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Experimental Brain Research

, Volume 234, Issue 9, pp 2677–2686 | Cite as

Repeated exposure to vicarious pain alters electrocortical processing of pain expressions

  • Michel-Pierre Coll
  • Mathieu Grégoire
  • Kenneth M. Prkachin
  • Philip L. JacksonEmail author
Research Article

Abstract

Repeated exposure to others in pain has been shown to bias vicarious pain perception, but the neural correlates of this effect are currently not known. The current study therefore aimed at measuring electrocortical responses to facial expressions of pain following exposure to expressions of pain. To this end, a between-subject design was adopted. Participants in the Exposure group were exposed to facial expressions of intense pain, while the participants in the Control group were exposed to neutral expressions before performing the same pain detection task. As in previous studies, participants in the Exposure group showed a significantly more conservative bias when judging facial expressions pain, meaning that they were less inclined to judge moderate pain expressions as painful compared to participants in the Control group. Event-related potential analyses in response to pain or neutral expressions indicated that this effect was related to a relative decrease in the central late positive potential responses to pain expressions. Furthermore, while the early N170 response was not influenced by repeated exposure to pain expressions, the P100 component showed an adaptation effect in the Control group only. These results suggest that repeated exposure to vicarious pain do not influence early event-related potential responses to pain expressions but decreases the late central positive potential. These results are discussed in terms of changes in the perceived saliency of pain expressions following repeated exposure.

Keywords

Facial expression Vicarious pain Event-related potential Late positive potential 

Notes

Acknowledgments

The authors would like to thank Pierre-Emmanuel Michon and Sophie Blais-Michaud for their technical assistance and Fanny Eugène for revision of the manuscript. M.P. Coll was funded by a Canadian Institutes of Health Research (CIHR) graduate scholarship and M. Grégoire by a Fonds de recherche du QuébecSanté (FRQ-S) graduate scholarship. P. L. Jackson was supported by salary grants from the CIHR and the FRQ-S. This research was funded by a CIHR grant to P. L. Jackson and K. M. Prkachin.

Compliance with ethical standards

Conflict of interest

Authors declare no conflict of interest.

Ethical approval

All procedures performed in this study were approved by the Institut de réadaptation en déficience physique de Québec research ethics committee and were in accordance with the 1964 Helsinki Declaration and its later amendments.

References

  1. Amihai I, Deouell LY, Bentin S (2011) Neural adaptation is related to face repetition irrespective of identity: a reappraisal of the N170 effect. Exp Brain Res 209:193–204. doi: 10.1007/s00221-011-2546-x CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bentin S, Allison T, Puce A et al (1996) Electrophysiological studies of face perception in humans. J Cogn Neurosci 8:551–565. doi: 10.1162/jocn.1996.8.6.551 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chen C, Yang C-Y, Cheng Y (2012) Sensorimotor resonance is an outcome but not a platform to anticipating harm to others. Soc Neurosci 7:578–590. doi: 10.1080/17470919.2012.686924 CrossRefPubMedGoogle Scholar
  4. Choinière M, Melzack R, Girard N et al (1990) Comparisons between patients’ and nurses’ assessment of pain and medication efficacy in severe burn injuries. Pain 40:143–152. doi: 10.1016/0304-3959(90)90065-L CrossRefPubMedGoogle Scholar
  5. Codispoti M, Ferrari V, Bradley MM (2006) Repetitive picture processing: autonomic and cortical correlates. Brain Res 1068:213–220. doi: 10.1016/j.brainres.2005.11.009 CrossRefPubMedGoogle Scholar
  6. Codispoti M, Ferrari V, Bradley MM (2007) Repetition and event-related potentials: distinguishing early and late processes in affective picture perception. J Cogn Neurosci 19:577–586. doi: 10.1162/jocn.2007.19.4.577 CrossRefPubMedGoogle Scholar
  7. Coll M-P, Grégoire M, Latimer M et al (2011) Perception of pain in others: implication for caregivers. Pain Manag 1:257–265. doi: 10.2217/pmt.11.21 CrossRefPubMedGoogle Scholar
  8. Craig KD, Prkachin KM, Grunau RVE (2010) The facial expression of pain. In: Turk D, Melzack R (eds) Handbook of pain assessment, 3rd edn. Guilford Press, New York, pp 117–133Google Scholar
  9. De Wied M, Verbaten MN (2001) Affective pictures processing, attention, and pain tolerance. Pain 90:163–172. doi: 10.1016/S0304-3959(00)00400-0 CrossRefPubMedGoogle Scholar
  10. Decety J, Yang CY, Cheng Y (2010) Physicians down-regulate their pain empathy response: an event-related brain potential study. Neuroimage 50:1676–1682. doi: 10.1016/j.neuroimage.2010.01.025 CrossRefPubMedGoogle Scholar
  11. Delorme A, Makeig S (2004) EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. doi: 10.1016/j.jneumeth.2003.10.009 CrossRefPubMedGoogle Scholar
  12. Dittmar O, Baum C, Schneider R, Lautenbacher S (2015) Effects of context and individual predispositions on hypervigilance to pain-cues: an ERP study. J Pain Res 8:507–521. doi: 10.2147/JPR.S80990 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Eimer M (2011) The face-sensitive N170 component of the event-related brain potential. In: Calder A, Rhodes G, Johnson M, Haxby J (eds) The Oxford handbook of face perception. Oxford Univ Press, New York, pp 329–344Google Scholar
  14. Ekman P, Friesen WV (1978) Facial action coding system. Consulting Psychologists Press, Palo AltoGoogle Scholar
  15.  Godinho F, Magnin M, Frot M et al (2006) Emotional modulation of pain: is it the sensation or what we recall? J Neurosci 26:11454–11461. doi: 10.1523/JNEUROSCI.2260-06.2006 CrossRefPubMedGoogle Scholar
  16. González-Roldan AM, Martínez-Jauand M, Muñoz-García MA et al (2011) Temporal dissociation in the brain processing of pain and anger faces with different intensities of emotional expression. Pain 152:853–859. doi: 10.1016/j.pain.2010.12.037 CrossRefPubMedGoogle Scholar
  17. Grier JB (1971) Nonparametric indexes for sensitivity and bias: computing formulas. Psychol Bull 75:424–429. doi: 10.1037/h0031246 CrossRefPubMedGoogle Scholar
  18. Hadjistavropoulos T, Craig KD, Duck S et al (2011) A biopsychosocial formulation of pain communication. Psychol Bull 137:910–939. doi: 10.1037/a0023876 CrossRefPubMedGoogle Scholar
  19. Hajcak G, MacNamara A, Olvet DM (2010) Event-related potentials, emotion, and emotion regulation: an integrative review. Dev Neuropsychol 35:129–155. doi: 10.1080/87565640903526504 CrossRefPubMedGoogle Scholar
  20. Hajcak G, Weinberg A, MacNamara A, Foti D (2012) ERPs and the study of emotion. In: Luck SJ, Kappenman ES (eds) The Oxford handbook of event-related potential components. Oxford Univ Press, New York, pp 441–474Google Scholar
  21. Hillyard SA, Vogel EK, Luck SJ (1998) Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. Philos Trans R Soc Lond B Biol Sci 353:1257–1270. doi: 10.1098/rstb.1998.0281 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Iafrati NS (1986) Pain on the burn unit: patient versus nurse perceptions. J Burn Care Rehabil 7:413–416CrossRefPubMedGoogle Scholar
  23. Kappesser J, Williams ACDC, Prkachin KM (2006) Testing two accounts of pain underestimation. Pain 124:109–116. doi: 10.1016/j.pain.2006.04.003 CrossRefPubMedGoogle Scholar
  24. Kloth N, Schweinberger SR, Kovács G (2010) Neural correlates of generic versus gender-specific face adaptation. J Cogn Neurosci 22:2345–2356. doi: 10.1162/jocn.2009.21329 CrossRefPubMedGoogle Scholar
  25. Kovács G, Zimmer M, Bankó E et al (2006) Electrophysiological correlates of visual adaptation to faces and body parts in humans. Cereb Cortex 16:742–753. doi: 10.1093/cercor/bhj020 CrossRefPubMedGoogle Scholar
  26. Kunz M, Mylius V, Schepelmann K, Lautenbacher S (2004) On the relationship between self-report and facial expression of pain. J Pain 5:368–376. doi: 10.1016/j.jpain.2004.06.002 CrossRefPubMedGoogle Scholar
  27. Lautenbacher S, Dittmar O, Baum C et al (2013) Vigilance for pain-related faces in a primary task paradigm: an ERP study. J Pain Res 6:437–447. doi: 10.2147/JPR.S45097 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lopez-Calderon J, Luck SJ (2014) ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci 8:213. doi: 10.3389/fnhum.2014.00213 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lucey P, Cohn JF, Prkachin KM et al (2011) Painful data: The UNBC-McMaster shoulder pain expression archive database. IEEE Int Conf Autom Face Gesture Recognit Work FG 2011:57–64. doi: 10.1109/FG.2011.5771462 Google Scholar
  30. Mason DJ (1981) An investigation of the influences of selected factors on nurses’ inferences of patient suffering. Int J Nurs Stud 18:251–259. doi: 10.1016/0020-7489(81)90038-9 CrossRefPubMedGoogle Scholar
  31. Olofsson JK, Polich J (2007) Affective visual event-related potentials: arousal, repetition, and time-on-task. Biol Psychol 75:101–108. doi: 10.1016/j.biopsycho.2006.12.006 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pollack I, Norman DA (1964) A non-parametric analysis of recognition experiments. Psychon Sci 1:125–126CrossRefGoogle Scholar
  33. Pourtois G, Grandjean D, Sander D, Vuilleumier P (2004) Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cereb Cortex 14:619–633. doi: 10.1093/cercor/bhh023 CrossRefPubMedGoogle Scholar
  34. Pourtois G, Vuilleumier P (2006) Dynamics of emotional effects on spatial attention in the human visual cortex. Prog Brain Res 156:67–91. doi:  10.1016/S0079-6123(06)56004-2 CrossRefPubMedGoogle Scholar
  35. Preis MA, Kroner-Herwig B, Schmidt-Samoa C et al (2015) Neural correlates of empathy with pain show habituation effects. An fMRI study. PLoS One 10:1–19. doi: 10.1371/journal.pone.0137056 CrossRefGoogle Scholar
  36. Priebe JA, Messingschlager M, Lautenbacher S (2015) Gaze behaviour when monitoring pain faces: an eye-tracking study. Eur J Pain (United Kingdom) 19:817–825. doi: 10.1002/ejp.608 CrossRefGoogle Scholar
  37. Prkachin KM (1992) The consistency of facial expressions of pain: a comparison across modalities. Pain 51:297–306. doi: 10.1016/0304-3959(92)90213-U CrossRefPubMedGoogle Scholar
  38. Prkachin KM, Rocha EM (2010) High levels of vicarious exposure bias pain judgments. J Pain 11:904–909. doi: 10.1016/j.jpain.2009.12.015 CrossRefPubMedGoogle Scholar
  39. Prkachin KM, Solomon PE (2008) The structure, reliability and validity of pain expression: evidence from patients with shoulder pain. Pain 139:267–274. doi: 10.1016/j.pain.2008.04.010 CrossRefPubMedGoogle Scholar
  40. Prkachin KM, Berzins S, Mercer SR (1994) Encoding and decoding of pain expressions: a judgement study. Pain 58:253–259. doi: 10.1016/0304-3959(94)90206-2 CrossRefPubMedGoogle Scholar
  41. Prkachin KM, Mass H, Mercer SR (2004) Effects of exposure on perception of pain expression. Pain 111:8–12. doi: 10.1016/j.pain.2004.03.027 CrossRefPubMedGoogle Scholar
  42. Prkachin KM, Rash JA. The index of facial pain expression (IFPE) manual. http://psyc.ucalgary.ca/ifpe/e/. Accessed 6 May 2016
  43. Prkachin KM, Solomon PE, Ross J (2007) Underestimation of pain by health-care providers: towards a model of the process of inferring pain in others. Can J Nurs Res 39:88–106PubMedGoogle Scholar
  44. Prkachin KM, Kaseweter KA, Browne ME (2015) Understanding the suffering of others: the sources and consequences of third-person pain. In: Pickering G, Gibson S (eds) Pain, emotion and cognition. Springer International Publishing, Switzerland, pp 53–72Google Scholar
  45. Reicherts P, Wieser MJ, Gerdes ABM et al (2012) Electrocortical evidence for preferential processing of dynamic pain expressions compared to other emotional expressions. Pain 153:1959–1964. doi: 10.1016/j.pain.2012.06.017 CrossRefPubMedGoogle Scholar
  46. Richards A, Holmes A, Pell PJ, Bethell EJ (2013) Adapting effects of emotional expression in anxiety: evidence for an enhanced late positive potential. Soc Neurosci 8:650–664. doi: 10.1080/17470919.2013.854273 CrossRefPubMedGoogle Scholar
  47. Santos A, Mier D, Kirsch P, Meyer-Lindenberg A (2011) Evidence for a general face salience signal in human amygdala. Neuroimage 54:3111–3116. doi: 10.1016/j.neuroimage.2010.11.024 CrossRefPubMedGoogle Scholar
  48. Solomon P (2001) Congruence between health professionals’ and patients’ pain ratings: a review of the literature. Scand J Caring Sci 15:174–180. doi: 10.1046/j.1471-6712.2001.00027.x CrossRefPubMedGoogle Scholar
  49. Wieser MJ, Gerdes ABM, Greiner R et al (2012) Tonic pain grabs attention, but leaves the processing of facial expressions intact-Evidence from event-related brain potentials. Biol Psychol 90:242–248. doi: 10.1016/j.biopsycho.2012.03.019 CrossRefPubMedGoogle Scholar
  50. Wieser MJ, Gerdes ABM, Büngel I et al (2014a) Not so harmless anymore: how context impacts the perception and electrocortical processing of neutral faces. Neuroimage 92:74–82. doi: 10.1016/j.neuroimage.2014.01.022 CrossRefPubMedGoogle Scholar
  51. Wieser MJ, Gerdes ABM, Reicherts P, Pauli P (2014b) Mutual influences of pain and emotional face processing. Front Psychol 5:1160. doi: 10.3389/fpsyg.2014.01160 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Williams AC de C (2002) Facial expression of pain, empathy, evolution, and social learning. Behav Brain Sci. 25:439–488PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Michel-Pierre Coll
    • 1
    • 2
    • 3
  • Mathieu Grégoire
    • 1
    • 2
    • 3
  • Kenneth M. Prkachin
    • 4
  • Philip L. Jackson
    • 1
    • 2
    • 3
    Email author
  1. 1.Faculté des sciences sociales, École de psychologie, Pavillon Félix-Antoine-SavardUniversité LavalQuebec CityCanada
  2. 2.Centre interdisciplinaire de recherche en réadaptation et intégration socialeQuebec CityCanada
  3. 3.Centre de recherche de l’Institut universitaire en santé mentale de QuébecQuebec CityCanada
  4. 4.Department of PsychologyUniversity of Northern British ColumbiaPrince GeorgeCanada

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