Emotional contagion to vocal smile revealed by combined pupil reactivity and motor resonance.
Emotional contagion
Motor resonance
Pupil reactivity
Vocal smile
fEMG
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
23 10 2024
23 10 2024
Historique:
received:
17
05
2024
accepted:
30
09
2024
medline:
24
10
2024
pubmed:
24
10
2024
entrez:
23
10
2024
Statut:
epublish
Résumé
The interplay between the different components of emotional contagion (i.e. emotional state and facial motor resonance), both during implicit and explicit appraisal of emotion, remains controversial. The aims of this study were (i) to distinguish between these components thanks to vocal smile processing and (ii) to assess how they reflect implicit processes and/or an explicit appraisal loop. Emotional contagion to subtle vocal emotions was studied in 25 adults through motor resonance and Autonomic Nervous System (ANS) reactivity. Facial expressions (fEMG: facial electromyography) and pupil dilation were assessed during the processing and judgement of artificially emotionally modified sentences. fEMG revealed that Zygomaticus major was reactive to the perceived valence of sounds, whereas the activity of Corrugator supercilii reflected explicit judgement. Timing analysis of pupil dilation provided further insight into both the emotional state and the implicit and explicit processing of vocal emotion, showing earlier activity for emotional stimuli than for neutral stimuli, followed by valence-dependent variations and a late judgement-dependent increase in pupil diameter. This innovative combination of different electrophysiological measures shed new light on the debate between central and peripherical views within the framework of emotional contagion.
Identifiants
pubmed: 39443497
doi: 10.1038/s41598-024-74848-w
pii: 10.1038/s41598-024-74848-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
25043Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-19-CE37-0022-01
Informations de copyright
© 2024. The Author(s).
Références
Hatfield, E., Cacioppo, J. T. & Rapson, R. L. Emotional Contagion (Cambridge University Press, 1993). https://doi.org/10.1017/CBO9781139174138
Premack, D. & Woodruff, G. Does the chimpanzee have a theory of mind? ISTEX. 1, 515–526 (1978).
Damasio, A. R. & Blanc, M. L’erreur De Descartes: La Raison Des émotions (O. Jacob, 1995).
Carsten, T., Desmet, C., Krebs, R. M. & Brass, M. Pupillary contagion is independent of the emotional expression of the face. Emot. Wash. DC. 19, 1343–1352 (2019).
Izard, C. E. The Face of Emotion. xii, 468 (Appleton-Century-Crofts, East Norwalk, CT, US, (1971).
Coles, N. A. et al. A multi-lab test of the facial feedback hypothesis by the many smiles collaboration. Nat. Hum. Behav. 6, 1731–1742 (2022).
pubmed: 36266452
doi: 10.1038/s41562-022-01458-9
Soussignan, R. Regulatory function of facial actions in emotion processes. In Advances in psychology research, Vol. 31, 173–198. (Nova Science Publishers, Hauppauge, NY, US, 2004).
James, W. What is an emotion? Mind. 9, 188–205 (1884).
doi: 10.1093/mind/os-IX.34.188
Cannon, W. B. The James-Lange theory of emotions: A critical examination and an alternative theory. Am. J. Psychol. 39, 106–124 (1927).
doi: 10.2307/1415404
Scherer, K. R. Appraisal considered as a process of multilevel sequential checking. In: Appraisal processes in emotion: Theory, methods, research. New York, NY, US: Oxford University Press; 2001. p. 92–120. (Series in affective science).
doi: 10.1093/oso/9780195130072.003.0005
Scherer, K. R. Emotions are emergent processes: they require a dynamic computational architecture. Philos. Trans. R Soc. B Biol. Sci. 364, 3459–3474 (2009).
doi: 10.1098/rstb.2009.0141
Hess, U. & Blairy, S. Facial mimicry and emotional contagion to dynamic emotional facial expressions and their influence on decoding accuracy. Int. J. Psychophysiol. 40, 129–141 (2001).
pubmed: 11165351
doi: 10.1016/S0167-8760(00)00161-6
Dimberg, U., Thunberg, M. & Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 11, 86–89 (2000).
pubmed: 11228851
doi: 10.1111/1467-9280.00221
Simpson, E. A., Murray, L., Paukner, A. & Ferrari, P. F. The mirror neuron system as revealed through neonatal imitation: Presence from birth, predictive power and evidence of plasticity. Philos. Trans. R. Soc. 369, 20130289 (2014).
doi: 10.1098/rstb.2013.0289
Burrows, A. M., Waller, B. M., Parr, L. A. & Bonar, C. J. Muscles of facial expression in the chimpanzee (Pan troglodytes): Descriptive, comparative and phylogenetic contexts. J. Anat. 208, 153–167 (2006).
pubmed: 16441560
pmcid: 2100197
doi: 10.1111/j.1469-7580.2006.00523.x
Olszanowski, M., Wróbel, M. & Hess, U. Mimicking and sharing emotions: A re-examination of the link between facial mimicry and emotional contagion. Cogn. Emot. 34, 367–376 (2020).
pubmed: 31072246
doi: 10.1080/02699931.2019.1611543
Rychlowska, M. et al. Functional smiles: tools for love, sympathy, and war. Psychol. Sci. 28, 1259–1270 (2017).
pubmed: 28741981
pmcid: 6056899
doi: 10.1177/0956797617706082
Shore, D. M. & Heerey, E. A. The value of genuine and polite smiles. Emotion. 11, 169–174 (2011).
pubmed: 21401236
doi: 10.1037/a0022601
Hess, U. & Bourgeois, P. You smile–I smile: Emotion expression in social interaction. Biol. Psychol. 84, 514–520 (2010).
pubmed: 19913071
doi: 10.1016/j.biopsycho.2009.11.001
Wood, A., Rychlowska, M., Korb, S. & Niedenthal, P. Fashioning the face: Sensorimotor simulation contributes to facial expression recognition. Trends Cogn. Sci. 20, 227–240 (2016).
pubmed: 26876363
doi: 10.1016/j.tics.2015.12.010
Ohala, J. J. The acoustic origin of the smile. J. Acoust. Soc. Am. 68, S33–S33 (1980).
doi: 10.1121/1.2004679
Aubergé, V. & Cathiard, M. Can we hear the prosody of smile? Speech Commun. 40, 87–97 (2003).
doi: 10.1016/S0167-6393(02)00077-8
Tartter, V. C. Happy talk: Perceptual and acoustic effects of smiling on speech. Percept. Psychophys. 27, 24–27 (1980).
pubmed: 7367197
doi: 10.3758/BF03199901
Tartter, V. C. & Braun, D. Hearing smiles and frowns in normal and whisper registers. J. Acoust. Soc. Am. 96, 2101–2107 (1994).
pubmed: 7963024
doi: 10.1121/1.410151
Ponsot, E., Arias, P. & Aucouturier, J. J. Uncovering mental representations of smiled speech using reverse correlation. J. Acoust. Soc. Am. 143, EL19–EL24 (2018).
pubmed: 29390775
doi: 10.1121/1.5020989
Bradley, M. M. & Lang, P. J. The international affective digitized sounds: affective ratings of sounds and instruction manual (Technical Report No. B-3). University of Florida. NIMH Cent. Study Emot. Atten. Gainesv. FL 30 (2007).
Hietanen, J. K., Surakka, V. & Linnankoski, I. Facial electromyographic responses to vocal affect expressions. Psychophysiology. 35, 530–536 (1998).
pubmed: 9715097
doi: 10.1017/S0048577298970445
Larsen, J. T., Norris, C. J. & Cacioppo, J. T. Effects of positive and negative affect on electromyographic activity over zygomaticus major and corrugator supercilii. Psychophysiology. 40, 776–785 (2003).
pubmed: 14696731
doi: 10.1111/1469-8986.00078
Verona, E., Patrick, C. J., Curtin, J. J., Bradley, M. M. & Lang, P. J. Psychopathy and physiological response to emotionally evocative sounds. J. Abnorm. Psychol. 113, 99–108 (2004).
pubmed: 14992662
doi: 10.1037/0021-843X.113.1.99
Dimberg, U., Thunberg, M. & Grunedal, S. Facial reactions to emotional stimuli: Automatically controlled emotional responses. Cogn. Emot. 16, 449–471 (2002).
doi: 10.1080/02699930143000356
Dimberg, U. & Thunberg, M. Rapid facial reactions to emotional facial expressions. Scand. J. Psychol. 39, 39–45 (1998).
pubmed: 9619131
doi: 10.1111/1467-9450.00054
Lindström, R. et al. Atypical perceptual and neural processing of emotional prosodic changes in children with autism spectrum disorders. Clin. Neurophysiol. 129, 2411–2420 (2018).
pubmed: 30278390
doi: 10.1016/j.clinph.2018.08.018
Arias, P., Belin, P. & Aucouturier, J. J. Auditory smiles trigger unconscious facial imitation. Curr. Biol. 28, R782–R783 (2018).
pubmed: 30040936
doi: 10.1016/j.cub.2018.05.084
Arias, P., Bellmann, C. & Aucouturier, J. J. Facial mimicry in the congenitally blind. Curr. Biol. 31, R1112–R1114 (2021).
pubmed: 34637708
doi: 10.1016/j.cub.2021.08.059
Babiker, A., Faye, I. & Malik, A. Pupillary behavior in positive and negative emotions. In IEEE International Conference on Signal and Image Processing Applications 379–383 (IEEE, Melaka, Malaysia, 2013) . https://doi.org/10.1109/ICSIPA.2013.6708037
Aston-Jones, G. & Cohen, J. D. An integrative theory of & locus coeruleus-norepinephrine function. Adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403–450 (2005).
Bradley, M. M., Miccoli, L., Escrig, M. A. & Lang, P. J. The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology. 45, 602–607 (2008).
pubmed: 18282202
pmcid: 3612940
doi: 10.1111/j.1469-8986.2008.00654.x
Aguillon-Hernandez, N. et al. The pupil: A window on social automatic processing in autism spectrum disorder children. J. Child. Psychol. Psychiatry 61, 768–778 (2020).
pubmed: 31823380
doi: 10.1111/jcpp.13170
Babiker, A., Faye, I., Prehn, K. & Malik, A. Machine Learning to differentiate between positive and negative emotions using pupil diameter. Front. Psychol. 6, (2015).
Beatty, J. Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychol. Bull. 91, 276–292 (1982).
pubmed: 7071262
doi: 10.1037/0033-2909.91.2.276
Hess, E. H. & Polt, J. M. Pupil size in relation to mental activity during simple problem-solving. Science 143, 1190–1192 (1964).
pubmed: 17833905
doi: 10.1126/science.143.3611.1190
Samuels, E. R. & Szabadi, E. Functional neuroanatomy of the noradrenergic locus Coeruleus: Its roles in the regulation of Arousal and autonomic function part II: Physiological and pharmacological manipulations and pathological alterations of Locus Coeruleus activity in humans. Curr. Neuropharmacol. 6, 254–285 (2008).
pubmed: 19506724
pmcid: 2687931
doi: 10.2174/157015908785777193
Prochazkova, E. & Kret, M. E. Connecting minds and sharing emotions through mimicry: A neurocognitive model of emotional contagion. Neurosci. Biobehav Rev. 80, 99–114 (2017).
pubmed: 28506927
doi: 10.1016/j.neubiorev.2017.05.013
Bradley, M. M., Codispoti, M., Cuthbert, B. N. & Lang, P. J. Emotion and motivation I: Defensive and appetitive reactions in picture processing. Emotion 1, 276–298 (2001).
pubmed: 12934687
doi: 10.1037/1528-3542.1.3.276
Geangu, E., Hauf, P., Bhardwaj, R. & Bentz, W. Infant pupil diameter changes in response to others’ positive and negative emotions. PLoS ONE. 6, e27132 (2011).
pubmed: 22110605
pmcid: 3217958
doi: 10.1371/journal.pone.0027132
Burley, D. T. & Daughters, K. The effect of oxytocin on pupil response to naturalistic dynamic facial expressions. Horm. Behav. 125, 104837 (2020).
pubmed: 32750332
doi: 10.1016/j.yhbeh.2020.104837
Aktar, E., Raijmakers, M. E. J. & Kret, M. E. Pupil mimicry in infants and parents. Cogn. Emot. 34, 1160–1170 (2020).
pubmed: 32116126
doi: 10.1080/02699931.2020.1732875
Legris, E. et al. Relationship between behavioral and objective measures of sound intensity in normal-hearing listeners and hearing-aid users: A pilot study. Brain Sci. 12, 392 (2022).
pubmed: 35326347
pmcid: 8946736
doi: 10.3390/brainsci12030392
Cherng, Y. G., Baird, T., Chen, J. T. & Wang, C. A. Background luminance effects on pupil size associated with emotion and saccade preparation. Sci. Rep. 10, 15718 (2020).
pubmed: 32973283
pmcid: 7515892
doi: 10.1038/s41598-020-72954-z
Zekveld, A. A., Koelewijn, T. & Kramer, S. E. The pupil dilation response to auditory stimuli: Current state of knowledge. Trends Hear. 22, 233121651877717 (2018).
Cosme, G. et al. Pupil dilation reflects the authenticity of received nonverbal vocalizations. Sci. Rep. 11, 1–14 (2021).
doi: 10.1038/s41598-021-83070-x
Jin, A. B., Steding, L. H. & Webb, A. K. Reduced emotional and cardiovascular reactivity to emotionally evocative stimuli in major depressive disorder. Int. J. Psychophysiol. 97, 66–74 (2015).
pubmed: 25931112
doi: 10.1016/j.ijpsycho.2015.04.014
Partala, T. & Surakka, V. Pupil size variation as an indication of affective processing. Int. J. Hum. Comput Stud. 59, 185–198 (2003).
doi: 10.1016/S1071-5819(03)00017-X
Jürgens, R., Fischer, J. & Schacht, A. Hot speech and exploding bombs: Autonomic arousal during emotion classification of prosodic utterances and affective sounds. Front. Psychol. 9, (2018).
Lewis, M. B. The interactions between botulinum-toxin-based facial treatments and embodied emotions. Sci. Rep. 8, 14720 (2018).
pubmed: 30283017
pmcid: 6170457
doi: 10.1038/s41598-018-33119-1
Vilaverde, R. F. et al. Inhibiting orofacial mimicry affects authenticity perception in vocal emotions. Emotion. 24 (6), 1376–1385 (2024).
pubmed: 38512197
doi: 10.1037/emo0001361
Calder, A. J., Keane, J., Cole, J., Campbell, R. & Young, A. W. Facial expression recognition by people with mobius syndrome. Cogn. Neuropsychol. 17, 73–87 (2000).
pubmed: 20945172
doi: 10.1080/026432900380490
Rives Bogart, K. & Matsumoto, D. Facial mimicry is not necessary to recognize emotion: Facial expression recognition by people with Moebius syndrome. Soc. Neurosci. 5, 241–251 (2010).
pubmed: 19882440
doi: 10.1080/17470910903395692
Bate, S., Cook, S. J., Mole, J. & Cole, J. First report of generalized face processing difficulties in möbius sequence. PloS One. 8, e62656 (2013).
pubmed: 23638131
pmcid: 3634771
doi: 10.1371/journal.pone.0062656
Bullack, A., Büdenbender, N., Roden, I. & Kreutz, G. Psychophysiological responses to happy and sad MusicA replication study. Music Percept. 35, 502–517 (2018).
doi: 10.1525/mp.2018.35.4.502
Ferencova, N., Visnovcova, Z., Bona Olexova, L. & Tonhajzerova, I. Eye pupil – a window into central autonomic regulation via emotional/cognitive processing. Physiol. Res. 70, S669–S682 (2021).
pubmed: 35199551
pmcid: 9054187
doi: 10.33549/physiolres.934749
Oliva, M. & Anikin, A. Pupil dilation reflects the time course of emotion recognition in human vocalizations. Sci. Rep. 8, 4871 (2018).
pubmed: 29559673
pmcid: 5861097
doi: 10.1038/s41598-018-23265-x
van der Wel, P. & van Steenbergen, H. Pupil dilation as an index of effort in cognitive control tasks: A review. Psychon. Bull. Rev. 25, 2005–2015 (2018).
pubmed: 29435963
pmcid: 6267528
doi: 10.3758/s13423-018-1432-y
Zekveld, A. A., Heslenfeld, D. J., Johnsrude, I. S., Versfeld, N. J. & Kramer, S. E. The eye as a window to the listening brain: neural correlates of pupil size as a measure of cognitive listening load. NeuroImage. 101, 76–86 (2014).
pubmed: 24999040
doi: 10.1016/j.neuroimage.2014.06.069
Kuchinke, L., Schneider, D., Kotz, S. A. & Jacobs, A. M. Spontaneous but not explicit processing of positive sentences impaired in Asperger’s syndrome: Pupillometric evidence. Neuropsychologia 49, 331–338 (2011).
pubmed: 21195104
doi: 10.1016/j.neuropsychologia.2010.12.026
Tereshenko, V. et al. Axonal mapping of the motor cranial nerves. Front. Neuroanat. 17, (2023).
Soussignan, R. Duchenne smile, emotional experience, and autonomic reactivity: A test of the facial feedback hypothesis. Emot. Wash. DC 2, 52–74 (2002).
Porges, S. W. The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system. Cleve Clin. J. Med. 76, S86–S90 (2009).
pubmed: 19376991
pmcid: 3108032
doi: 10.3949/ccjm.76.s2.17
Sorinas, J., Ferrández, J. M. & Fernandez, E. Brain and body emotional responses: Multimodal approximation for valence classification. Sensors 20, 313 (2020).
pubmed: 31935909
pmcid: 6982758
doi: 10.3390/s20010313
Chartrand, T. L. & Bargh, J. A. The chameleon effect: The perception–behavior link and social interaction. J. Personal. Soc. Psychol. 76, 893–910 (1999).
doi: 10.1037/0022-3514.76.6.893
Beall, P. M., Moody, E. J., McIntosh, D. N., Hepburn, S. L. & Reed, C. L. Rapid facial reactions to emotional facial expressions in typically developing children and children with autism spectrum disorder. J. Exp. Child. Psychol. 101, 206–223 (2008).
pubmed: 18561942
doi: 10.1016/j.jecp.2008.04.004
McIntosh, D. N., Reichmann-Decker, A., Winkielman, P. & Wilbarger, J. L. When the social mirror breaks: Deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. Dev. Sci. 9, 295–302 (2006).
pubmed: 16669800
doi: 10.1111/j.1467-7687.2006.00492.x
Vrana, S. R. & Gross, D. Reactions to facial expressions: Effects of social context and speech anxiety on responses to neutral, anger, and joy expressions. Biol. Psychol. 66, 63–78 (2004).
pubmed: 15019171
doi: 10.1016/j.biopsycho.2003.07.004
Rymarczyk, K., Biele, C., Grabowska, A. & Majczynski, H. EMG activity in response to static and dynamic facial expressions. Int. J. Psychophysiol. 79, 330–333 (2011).
pubmed: 21074582
doi: 10.1016/j.ijpsycho.2010.11.001
Sato, W., Fujimura, T. & Suzuki, N. Enhanced facial EMG activity in response to dynamic facial expressions. Int. J. Psychophysiol. 70, 70–74 (2008).
pubmed: 18598725
doi: 10.1016/j.ijpsycho.2008.06.001
Bufo, M. R. et al. Autonomic tone in children and adults: Pupillary, electrodermal and cardiac activity at rest. Int. J. Psychophysiol. 180, 68–78 (2022).
pubmed: 35914548
doi: 10.1016/j.ijpsycho.2022.07.009
Ricou, C., Rabadan, V., Mofid, Y., Aguillon-Hernandez, N. & Wardak, C. Pupil dilation reflects the social and motion content of faces. Soc. Cognit. Affect. Neurosci. 19, nsae055 (2024).
doi: 10.1093/scan/nsae055
Baron-Cohen, S. & Wheelwright, S. The empathy quotient: An investigation of adults with asperger syndrome or high functioning autism, and normal sex differences. J. Autism Dev. Disord 34, 163–175 (2004).
pubmed: 15162935
doi: 10.1023/B:JADD.0000022607.19833.00
Russ, J. B., Gur, R. C. & Bilker, W. B. Validation of affective and neutral sentence content for prosodic testing. Behav. Res. Methods. 40, 935–939 (2008).
pubmed: 19001384
pmcid: 8042646
doi: 10.3758/BRM.40.4.935
Boersma, P. Praat, a system for doing phonetics by computer. Glot Int. 5, 341–345 (2002).
Fridlund, A. J. & Cacioppo, J. T. Guidelines for human electromyographic research. Psychophysiology. 23, 567–589 (1986).
pubmed: 3809364
doi: 10.1111/j.1469-8986.1986.tb00676.x
Steinhauer, S. R., Bradley, M. M., Siegle, G. J., Roecklein, K. A. & Dix, A. Publication guidelines and recommendations for pupillary measurement in psychophysiological studies. Psychophysiology. 59, e14035 (2022).
pubmed: 35318693
pmcid: 9272460
doi: 10.1111/psyp.14035
Kret, M. E. & Sjak-Shie, E. E. Preprocessing pupil size data: Guidelines and code. Behav. Res. Methods 51, 1336–1342 (2019).
pubmed: 29992408
doi: 10.3758/s13428-018-1075-y
Nyström, M. & Holmqvist, K. An adaptive algorithm for fixation, saccade, and glissade detection in eyetracking data. Behav. Res. Methods. 42, 188–204 (2010).
pubmed: 20160299
doi: 10.3758/BRM.42.1.188
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).
Team, R. Boston, MA,. RStudio: Integrated Development for R. in RStudio, PBC (2020).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-, 2016).
Lawrence, M. A. Ez: Easy Analysis and Visualization of Factorial Experiments. (2016).
Wickham, H. et al. Welcome to the Tidyverse. J. Open. Source Softw. 4, 1686 (2019).
doi: 10.21105/joss.01686
Wickham, H., François, R., Henry, L. & Müller, K. Dplyr: A Grammar of Data Manipulation. (2021).
Voeten, C. C. Permutes: Permutation Tests for Time Series Data. (2022).
Guthrie, D. & Buchwald, J. S. Significance testing of difference potentials. Psychophysiology. 28, 240–244 (1991).
pubmed: 1946890
doi: 10.1111/j.1469-8986.1991.tb00417.x
Gramfort, A. et al. MNE software for processing MEG and EEG data. NeuroImage. 86, 446–460 (2014).
pubmed: 24161808
doi: 10.1016/j.neuroimage.2013.10.027
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: tests in Linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).
doi: 10.18637/jss.v082.i13