The effect of emotional information from eyes on empathy for pain: A subliminal ERP study

Autoři: Juan Song aff001;  Yanqiu Wei aff001;  Han Ke aff002
Působiště autorů: Key Research Base of Humanities and Social Sciences of the Ministry of Education, Academy of Psychology and Behavior, Faculty of Psychology, Tianjin Normal University, Tianjin, China aff001;  Psychology, School of Social Science, Nanyang Technological University, Singapore aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226211


Facial expressions are deeply tied to empathy, which plays an important role during social communication. The eye region is effective at conveying facial expressions, especially fear and sadness emotions. Further, it was proved that subliminal stimuli could impact human behavior. This research aimed to explore the effect of subliminal sad, fearful and neutral emotions conveyed by the eye region on a viewer’s empathy for pain using event-related potentials (ERP). The experiment used an emotional priming paradigm of 3 (prime: subliminal neutral, sad, fear eye region information) × 2 (target: painful, nonpainful pictures) within-subject design. Participants were told to judge whether the targets were in pain or not. Results showed that the subliminal sad eye stimulus elicited a larger P2 amplitude than the subliminal fearful eye stimulus when assessing pain. For P3 and late positive component (LPC), the amplitude elicited by the painful pictures was larger than the amplitude elicited by the nonpainful pictures. The behavioral results demonstrated that people reacted to targets depicting pain more slowly after the sad emotion priming. Moreover, the subjective ratings of Personal Distress (PD) (one of the dimensions in Chinese version of Interpersonal Reactivity Index scale) predicted the pain effect in empathic neural responses in the N1 and N2 time window. The current study showed that subliminal eye emotion affected the viewer’s empathy for pain. Compared with the subliminal fearful eye stimulus, the subliminal sad eye stimulus had a greater impact on empathy for pain. The perceptual level of pain was deeper in the late controlled processing stage.

Klíčová slova:

Behavior – Emotions – Event-related potentials – Eyes – Face – Fear – Prosocial behavior – Priming (psychology)


1. Decety J, Jackson PL (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews 3: 71–100. doi: 10.1177/1534582304267187 15537986

2. Gladstein GA (1983). Understanding empathy: integrating counseling, developmental, and social psychology perspectives. Journal of Counseling Psychology 4: 467–482. doi: 10.1037/0022-0167.30.4.467

3. Davis MH (1983). Measuring individual differences in empathy: evidence for a multidimensional approach. Journal of Personality & Social Psychology 1: 113–126. doi: 10.1037/0022-3514.44.1.113

4. Zaki J, Ochsner K (2012). The neuroscience of empathy: progress, pitfalls and promise. Nature Neuroscience 15: 675–680. doi: 10.1038/nn.3085 22504346

5. Cameron CD., Spring VL., Todd AR (2017). The empathy impulse: a multinomial model of intentional and unintentional empathy for pain. Emotion 17: 395–411. doi: 10.1037/emo0000266 28080083

6. Ma Y, Wang C, Han S (2011). Neural responses to perceived pain in others predict real-life monetary donations in different socioeconomic contexts. Neuroimage 57: 1273–1280. doi: 10.1016/j.neuroimage.2011.05.003 21596143

7. Singer T, Lamm C (2009). The social neuroscience of empathy. Annals of the New York Academy of Sciences 1156: 81–96. doi: 10.1111/j.1749-6632.2009.04418.x 19338504

8. Yan Z, Su Y (2017). Evolution in research topics on empathy: Evidence from Bibliometrics (in Chinese). Psychological Science (Chin Ver) 3: 699–707.

9. Cheng J, Jiao C, Luo Y, Cui F (2017). Music induced happy mood suppresses the neural responses to other's pain: evidences from an ERP study. Scientific Reports 7. doi: 10.1038/s41598-017-13386-0 29026123

10. Danziger N, Faillenot I, Peyron R (2009). Can we share a pain we never felt? neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 2: 203–212. doi: 10.1016/j.neuron.2008.11.023 19186163

11. Chiesa PA., Liuzza MT., Macaluso E, Aglioti SM (2017). Brain activity induced by implicit processing of others’ pain and pleasure. Human Brain Mapping 11: 5562–5576. doi: 10.1002/hbm.23749 28833833

12. Lee TH., Qu Y, Telzer EH (2017). Love flows downstream: mothers' and children's neural representation similarity in perceiving distress of self and family. Social Cognitive and Affective Neuroscience 12: 1916–1927. doi: 10.1093/scan/nsx125 29069521

13. Ye H (2016). The significances of mirror neurons (in Chinese). Acta Psychologica Sinica. (Chin Ver) 4: 444–456. doi: 10.3724/SP.J.1041.2016.00444

14. Yamada M, Decety J (2009). Unconscious affective processing and empathy: An investigation of subliminal priming on the detection of painful facial expressions. Pain 143: 71–75. doi: 10.1016/j.pain.2009.01.028 19254825

15. Wang L, Fu S, Feng C, Luo W, Zhu X, Luo Y (2012). The neural processing of fearful faces without attention and consciousness: an event-related potential study. Neuroscience Letters 506: 317–321. doi: 10.1016/j.neulet.2011.11.034 22155093

16. Choi D, Nishimura T, Motoi M, Egashira Y, Matsumoto R, and Watanuki S (2014). Effect of empathy trait on attention to various facial expressions: evidence from N170 and late positive potential (LPP). Journal of Physiological Anthropology 33: 18. doi: 10.1186/1880-6805-33-18 24975115

17. Gu L, Bai X (2014). Visual preference of facial expressions in children and adults: Evidence from eye movements (in Chinese). Journal of Psychological Science (Chin Ver) 37: 101–105

18. Elsenbarth H, and Alpers GW (2011). Happy mouth and sad eyes: scanning emotional facial expressions. Emotion 11: 860–865. doi: 10.1037/a0022758 21859204

19. Fox E, Damjanovic L (2006). The eyes are sufficient to produce a threat superiority effect. Emotion 3: 534–539. doi: 10.1037/1528-3542.6.3.534 16938095

20. Qiao J (1989). The function of the emotions’ type and intensity in the facial expression discrimination (in Chinese). Journal of Psychological Science (Chin Ver) 9–14.

21. Montgomery CB., Allison C, Lai MC., Cassidy S, Langdon PE., and Baron-Cohen S (2016). Do adults with high functioning autism or asperger syndrome differ in empathy and emotion recognition? Journal of Autism and Developmental Disorders 6: 1931–1940. doi: 10.1007/s10803-016-2698-4 26883645

22. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, and Plumb I (2001). The “reading the mind in the eyes” test revised version: a study with normal adults, and adults with asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry 42: 241–251. doi: 10.1111/1469-7610.00715 11280420

23. Luo Y, Zhang S, Tao R, Geng H (2016). The power of subliminal and supraliminal eye contact on social decision making: an individual-difference perspective. Consciousness and Cognition 40: 131–140. doi: 10.1016/j.concog.2016.01.001 26821242

24. Li S, Li P, Wang W, Zhu X, and Luo W (2017). The effect of emotionally valenced eye region images on visuocortical processing of surprised faces. Psychophysiology 55: e13039. doi: 10.1111/psyp.13039 29239478

25. Itier RJ, & Batty M (2009). Neural bases of eye and gaze processing: The core of social cognition. Neuroscience and Biobehavioral Reviews, 6: 843–863. doi: 10.1016/j.neubiorev.2009.02.004 19428496

26. Meng J, Hu L, Shen L, Yang Z, Chen H, Huang X, Jackson T (2012). Emotional primes modulate the responses to others’ pain: an ERP study. Exp. Brain. Res. 220: 277–286. doi: 10.1007/s00221-012-3136-2 22695721

27. Li, A (2013). Anger expression and fear expression impact on empathy for pain. (Master’s thesis). Southwest University.

28. Fan Y, Han S (2008). Temporal dynamic of neural mechanisms involved in empathy for pain: An event-related brain potential study. Neuropsychologia 46: 160–173. doi: 10.1016/j.neuropsychologia.2007.07.023 17825852

29. Han X, Luo S, Han S (2015). Embodied neural responses to others’ suffering. Cognitive Neuroscience 1–4: 114–127. doi: 10.1080/17588928.2015.1053440 26111085

30. Jiao C, Wang T, Peng X, Cui F (2017). Impaired empathy processing in individuals with internet addiction disorder: an Event-Related Potential study. Frontiers in Human Neuroscience 498. doi: 10.3389/fnhum.2017.00498 29085290

31. Song J, Wei Y, Du M, Xie H, Lian T, Hu Y, et al. (2019). Effect of eye emotional information on pain empathy: An ERP study (in Chinese). Studies of psychology and behavior (Chin Ver) 2: 326–332.

32. Grassini S, Holm SK, Railo H, Koivisto M (2016). Who is afraid of the invisible snake? Subjective visual awareness modulates posterior brain activity for evolutionarily threatening stimuli. Biological Psychology 121: 53–61. doi: 10.1016/j.biopsycho.2016.10.007 27760371

33. Nomura M, Ohira H, Haneda K, Iidaka T, Sadato N, Okada T, Yonekura Y (2004). Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. NeuroImage 21: 352–363. doi: 10.1016/j.neuroimage.2003.09.021 14741673

34. Suslow T, Konrad C, Kugel H, Rumstadt D, Zwitserlood P, Schöning S, et al. (2010). Automatic mood-congruent amygdala responses to masked facial expressions in major depression. Biol. Psychiatry 67: 155–160. doi: 10.1016/j.biopsych.2009.07.023 19748075

35. Gendolla GHE., Silvestrini N (2011). Smiles make it easier and so do frowns: masked affective stimuli influence mental effort. Emotion 11: 320–328. doi: 10.1037/a0022593 21500901

36. Yang J, Xu X, Du X, Shi C, Fang F (2011). Effects of unconscious processing on implicit memory for fearful faces. PLOS ONE 6: e14641. doi: 10.1371/journal.pone.0014641 21408105

37. Xu Q, Jiang Y (2012). Unconscious processing of emotional faces and its probable neural mechanism (in Chinese). Chinese Science Bulletin (Chin Ver) 57: 3358–3366.

38. Neumeister P, Feldker K, Heitmann CY, Buff C, Brinkmann L, Bruchmann M, Straube T (2017). Specific amygdala response to masked fearful faces in post-traumatic stress relative to other anxiety disorders. Psychological Medicine 48: 1209–1217. doi: 10.1017/S0033291717002513 28950918

39. Tsushima Y, Sasaki Y, Watanabe T (2006). Greater disruption due to failure of inhibitory control on an ambiguous distractor. Science 314: 1786–1788. doi: 10.1126/science.1133197 17170308

40. Ibáñez A, Hurtado E, Lobos A, Escobar J, Trujillo N, Baez S, et al. (2011). Subliminal presentation of other faces (but not own face) primes behavioral and evoked cortical processing of empathy for pain. Brain Research 72–85. doi: 10.1016/j.brainres.2011.05.014 21624566

41. Decety J, Sommerville JA (2003). Shared representations between self and other: a social cognitive neuroscience view. Trends in cognitive science 7: 527–533. doi: 10.1016/j.tics.2003.10.004 14643368

42. Bin KW, Cho JH. (2017). Encoding of discriminative fear memory by input-specific LTP in the amygdala. Neuron 95: 1129. doi: 10.1016/j.neuron.2017.08.004 28823727

43. Conty L, George N, Hietanen JK (2016). Watching eyes effects: when others meet the self. Consciousness and Cognition 45: 184–197. doi: 10.1016/j.concog.2016.08.016 27639066

44. Delplanque S, Lavoie ME., Hot P, Silvert L, Sequeira H (2004). Modulation of cognitive processing by emotional valence studied through event-related potentials in humans. Neuroscience Letters 356: 1–4. doi: 10.1016/j.neulet.2003.10.014 14746887

45. Sheng F, Liu Y, Zhou B, Zhou W, Han S (2013). Oxytocin modulates the racial bias in neural responses to others’ suffering. Biological Psychology 92: 380–386. doi: 10.1016/j.biopsycho.2012.11.018 23246533

46. Gong X, Huang Y, Wang Y, Luo Y (2011). Revision of the Chinese facial affective pictures system (in Chinese). Chinese Mental Health Journal (Chin Ver). 25: 40–46.

47. Wang Y, Song J, Guo F, Zhang Z, Yuan S, Stephanie C (2016). Spatiotemporal brain dynamics of empathy for pain and happiness in friendship. Frontiers in Behavioral Neuroscience 10: 45. doi: 10.3389/fnbeh.2016.00045 27065822

48. Song J, et al. (2016). Interpersonal distance influences on pain empathy: Friends priming effect (in Chinese). Acta Psychologica Sinica (Chin Ver) 48: 833–844.

49. Zhang F, Dong Y, Wang K, Zhan Z, Xie L (2010). Reliability and validity of the Chinese version of the Interpersonal Reactivity Index-C (in Chinese). Chinese Journal of Clinical Psychology 18: 155–157. doi: 10.3969/j.issn.1005-9202.2014.20.130

50. Trumpp NM, Traub F, Kiefer M (2013). Masked priming of conceptual features reveals differential brain activation during unconscious access to conceptual action and sound information, PLOS ONE 8 (5): e65910. doi: 10.1371/journal.pone.0065910 23741518

51. Trumpp NM, Traub F, Pulvermuller F, Kiefer M (2014). Unconscious automatic brain activation of acoustic and action-related conceptual features during masked repetition priming. Journal of Cognitive Neuroscience 26: 352–364. doi: 10.1162/jocn_a_00473 24001008

52. Luo W, Feng W, He W, Wang N, Luo Y (2010). Three stages of facial expression processing: ERP study with rapid serial visual presentation. Neuroimage 49: 1857–1867. doi: 10.1016/j.neuroimage.2009.09.018 19770052

53. Mu Y, Han S (2013). Neural oscillations dissociate between self-related attentional orientation versus evaluation. Neuroimage 67: 247–256. doi: 10.1016/j.neuroimage.2012.11.016 23194818

54. Stoerig P (2006). The impact of invisible stimuli. Science 314: 1694–1695. doi: 10.1126/science.1136956 17170285

55. Zhang X, Pang Z, Jiang Y, Zhang M, Jiang Y (2018). Access to awareness is improved by affective learning (in Chinese). Acta Psychologica Sinica (Chin Ver) 3: 253–259. doi: 10.3724/SP.J.1041.2018.00253

56. Sheng F, Han S (2012). Manipulations of cognitive strategies and intergroup relationships reduce the racial bias in empathic neural responses. NeuroImage 61: 786–797. doi: 10.1016/j.neuroimage.2012.04.028 22542636

57. Kahan TA (2000). Negative priming from masked words: Retrospective prime clarification or center-surround inhibition? Journal of Experimental Psychology: Learning, Memory, and Cognition. 26(6): 1392–1410. doi: 10.1037//0278-7393.26.6.1392 11185772

58. Liu T, Pinheiro A, Zhao Z, Nestor PG, McCarley RW, Niznikiewicz MA (2012). Emotional cues during simultaneous face and voice processing: electrophysiological insights. PLOS ONE 7: e31001. doi: 10.1371/journal.pone.0031001 22383987

59. Carretié L, Martín-loeches M, Hinojosa J, Mercado F (2001). Emotion and attention interaction studied through event-related potentials. Journal of Cognitive Neuroscience 13: 1109–1128. doi: 10.1162/089892901753294400 11784449

60. Xu M, Li Z, Ding C, Zhang J, Fan L, Diao L, Yang D (2015). The divergent effects of fear and disgust on Inhibitory control: an ERP study. PLOS ONE 10: e0128932. doi: 10.1371/journal.pone.0128932 26030871

61. Buffone AEK., Poulin M, Delury S, Ministero L, Morrisson C, Scalo M (2017). Don’t walk in her shoes! Different forms of perspective taking affect stress physiology. Journal of Experimental Social Psychology 72: 161–168. doi: 10.1016/j.jesp.2017.04.001

62. Li S, Li P, Wang W, He W, Luo W (2017). The neural mechanisms of the processing of facial expressions based on cues from eye region (in Chinese). Advances in Psychological Science (Chin Ver) 2: 221–229.

63. Ren Y, Hao F (2018). The influence of emotional perception and interpersonal distance on altruistic option (in Chinese). Studies of psychology and behavior (Chin Ver) 16: 321–326.

64. Luo S, Han X, Na D, Han S (2017). Physical coldness enhances racial in-group bias in empathy: electrophysiological evidence. Neuropsychologia 116: 117–125. doi: 10.1016/j.neuropsychologia.2017.05.002 28478242

65. Balconi M, Lucchiai C (2005). In the face of emotions: Event-Related Potentials in supraliminal and subliminal facial expression recognition. Genetic, Social, and General Psychology Monographs 131: 41–69. doi: 10.3200/MONO.131.1.41-69 16482783

66. Preston SD., De Waal FBM. (2002). Empathy: its ultimate and proximate bases. Behavioral and Brain Sciences 25: 1–20. doi: 10.1017/s0140525x02000018 12625087

67. Gallese V (2003). The roots of empathy: the shared manifold hypothesis and the neural basis of intersubjectivity. Psychopathology 36: 171–180. doi: 10.1159/000072786 14504450

68. Lamm C, Nusbaum HC, Meltzoff AN, Decety J (2007). What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLOS ONE 2: e1292. doi: 10.1371/journal.pone.0001292 18091986

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2019 Číslo 12