Abstract
Previous event-related potential (ERP) and brain imaging studies have suggested observer responses to others’ pain are modulated by various bottom-up and top-down factors, including emotional primes. However, the temporal dynamics underlying the impact of emotional primes on responses to others’ pain remains poorly understood. In the present study, we explored effects of negative, neutral, and positive emotional priming stimuli on behavioral and cortical responses to visual depictions of others in pain. ERPs were recorded from 20 healthy adults, who were presented with painful and non-painful target pictures following observation of negative, neutral, and positive emotional priming pictures. ERP analyses revealed that relative to non-painful pictures, differential P3 amplitudes for painful pictures were larger followed by negative primes than either neutral or positive primes. There were no significant differential P3 amplitudes for painful pictures relative to non-painful pictures were found followed neutral and positive emotional primes. These results suggest that negative emotional primes strengthen observers’ attention toward others’ pain. These results support the threat value of pain hypothesis.
Similar content being viewed by others
References
Avenanti A, Bueti D, Galati G, Aglioti SM (2005) Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8(7):955–960
Avenanti A, Minio-Paluello I, Bufalari I, Aglioti SM (2006) Stimulus-driven modulation of motor-evoked potentials during observation of others’ pain. Neuroimage 32(1):316–324
Avenanti A, Sirigu A, Aglioti SM (2010) Racial bias reduces empathic sensorimotor resonance with other-race pain. Curr Biol 20(8):1018–1022
Bartholow BD, Riordan MA, Saults JS, Lust SA (2009) Psychophysiological evidence of response conflict and strategic control of responses in affective priming. J Exp Soc Psychol 45(4):655–666
Boly M, Garrido MI, Gosseries O, Bruno M-A, Boveroux P, Schnakers C, Massimini M, Litvak V, Laureys S, Friston K (2011) Preserved feedforward but impaired top-down processes in the vegetative state. Science 332(6031):858–862
Bonica JJ (1987) Importance of effective pain control. Acta Anaesthesiol Scand Suppl 85:1–16
Decety J (2011) Dissecting the neural mechanisms mediating empathy. Emot Rev 3(1):92–108
Decety J, Grezes J (2006) The power of simulation: imagining one’s own and other’s behavior. Brain Res 1079:4–14
Decety J, Lamm C (2006) Human empathy through the lens of social neuroscience. Scientific World J 6:1146–1163
Decety J, Yang CY, Cheng YW (2010) Physicians down-regulate their pain empathy response: an event-related brain potential study. Neuroimage 50(4):1676–1682
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(1):9–21
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. Neurosci Lett 356(1):1–4
Delplanque S, Silvert L, Hot P, Sequeira H (2005) Event-related P3a and P3b in response to unpredictable emotional stimuli. Biol Psychol 68(2):107–120
Demaree HA, Everhart DE, Youngstrom EA, Harrison DW (2005) Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behav Cogn Neurosci Rev 4(1):3–20
Eccleston C, Crombez G (1999) Pain demands attention: a cognitive-affective model of the interruptive function of pain. Psychol Bull 125(3):356–366
Fan Y, Han SH (2008) Temporal dynamic of neural mechanisms involved in empathy for pain: an event-related brain potential study. Neuropsychologia 46(1):160–173
Friedman D, Cycowicz YM, Gaeta H (2001) The novelty P3: an event-related brain potential (ERP) sign of the brain’s evaluation of novelty. Neurosci Biobehav Rev 25(4):355–373
Godinho F, Magnin M, Frot M, Perchet C, Garcia-Larrea L (2006) Emotional modulation of pain: is it the sensation or what we recall? J Neurosci 26(44):11454–11461
Han SH, Fan Y, Mao L (2008) Gender difference in empathy for pain: an electrophysiological investigation. Brain Res 1196:85–93
Han SH, Fan Y, Xu XJ, Qin JG, Wu B, Wang XY, Aglioti SM, Lihua Mao LH (2009) Empathic neural responses to others’ pain are modulated by emotional contexts. Hum Brain Mapp 30:3227–3237
Hein G, Silani G, Preuschoff K, Batson CD, Singer T (2010) Neural responses to ingroup and outgroup members’ suffering predict individual differences in costly helping. Neuron 68(1):149–160
Ibáñez A, Hurtado E, Lobos A, Escobar J, Trujillo N, Baez S, Huepe D, Manes F, Decety J (2011) Subliminal presentation of other faces (but not own face) primes behavioral and evoked cortical processing of empathy for pain. Brain Res 1398(29):72–85
Ito TA, Larsen JT, Smith NK, Cacioppo JT (1998) Negative information weighs more heavily on the brain: the negativity bias in evaluative categorizations. J Pers SocPsychol 75(4):887–900
Jackson PL, Brunet E, Meltzoff AN, Decety J (2006) Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia 44(5):752–761
Kirwilliam SS, Derbyshire SWG (2008) Increased bias to report heat or pain following emotional priming of pain-related fear. Pain 137(1):60–65
Lang PJ (1995) The emotion probe: studies of motivation and attention. Am Psychol 50(5):372–385
Lang PJ, Bradley MM, Cuthbert BN (1990) Emotion, attention, and the startle reflex. Psychol Rev 97(3):377–395
Lang PJ, Bradley MM, Cuthbert BN (1999) International Affective Picture System (IAPS): instruction manual and affective ratings. (Technical Report No. A-4). The Center for Research in Psychophysiology, University of Florida, Gainsville, Florida
McCarthy G, Donchin E (1981) A metric for thought—a comparison of P300 latency and reaction time. Science 211(4477):77–80
Meagher MW, Arnau RC, Rhudy JL (2001) Pain and emotion: effects of affective picture modulation. Psychosom Med 63:79–90
Minio-Paluello I, Avenanti A, Aglioti SM (2006) Left hemisphere dominance in reading the sensory qualities of others’ pain? Soc Neurosci 1(3–4):320–333
Morrison I, Lloyd D, di Pellegrino G, Roberts N (2004) Vicarious responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cogn Affect Behav Neurosci 4(2):270–278
Olofsson JK, Nordin S, Sequeira H, Polich J (2008) Affective picture processing: an integrative review of ERP findings. Biol Psychol 77(3):247–265
Rainville P (2002) Brain mechanisms of pain affect and pain modulation. Curr Opin Neurobiol 12(2):195–204
Rozenkrants B, Polich J (2008) Affective ERP processing in a visual oddball task: arousal, valence, and gender. Clin Neurophysiol 119(10):2260–2265
Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303(5661):1157–1162
Villemure C, Bushnell MC (2002) Cognitive modulation of pain: how do attention and emotion influence pain processing? Pain 95(3):195–199
Williams ACD (2002) Facial expression of pain, empathy, evolution, and social learning. Behav Brain Sci 25(4):475–488
Yamada M, Decety J (2009) Unconscious affective processing and empathy: an investigation of subliminal priming on the detection of painful facial expressions. Pain 143(1–2):71–75
Yuan JJ, Zhang QL, Chen AT, Li H, Wang QH, Zhuang ZCX, Jia SW (2007) Are we sensitive to valence differences in emotionally negative stimuli? Electrophysiological evidence from an ERP study. Neuropsychologia 45(12):2764–2771
Acknowledgments
This research was supported by the Fundamental Research Funds for the Central Universities (SWU1109084) and the Key Discipline Fund of the National 211 Project, China Education Ministry (NSKD08020).
Author information
Authors and Affiliations
Corresponding author
Appendix: Identification numbers of IAPS pictures presented in this study
Appendix: Identification numbers of IAPS pictures presented in this study
Negative: 2,276, 2,750, 2,900, 3,160, 3,181, 3,300, 9,007, 9,041, 9,265, 9,280, 9,290, 9,320, 9,330, 9,331, 9,340, 9,415, 9,430, 9,530, 9,561, 9,830.
Neutral: 1,112, 1,945, 2,220, 2,351, 35,502, 4,001, 4,003, 4,004, 4,005, 4,230, 4,240, 4,279, 4,550, 4,561, 4,613, 4,631, 5,395, 7,211, 7,820, 8,232.
Positive: 1,440, 1,460, 1,590, 1,600, 1,721, 2,310, 2,352, 2,650, 4,610, 5,600, 5,660, 5,820, 5,982, 7,260, 7,430, 7,470, 7,480, 7,580, 8,350, 8,540.
Rights and permissions
About this article
Cite this article
Meng, J., Hu, L., Shen, L. et al. Emotional primes modulate the responses to others’ pain: an ERP study. Exp Brain Res 220, 277–286 (2012). https://doi.org/10.1007/s00221-012-3136-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-012-3136-2