Convergence of physiological responses to pain during face-to-face interaction.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
16 01 2020
16 01 2020
Historique:
received:
10
01
2019
accepted:
30
12
2019
entrez:
18
1
2020
pubmed:
18
1
2020
medline:
18
11
2020
Statut:
epublish
Résumé
Empathy with another's pain is an important social glue for maintaining interpersonal relationships. In most previous studies investigating the sharing of pain, a signal conveying a painful experience is presented by a target ("sender") as a stimulus to a participant ("receiver"), and the emotional/physiological responses of the participant are measured. However, this unilateral "sender-receiver" paradigm does not adequately address the possible bidirectional experience of shared pain accruing from interaction. Our aim was therefore to investigate the bidirectional effects of sharing pain in social settings. Thirty-six unfamiliar pairs were simultaneously and repeatedly exposed to the same pain-provoking (thermal) stimuli, either in a face-to-face or a "shielded" condition where a partition prevented the partner's responses from being fully observed. We recorded the blood volume pulse of each participant to measure the acute sympathetic response while a pair of participants experienced the stimuli simultaneously. The results revealed that participants with weaker reactions elevated their physiological reactivity to the stimulus in accordance with their partner's reactions in the face-to-face condition. The pair-level physiological similarity was also higher compared to the shielded condition. Such a low-to-high physiological convergence may underlie the collective elevation of pain expressions, which is often observed in interactive settings.
Identifiants
pubmed: 31949248
doi: 10.1038/s41598-019-57375-x
pii: 10.1038/s41598-019-57375-x
pmc: PMC6965106
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
450Références
Merskey, H. & Bogduk N. Classification of chronic pain. Part III: Pain terms, a current list with definitions and notes on usage. 2nd Edition, IASP task force on taxonomy. 209–214 (IASP Press, 1994).
Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science. 303(5661), 1157–1162 (2004).
doi: 10.1126/science.1093535
Jackson, P. L., Meltzoff, A. N. & Decety, J. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage. 24(3), 771–779 (2005).
doi: 10.1016/j.neuroimage.2004.09.006
Preston, S. D. & De Waal, F. B. Empathy: Its ultimate and proximate bases. Behav Brain Sci. 25(1), 1–20 (2002).
doi: 10.1017/S0140525X02000018
De Waal, F. B. Putting the altruism back into altruism: the evolution of empathy. Annu. Rev. Psychol. 59, 279–300 (2008).
doi: 10.1146/annurev.psych.59.103006.093625
Singer, T. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature. 439(7075), 466 (2006).
doi: 10.1038/nature04271
Lamm, C., Meltzoff, A. N. & Decety, J. How do we empathize with someone who is not like us? A functional magnetic resonance imaging study. J. Cogn. Neurosci. 22(2), 362–376 (2010).
doi: 10.1162/jocn.2009.21186
Perry, A., Bentin, S., Bartal, I. B. A., Lamm, C. & Decety, J. “Feeling” the pain of those who are different from us: Modulation of EEG in the mu/alpha range. Cogn Affect Behav Neurosci. 10(4), 493–504 (2010).
doi: 10.3758/CABN.10.4.493
Decety, J., Yang, C. Y. & Cheng, Y. Physicians down-regulate their pain empathy response: an event-related brain potential study. Neuroimage. 50(4), 1676–1682 (2010).
doi: 10.1016/j.neuroimage.2010.01.025
Schilbach, L. et al. Toward a second-person neuroscience. Behav Brain Sci. 36(4), 393–414 (2013).
doi: 10.1017/S0140525X12000660
Schilbach, L. Eye to eye, face to face and brain to brain: Novel approaches to study the behavioral dynamics and neural mechanisms of social interactions. Curr Opin Behav Sci. 3, 130–135 (2015).
doi: 10.1016/j.cobeha.2015.03.006
Langford, D. J. et al. Social modulation of pain as evidence for empathy in mice. Science. 312(5782), 1967–1970 (2006).
doi: 10.1126/science.1128322
Martin, L. J. et al. Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Curr Biol. 25(3), 326–332 (2015).
doi: 10.1016/j.cub.2014.11.028
James, W. Principles of Psychology (Holt, New York, 1890). James, W. Principles of Psychology (Holt, New York, 1890).
Laird, J. D. & Lacasse, K. Bodily influences on emotional feelings: Accumulating evidence and extensions of William James’s theory of emotion. Emot Rev. 6(1), 27–34 (2013).
doi: 10.1177/1754073913494899
Ooishi, Y. & Kashino, M. Habituation of rapid sympathetic response to aversive timbre eliminated by change in basal sympathovagal balance. Psychophysiology. 49(8), 1059–1071 (2012).
pubmed: 22646525
Awad, A. et al. Different responses of ear and finger pulse oximeter wave form to cold pressor test. Anesth Analg. 92(6), 1483–1486 (2001).
doi: 10.1097/00000539-200106000-00026
Chalacheva, P. et al. Biophysical markers of the peripheral vasoconstriction response to pain in sickle cell disease. PloS one. 12(5), e0178353 (2017).
doi: 10.1371/journal.pone.0178353
Bates, D. M., Mäechler, M., Bolker, B. & Walker, S. “Fitting Linear Mixed-Effects Models Using lme4.”. J Stat Softw. 67(1), 1–48 (2015).
Dimberg, U., Thunberg, M. & Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol Sci. 11(1), 86–89 (2000).
doi: 10.1111/1467-9280.00221
Harrison, N. A., Singer, T., Rotshtein, P., Dolan, R. J. & Critchley, H. D. Pupillary contagion: central mechanisms engaged in sadness processing. Soc Cogn Affect Neurosci. 1(1), 5–17 (2006).
doi: 10.1093/scan/nsl006
Hofman, D., Bos, P. A., Schutter, D. J. & van Honk, J. Fairness modulates non-conscious facial mimicry in women. Proc Biol Sci. 279(1742), 3535–3539 (2012).
doi: 10.1098/rspb.2012.0694
Murata, A., Saito, H., Schug, J., Ogawa, K. & Kameda, T. Spontaneous facial mimicry is enhanced by the goal of inferring emotional states: evidence for moderation of “automatic” mimicry by higher cognitive processes. PloS one. 11(4), e0153128 (2016).
doi: 10.1371/journal.pone.0153128
Saarela, M. V. et al. The compassionate brain: humans detect intensity of pain from another’s face. Cereb Cortex. 17(1), 230–237 (2006).
doi: 10.1093/cercor/bhj141
Wakabayashi, A., Tojo, Y., Baron-Cohen, S. & Wheelwright, S. The Autism-Spectrum Quotient (AQ) Japanese version: evidence from high-functioning clinical group and normal adults. Shinrigaku kenkyu. 75(1), 78–84 (2004).
doi: 10.4992/jjpsy.75.78
Davis, M. H. Measuring individual differences in empathy: Evidence for a multidimensional approach. J Pers Soc Psychol. 44(1), 113 (1983).
doi: 10.1037/0022-3514.44.1.113
Craig, K. D. Social communication of pain enhances protective functions: a comment on Deyo, Prkachin and Mercer 2004. Pain. 107, 5–6 (2004).
doi: 10.1016/S0304-3959(03)00264-1
Olsson, A. & Phelps, E. A. Social learning of fear. Nat Neurosci. 10(9), 1095 (2007).
doi: 10.1038/nn1968
Coan, J. A., Schaefer, H. S. & Davidson, R. J. Lending a hand: Social regulation of the neural response to threat. Psychol Sci. 17(12), 1032–1039 (2006).
doi: 10.1111/j.1467-9280.2006.01832.x
Goldstein, P., Weissman-Fogel, I. & Shamay-Tsoory, S. G. The role of touch in regulating inter-partner physiological coupling during empathy for pain. Sci Rep. 7(1), 3252 (2017).
doi: 10.1038/s41598-017-03627-7
Dawson, G. et al. Early social attention impairments in autism: social orienting, joint attention, and attention to distress. Dev Psychol. 40((2)), 271 (2004).
doi: 10.1037/0012-1649.40.2.271
Klin, A., Jones, W., Schultz, R., Volkmar, F. & Cohen, D. Defining and quantifying the social phenotype in autism. Am J Psychiatry. 159(6), 895–908 (2002).
doi: 10.1176/appi.ajp.159.6.895
Spezio, M. L., Adolphs, R., Hurley, R. S. & Piven, J. Analysis of face gaze in autism using “Bubbles”. Neuropsychologia. 45(1), 144–151 (2007).
doi: 10.1016/j.neuropsychologia.2006.04.027
von dem Hagen, E. A. & Bright, N. High autistic trait individuals do not modulate gaze behaviour in response to social presence but look away more when actively engaged in an interaction. Autism Res. 10(2), 359–368 (2017).
doi: 10.1002/aur.1666
Kameda, T. & Nakanishi, D. Cost-benefit analysis of social/cultural learning in a non-stationary uncertain environment: An evolutionary simulation and an experiment with human subjects. Evol Hum Behav. 23, 373–393 (2002).
doi: 10.1016/S1090-5138(02)00101-0
Kameda, T. & Nakanishi, D. Does social/cultural learning increase human adaptability? Rogers’ question revisited. Evol Hum Behav. 24, 242–260 (2003).
doi: 10.1016/S1090-5138(03)00015-1
Laland, K. N. Social learning strategies. Learn Behav. 32(1), 4–14 (2004).
doi: 10.3758/BF03196002
Prkachin, K. M. The consistency of facial expressions of pain: a comparison across modalities. Pain. 51(3), 297–306 (1992).
doi: 10.1016/0304-3959(92)90213-U
Ellermeier, W. & Westphal, W. Gender differences in pain ratings and pupil reactions to painful pressure stimuli. Pain. 61(3), 435–439 (1995).
doi: 10.1016/0304-3959(94)00203-Q
Ellrich, J., Bromm, B. & Hopf, H. C. Pain-evoked blink reflex. Muscle Nerve. 20(3), 265–270 (1997).
doi: 10.1002/(SICI)1097-4598(199703)20:3<265::AID-MUS1>3.0.CO;2-9
Lofland, J. Protest: Studies of collective behaviour and social movements. (Routledge 2017).
LeBon, G. The Crowd: A Study of the Popular Mind. (Cherokee Publishing Company, 1982, Original work published 1895).
Vierck, C. J., Mauderli, A. P. & Riley, J. L. III. Relationships between the intensity and duration of Peltier heat stimulation and pain magnitude. Exp. Brain Res. 225(3), 339–348 (2013).
doi: 10.1007/s00221-012-3375-2
Thorson, K. R., West, T. V. & Mendes, W. B. Measuring physiological influence in dyads: A guide to designing, implementing, and analyzing dyadic physiological studies. Psychol Methods. 23(4), 595 (2018).
doi: 10.1037/met0000166