movement direction (i.e., common fate). In Experiment 2, we rule out that synchrony takes precedence over common fate by replicating the null effect of movement direction while keeping synchrony constant. These results suggest that synchrony plays an important role in the processing of biological group movements. In contrast, the role of common fate is less clear and will require further research.
      (© 2024 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)
    • References:
      Abassi, E., & Papeo, L. (2020). The representation of two‐body shapes in the human visual cortex. The Journal of Neuroscience, 40(4), 852–863. https://doi.org/10.1523/JNEUROSCI.1378-19.2019.
      Abassi, E., & Papeo, L. (2022). Behavioral and neural markers of visual configural processing in social scene perception. NeuroImage, 260, 119506. https://doi.org/10.1016/j.neuroimage.2022.119506.
      Adibpour, P., Hochmann, J.‐R., & Papeo, L. (2021). Spatial relations trigger visual binding of people. Journal of Cognitive Neuroscience, 33(7), 1343–1353. https://doi.org/10.1162/jocn_a_01724.
      Alp, N., Nikolaev, A. R., Wagemans, J., & Kogo, N. (2017). EEG frequency tagging dissociates between neural processing of motion synchrony and human quality of multiple point‐light dancers. Scientific Reports, 7(August 2016), Article August 2016. https://doi.org/10.1038/srep44012, 7, 44012.
      Anderson, L. C., Bolling, D. Z., Schelinski, S., Coffman, M. C., Pelphrey, K. A., & Kaiser, M. D. (2013). Sex differences in the development of brain mechanisms for processing biological motion. NeuroImage, 83, 751–760. https://doi.org/10.1016/j.neuroimage.2013.07.040.
      Bellot, E., Abassi, E., & Papeo, L. (2021). Moving toward versus away from another: How body motion direction changes the representation of bodies and actions in the visual cortex. Cerebral Cortex, 31(5), 2670–2685. https://doi.org/10.1093/cercor/bhaa382.
      Blake, R., & Shiffrar, M. (2007). Perception of human motion. Annual Review of Psychology, 58, 47–73. https://doi.org/10.1146/annurev.psych.57.102904.190152.
      Braddick, O. J., O'Brien, J. M. D., Wattam‐Bell, J., Atkinson, J., Hartley, T., & Turner, R. (2001). Brain areas sensitive to coherent visual motion. Perception, 30(1), 61–72. https://doi.org/10.1068/p3048.
      Caspers, S., Zilles, K., Laird, A. R., & Eickhoff, S. B. (2010). ALE meta‐analysis of action observation and imitation in the human brain. NeuroImage, 50(3), 1148–1167. https://doi.org/10.1016/j.neuroimage.2009.12.112.
      Cheng, Y., Liu, W., Yuan, X., & Jiang, Y. (2022). Following other People's footsteps: A contextual‐attraction effect induced by biological motion. Psychological Science, 33(9), 1522–1531. https://doi.org/10.1177/09567976221091211.
      Cracco, E., Bernardet, U., Sevenhant, R., Vandenhouwe, N., Copman, F., Durnez, W., Bombeke, K., & Brass, M. (2022). Evidence for a two‐step model of social group influence. iScience, 25(9), 104891. https://doi.org/10.1016/j.isci.2022.104891.
      Cracco, E., & Brass, M. (2018). The role of sensorimotor processes in social group contagion. Cognitive Psychology, 103, 23–41. https://doi.org/10.1016/j.cogpsych.2018.02.001.
      Cracco, E., De Coster, L., Andres, M., & Brass, M. (2015). Motor simulation beyond the dyad: Automatic imitation of multiple actors. Journal of Experimental Psychology: Human Perception and Performance, 41(6), 1488–1501. https://doi.org/10.1037/a0039737.
      Cracco, E., De Coster, L., Andres, M., & Brass, M. (2016). Mirroring multiple agents: Motor resonance during action observation is modulated by the number of agents. Social Cognitive and Affective Neuroscience, 11(9), 1422–1427. https://doi.org/10.1093/scan/nsw059.
      Cracco, E., Keysers, C., Clauwaert, A., & Brass, M. (2019). Representing multiple observed actions in the motor system. Cerebral Cortex, 29(8), 3631–3641. https://doi.org/10.1093/cercor/bhy237.
      Cracco, E., Lee, H., van Belle, G., Quenon, L., Haggard, P., Rossion, B., & Orgs, G. (2022). EEG frequency tagging reveals the integration of form and motion cues into the perception of group movement. Cerebral Cortex, 32(13), 2843–2857. https://doi.org/10.1093/cercor/bhab385.
      Cracco, E., Linthout, T., & Orgs, G. (2023). The role of Objecthood and Animacy in apparent movement processing. Social Cognitive and Affective Neuroscience, ((1)nsad014. https://doi.org/10.1093/scan/nsad014.
      Cracco, E., Oomen, D., Papeo, L., & Wiersema, J. R. (2022). Using EEG movement tagging to isolate brain responses coupled to biological movements. Neuropsychologia, 177, 108395. https://doi.org/10.1016/j.neuropsychologia.2022.108395.
      Ding, X., Gao, Z., & Shen, M. (2017). Two equals one: Two human actions during social interaction are grouped as one unit in working memory. Psychological Science, 28(9), 1311–1320. https://doi.org/10.1177/0956797617707318.
      Elias, E., Dyer, M., & Sweeny, T. D. (2017). Ensemble perception of dynamic emotional groups. Psychological Science, 28(2), 193–203. https://doi.org/10.1177/0956797616678188.
      Federici, A., Parma, V., Vicovaro, M., Radassao, L., Casartelli, L., & Ronconi, L. (2020). Anomalous perception of biological motion in autism: A conceptual review and meta‐analysis. Scientific Reports, 10(1), 4576. https://doi.org/10.1038/s41598-020-61252-3.
      Giese, M. A., & Poggio, T. (2003). Neural mechanisms for the recognition of biological movements. Nature Reviews Neuroscience, 4(3), 179–192. https://doi.org/10.1038/nrn1057.
      Grosjean, M., Zwickel, J., & Prinz, W. (2009). Acting while perceiving: Assimilation precedes contrast. Psychological Research‐Psychologische Forschung, 73(1), 3–13. https://doi.org/10.1007/s00426-008-0146-6.
      Hafri, A., & Firestone, C. (2021). The perception of relations. Trends in Cognitive Sciences, 25(6), 475–492. https://doi.org/10.1016/j.tics.2021.01.006.
      Han, S. (2004). Interactions between proximity and similarity grouping: An event‐related brain potential study in humans. Neuroscience Letters, 367(1), 40–43. https://doi.org/10.1016/j.neulet.2004.05.098.
      Hoekstra, R. A., Bartels, M., Cath, D. C., & Boomsma, D. I. (2008). Factor structure, reliability and criterion validity of the autism‐Spectrum quotient (AQ): A study in Dutch population and patient groups. Journal of Autism and Developmental Disorders, 38(8), 1555–1566. https://doi.org/10.1007/s10803-008-0538-x.
      Ji, H., Yin, J., Huang, Y., & Ding, X. (2020). Selective attention operates on the group level for interactive biological motion. Journal of Experimental Psychology: Human Perception and Performance, 46(12), 1434–1442. https://doi.org/10.1037/xhp0000866.
      Kaiser, D., Quek, G. L., Cichy, R. M., & Peelen, M. V. (2019). Object vision in a structured world. Trends in Cognitive Sciences, 23(8), 672–685. https://doi.org/10.1016/j.tics.2019.04.013.
      Kim, J. G., & Biederman, I. (2011). Where do objects become scenes? Cerebral Cortex (New York, N.Y.: 1991), 21(8), 1738–1746. https://doi.org/10.1093/cercor/bhq240.
      Lakens, D. (2010). Movement synchrony and perceived entitativity. Journal of Experimental Social Psychology, 46(5), 701–708. https://doi.org/10.1016/j.jesp.2010.03.015.
      Lakens, D., & Stel, M. (2011). If they move in sync, they must feel in sync: Movement synchrony leads to attributions of rapport and Entitativity. Social Cognition, 29(1), 1–14. https://doi.org/10.1521/soco.2011.29.1.1.
      Lee, S.‐H., & Blake, R. (2001). Neural synergy in visual grouping: When good continuation meets common fate. Vision Research, 41(16), 2057–2064. https://doi.org/10.1016/S0042-6989(01)00086-4.
      Luck, S. J., & Gaspelin, N. (2017). How to get statistically significant effects in any ERP experiment (and why you shouldn't). Psychophysiology, 54(1), 146–157. https://doi.org/10.1111/psyp.12639.
      Morey, R. D. (2008). Confidence intervals from normalized data: A correction to Cousineau (2005). Tutorials in Quantitative Methods for Psychology, 4(2), 841–851. https://doi.org/10.3758/s13414-012-0291-2.
      Nguyen, T. T. N., Vuong, Q. C., Mather, G., & Thornton, I. M. (2021). Ensemble coding of crowd speed using biological motion. Attention, Perception, & Psychophysics, 83(3), 1014–1035. https://doi.org/10.3758/s13414-020-02163-3.
      Orgs, G., Bestmann, S., Schuur, F., & Haggard, P. (2011). From body form to biological motion: The apparent velocity of human movement biases subjective time. Psychological Science, 22(6), 712–717. https://doi.org/10.1177/0956797611406446.
      Orgs, G., Dovern, A., Hagura, N., Haggard, P., Fink, G. R., & Weiss, P. H. (2016). Constructing visual perception of body movement with the motor cortex. Cerebral Cortex, 26(1), 440–449. https://doi.org/10.1093/cercor/bhv262.
      Paparella, I., & Papeo, L. (2022). Chunking by social relationship in working memory. Visual Cognition, 30(5), 354–370. https://doi.org/10.1080/13506285.2022.2064950.
      Papeo, L. (2020). Twos in human visual perception. Cortex, 132, 473–478. https://doi.org/10.1016/j.cortex.2020.06.005.
      Papeo, L., Goupil, N., & Soto‐Faraco, S. (2019). Visual search for people among people. Psychological Science, 30(10), 1483–1496. https://doi.org/10.1177/0956797619867295.
      Papeo, L., Stein, T., & Soto‐Faraco, S. (2017). The two‐body inversion effect. Psychological Science, 28(3), 369–379. https://doi.org/10.1177/0956797616685769.
      Pavlova, M. A., Sokolov, A. N., & Bidet‐Ildei, C. (2015). Sex differences in the Neuromagnetic cortical response to biological motion. Cerebral Cortex, 25(10), 3468–3474. https://doi.org/10.1093/cercor/bhu175.
      Peirce, J., Gray, J. R., Simpson, S., MacAskill, M., Höchenberger, R., Sogo, H., Kastman, E., & Lindeløv, J. K. (2019). PsychoPy2: Experiments in behavior made easy. Behavior Research Methods, 51(1), 195–203. https://doi.org/10.3758/s13428-018-01193-y.
      Peterson, M. A., & Kimchi, R. (2013). Perceptual Organization in Vision. Oxford University Press. https://doi.org/10.1093/oxfordhb/9780195376746.013.0002.
      Pitcher, D., & Ungerleider, L. G. (2021). Evidence for a third visual pathway specialized for social perception. Trends in Cognitive Sciences, 25(2), 100–110. https://doi.org/10.1016/j.tics.2020.11.006.
      Reed, C. L., Stone, V. E., Bozova, S., & Tanaka, J. (2003). The body‐inversion effect. Psychological Science, 14(4), 302–308. https://doi.org/10.1111/1467-9280.14431.
      Rees, G., Friston, K., & Koch, C. (2000). A direct quantitative relationship between the functional properties of human and macaque V5. Nature Neuroscience, 3(7), 716–723. https://doi.org/10.1038/76673.
      Retter, T. L., & Rossion, B. (2016). Uncovering the neural magnitude and spatio‐temporal dynamics of natural image categorization in a fast visual stream. Neuropsychologia, 91, 9–28. https://doi.org/10.1016/j.neuropsychologia.2016.07.028.
      Retter, T. L., Rossion, B., & Schiltz, C. (2021). Harmonic amplitude summation for frequency‐tagging analysis. Journal of Cognitive Neuroscience, 33(11), 2372–2393. https://doi.org/10.1162/jocn_a_01763.
      Rina, A., Papanikolaou, A., Zong, X., Papageorgiou, D. T., Keliris, G. A., & Smirnakis, S. M. (2022). Visual motion coherence responses in human visual cortex. Frontiers in Neuroscience, 16, 719250. https://www.frontiersin.org/articles/10.3389/fnins.2022.719250.
      Roberts, K. L., & Humphreys, G. W. (2010). Action relationships concatenate representations of separate objects in the ventral visual system. NeuroImage, 52(4), 1541–1548. https://doi.org/10.1016/j.neuroimage.2010.05.044.
      Shiffrar, M., & Freyd, J. J. (1990). Apparent motion of the human body. Psychological Science, 1(4), 257–264. https://doi.org/10.1111/j.1467-9280.1990.tb00210.x.
      Stevens, J. A., Fonlupt, P., Shiffrar, M., & Decety, J. (2006). New aspects of motion perception: Selective neural encoding of apparent human movements. Neuroreport, 11(1), 109‐115.
      Sweeny, T. D., Haroz, S., & Whitney, D. (2013). Perceiving group behavior: Sensitive ensemble coding mechanisms for biological motion of human crowds. Journal of Experimental Psychology: Human Perception and Performance, 39(2), 329–337. https://doi.org/10.1037/a0028712.
      Sweeny, T. D., & Whitney, D. (2014). Perceiving crowd attention: Ensemble perception of a Crowd's gaze. Psychological Science, 25(10), 1903–1913. https://doi.org/10.1177/0956797614544510.
      Thurman, S. M., & Lu, H. (2014). Perception of social interactions for spatially scrambled biological motion. PLoS ONE, 9, e112539. https://doi.org/10.1371/journal.pone.0112539.
      Todorova, G. K., Hatton, R. E. M., & Pollick, F. E. (2019). Biological motion perception in autism spectrum disorder: A meta‐analysis. Molecular Autism, 10, 49. https://doi.org/10.1186/s13229-019-0299-8.
      Troje, N. F. (2002). Decomposing biological motion: A framework for analysis and synthesis of human gait patterns. Journal of Vision, 2(5), 2. https://doi.org/10.1167/2.5.2.
      Troje, N. F. (2008). Retrieving information from human movement patterns. In Understanding events: From perception to action (pp. 308–334). Oxford University Press. https://doi.org/10.1093/acprof:oso/9780195188370.003.0014.
      Tsantani, M., Yon, D., & Cook, R. (2022). Neural representations of observed interpersonal synchrony in the social perception network. PsyArXiv. https://doi.org/10.31234/osf.io/pjvke.
      Vanrie, J., Dekeyser, M., & Verfaillie, K. (2004). Bistability and biasing effects in the perception of ambiguous point‐light walkers. Perception, 33(5), 547–560. https://doi.org/10.1068/p5004.
      Vestner, T., Gray, K. L. H., & Cook, R. (2020). Why are social interactions found quickly in visual search tasks? Cognition, 200, 104270. https://doi.org/10.1016/j.cognition.2020.104270.
      Vestner, T., Over, H., Gray, K. L. H., & Cook, R. (2021). Objects that direct visuospatial attention produce the search advantage for facing dyads. Journal of Experimental Psychology: General., 151, 161–171. https://doi.org/10.1037/xge0001067.
      Vestner, T., Tipper, S. P., Hartley, T., Over, H., & Rueschemeyer, S.‐A. (2019). Bound together: Social binding leads to faster processing, spatial distortion, and enhanced memory of interacting partners. Journal of Experimental Psychology: General, 148(7), 1251–1268. https://doi.org/10.1037/xge0000545.
      Wagemans, J., Elder, J. H., Kubovy, M., Palmer, S. E., Peterson, M. A., Singh, M., & von der Heydt, R. (2012). A century of gestalt psychology in visual perception: I. Perceptual grouping and figure–ground organization. Psychological Bulletin, 138(6), 1172–1217. https://doi.org/10.1037/a0029333.
      Wagemans, J., Feldman, J., Gepshtein, S., Kimchi, R., Pomerantz, J. R., van der Helm, P. A., & van Leeuwen, C. (2012). A century of gestalt psychology in visual perception: II. Conceptual and theoretical foundations. Psychological Bulletin, 138(6), 1218–1252. https://doi.org/10.1037/a0029334.
      Whitney, D., & Leib, A. Y. (2018). Ensemble Perception. Annual Review of Psychology, 69, 105–129. https://doi.org/10.1146/annurev-psych-010416-044232.
      Wilson, S., & Gos, C. (2019). Perceiving social cohesion: Movement synchrony and task demands both matter. Perception, 48(4), 316–329. https://doi.org/10.1177/0301006619837878.
      Wilson, S., & Mansour, J. K. (2020). Collective directional movement and the perception of social cohesion. British Journal of Social Psychology, 59(4), 819–838. https://doi.org/10.1111/bjso.12361.
    • Grant Information:
      12U0322N Fonds Wetenschappelijk Onderzoek; (Project THEMPO-758473) European Research Council Grant
    • Contributed Indexing:
      Keywords: EEG frequency tagging; biological motion perception; gestalt perception; social grouping
    • Publication Date:
      Date Created: 20240506 Date Completed: 20240705 Latest Revision: 20240705
    • Publication Date:
      20240705
    • Accession Number:
      10.1111/ejn.16356
    • Accession Number:
      38706370