Abstract
Although gender differences in empathy have been well established through measuring subjective outcomes, some studies of the neural mechanisms of pain empathy have not found gender differences. This inconsistent evidence may be caused by different research methods or different paradigms. The present study adopted a different approach from the pain empathy paradigm to examine gender differences in empathic responses to others’ economic payoffs using event-related potentials. The results showed that the N2 amplitudes in female participants were more negative than those in male participants, indicating a greater female than male susceptibility to facial expressions at the early stage of empathy. The LPP amplitudes for male participants were found to be more positive in the observation condition (involving no self-interest) than in the participation condition (involving self-interest), but there was no significant difference in the LPP amplitudes for the female participants between the two conditions. The results suggest that females’ empathic responses are more likely to be elicited automatically by the perception of others’ emotional states. In contrast, males’ empathic responses are more likely to be mediated by self-interest, which subsequently reduces their empathic responses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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. https://doi.org/10.1016/j.neuroimage.2006.03.010
Balconi M, Mazza G (2009) Brain oscillations and BIS/BAS (behavioral inhibition/activation system) effects on processing masked emotional cues. ERS/ERD and coherence measures of alpha band. Int J Psychophysiol 74(2):158–165. https://doi.org/10.1016/j.ijpsycho.2009.08.006
Balconi M, Pozzoli U (2007) Event-related oscillations (EROs) and event-related potentials (ERPs) comparison in facial expression recognition. J Neuropsychol 1(2):283–294. https://doi.org/10.1348/174866407x184789
Baron-Cohen S (2009) Autism: the empathizing–systemizing (E–S) theory. Ann NY Acad Sci 1156(1):68–80. https://doi.org/10.1111/j.1749-6632.2009.04467.x
Baron-Cohen S, Wheelwright S (2004) The empathy quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. J Autism Dev Disord 34(2):163–175
Baron-Cohen S, Knickmeyer R, Belmonte MK (2005) Sex differences in the brain: implications for explaining autism. Science 310(5749):819–823
Berthoz S, Wessa M, Kedia G, Wicker B, Grezes J (2008) Cross-cultural validation of the empathy quotient in a French-speaking sample. Can J Psychiatry 53(7):469–477
Chen C, Yang CY, Cheng Y (2012) Sensorimotor resonance is an outcome but not a platform to anticipating harm to others. Soc Neurosci 7(6):578–590. https://doi.org/10.1080/17470919.2012.686924
Cheng Y, Chou K, Decety J, Chen I, Hung DM, Tzeng OJ, Lin C (2009) Sex differences in the neuroanatomy of human mirror-neuron system: a voxel-based morphometric investigation. Neuroscience 158(2):713–720
Cheng Y, Chen C, Decety J (2014) An EEG/ERP investigation of the development of empathy in early and middle childhood. Dev Cogn Neurosci 10:160–169
Collignon O, Girard S, Gosselin F, Saint-Amour D, Lepore F, Lassonde M (2010) Women process multisensory emotion expressions more efficiently than men. Neuropsychologia 48(1):220–225. https://doi.org/10.1016/j.neuropsychologia.2009.09.007
Cuthbert BN, Schupp HT, Bradley MM, Birbaumer N, Lang PJ (2000) Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol Psychol 52(2):95–111
Davis MH (1983) Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 44(1):113–126
Decety J (2011) Dissecting the neural mechanisms mediating empathy. Emot Rev 3:92–108
Decety J, Jackson PL (2004) The functional architecture of human empathy. Behav Cogn Neurosci Rev 3(2):71–100. https://doi.org/10.1177/1534582304267187
Decety J, Michalska KJ, Kinzler KD (2012) The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. Cereb Cortex 22(1):209–220
Decety J, Lewis KL, Cowell JM (2015) Specific electrophysiological components disentangle affective sharing and empathic concern in psychopathy. J Neurophysiol 114(1):493–504
Dennis TA, Hajcak G (2009) The late positive potential: a neurophysiological marker for emotion regulation in children. J Child Psychol Psychiatry 50(11):1373–1383. https://doi.org/10.1111/j.1469-7610.2009.02168.x
Derntl B, Habel U, Windischberger C, Robinson S, Kryspin-Exner I, Gur RC et al (2009) General and specific responsiveness of the amygdala during explicit emotion recognition in females and males. BMC Neurosci 10(1):91–91. https://doi.org/10.1186/1471-2202-10-91
Eagly AH (2009) The his and hers of prosocial behavior: an examination of the social psychology of gender. Am Psychol 64(8):644–658
Eisenberg N, Lennon R (1983) Sex differences in empathy and related capacities. Psychol Bull 94(1):100–131. https://doi.org/10.1037/0033-2909.94.1.100
Fan Y, Han S (2008) Temporal dynamic of neural mechanisms involved in empathy for pain: an event-related brain potential study. Neuropsychologia 46(1):160–173. https://doi.org/10.1016/j.neuropsychologia.2007.07.023
Fritsch N, Kuchinke L (2013) Acquired affective associations induce emotion effects in word recognition: an ERP study. Brain Lang 124:75–83. https://doi.org/10.1016/j.bandl.2012.12.001
Fukushima H, Hiraki K (2006) Perceiving an opponent’s loss: gender-related differences in the medial-frontal negativity. Soc Cogn Affect Neurosci 1(2):149–157. https://doi.org/10.1093/scan/nsl020
Gallese V (2003) The roots of empathy: the shared manifold hypothesis and the neural basis of intersubjectivity. Psychopathology 36(4):171–180. https://doi.org/10.1159/000072786
Gneezy U, Leonard KL, List JA (2008) Gender differences in competition: evidence from a matrilineal and a patriarchal society. Econometrica 77(5):1637–1664
Groen Y, Wijers AA, Tucha O, Althaus M (2013) Are there sex differences in ERPs related to processing empathy-evoking pictures? Neuropsychologia 51(1):142–155
Gu X, Han S (2007) Attention and reality constraints on the neural processes of empathy for pain. Neuroimage 36(1):256–267. https://doi.org/10.1016/j.neuroimage.2007.02.025
Hampson E, Vananders S, Mullin L (2006) A female advantage in the recognition of emotional facial expressions: test of an evolutionary hypothesis. Evol Hum Behav 27(6):401–416. https://doi.org/10.1016/j.evolhumbehav.2006.05.002
Hein G, Singer T (2008) “I feel how you feel but not always”: the empathic brain and its modulation. Curr Opin Neurobiol 18(2):153–158. https://doi.org/10.1016/j.conb.2008.07.012
Hoffmann H, Kessler H, Eppel T, Rukavina S, Traue HC (2010) Expression intensity, gender and facial emotion recognition: women recognize only subtle facial emotions better than men. Acta Psychol 135(3):278–283. https://doi.org/10.1016/j.actpsy.2010.07.012
Ibanez A, Hurtado E, Lobos A, Escobar J, Trujillo N, Baez S, … Decety J (2011) Subliminal presentation of other faces (but not own face) primes behavioral and evoked cortical processing of empathy for pain. Brain Res 1398:72–85
Ibanez A, Melloni M, Huepe D, Helgiu E, Rivera-Rei A, Canales-Johnson A, Baker P, Moya A (2012) What do event-related potentials (ERPs) bring to social neuroscience? Soc Neurosci 7(6):632–649. https://doi.org/10.1080/17470919.2012.691078
Itagaki S, Katayama J (2008) Self-relevant criteria determine the evaluation of outcomes induced by others. Neuroreport 19(3):383–387
Jie J, Luo P, Zhuang M, Li B, Pang Y, Li J, Zheng X (2019) Self-interest induces counter-empathy at the late stage of empathic responses to others’ economic payoffs. Front Psychol 10:372. https://doi.org/10.3389/fpsyg.2019.00372
Kiat JE, Cheadle JE (2017) The impact of individuation on the bases of human empathic responding. Neuroimage 155:312–321. https://doi.org/10.1016/j.neuroimage.2017.05.006
Klein KJ, Hodges SD (2001) Gender differences, motivation, and empathic accuracy: when it pays to understand. Pers Soc Psychol B 27(6):720–730
Knafo A, Zahn-Waxler C, Van Hulle C, Robinson JL, Rhee SH (2008) The developmental origins of a disposition toward empathy: genetic and environmental contributions. Emotion 8(6):737–752. https://doi.org/10.1037/a0014179
Lam CB, Solmeyer AR, McHale SM (2012) Sibling relationships and empathy across the transition to adolescence. J Youth Adolesc 41(12):1657–1670. https://doi.org/10.1007/s10964-012-9781-8
Lamm C, Decety J, Singer T (2011) Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. NeuroImage 54(3):2492–2502
Lawrence E, Shaw P, Baker D, Baroncohen S, David AS (2004) Measuring empathy: reliability and validity of the Empathy Quotient. Psychol Med 34(5):911–919
Lehmann A, Bahçesular K, Brockmann E-M, Biederbick S-E, Dziobek I, Gallinat J et al (2014) Subjective experience of emotions and emotional empathy in paranoid schizophrenia. Psychiatry Res 220(3):825–833. https://doi.org/10.1016/j.psychres.2014.09.009
Luo P, Zheng X, Chen X, Li Y, Wang J, Deng L, Zheng X (2014) Sex differences in affective response to different intensity of emotionally negative stimuli: an event-related potentials study. Neurosci Lett 578:85–89
Luo P, Wang J, Jin Y, Huang S, Xie M, Deng L et al (2015) Gender differences in affective sharing and self-other distinction during empathic neural responses to others’ sadness. Brain Imaging Behav 9(2):312–322. https://doi.org/10.1007/s11682-014-9308-x
Luo P, Pang Y, Li B, Jie J, Zhuang M, Yang S et al (2018) Competitive intensity modulates the pain empathy response: an event-related potentials study. Front Psychol 9:1854. https://doi.org/10.3389/fpsyg.2018.01854
Ma Q, Shen Q, Xu Q, Li D, Shu L, Weber B (2011) Empathic responses to others’ gains and losses: an electrophysiological investigation. Neuroimage 54(3):2472–2480. https://doi.org/10.1016/j.neuroimage.2010.10.045
Mella N, Studer J, Gilet A-L, Labouvie-Vief G (2012) Empathy for pain from adolescence through adulthood: an event-related brain potential study. Front Psychol 3:501. https://doi.org/10.3389/fpsyg.2012.00501
Michalska KJ, Kinzler KD, Decety J (2013) Age-related sex differences in explicit measures of empathy do not predict brain responses across childhood and adolescence. Dev Cogn Neurosci 3:22–32
Niedenthal PM (2007) Embodying emotion. Science 316:1002–1005
Niederle M, Vesterlund L (2007) Do women shy away from competition? Do men compete too much? Q J Econ 122(3):1067–1101
Olofsson JK, Polich J (2007) Affective visual event-related potentials: arousal, repetition, and time-on-task. Biol Psychol 75(1):101–108. https://doi.org/10.1016/j.biopsycho.2006.12.006
Olofsson JK, Nordin S, Sequeira H, Polich J (2008) Affective picture processing: an integrative review of ERP findings. Biol Psychol 77(3):247–265. https://doi.org/10.1016/j.biopsycho.2007.11.006
Perry A, Bentin S, Bartal IB, Lamm C, Decety J (2010) “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
Rand DG, Brescoll VL, Everett JA, Capraro V, Barcelo H (2016) Social heuristics and social roles: intuition favors altruism for women but not for men. J Exp Psychol Gen 145(4):389–396. https://doi.org/10.1037/xge0000154
Reniers RL, Corcoran R, Drake R, Shryane N, Vollm B (2011) The QCAE: a questionnaire of cognitive and affective empathy. J Pers Assess 93(1):84–95
Rose AJ, Rudolph KD (2006) A review of sex differences in peer relationship processes: potential trade-offs for the emotional and behavioral development of girls and boys. Psychol Bull 132(1):98–131. https://doi.org/10.1037/0033-2909.132.1.98
Saarela MV, Hlushchuk Y, Williams AC, Schurmann M, Kalso E, Hari R (2007) The compassionate brain: humans detect intensity of pain from another’s face. Cereb Cortex 17(1):230–237. https://doi.org/10.1093/cercor/bhj141
Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD (2003) The neural basis of economic decision-making in the Ultimatum Game. Science 300(5626):1755–1758
Schulte-Rüther M, Markowitsch HJ, Shah NJ, Fink GR, Piefke M (2008) Gender differences in brain networks supporting empathy. Neuroimage 42(1):393–403. https://doi.org/10.1016/j.neuroimage.2008.04.180
Sessa P, Meconi F, Castelli L, Dell’Acqua R (2014) Taking one’s time in feeling other-race pain: an event-related potential investigation on the time-course of cross-racial empathy. Soc Cogn Affect Neurosci 9(4):454–463. https://doi.org/10.1093/scan/nst003
Shamay-Tsoory SG, Aharon-Peretz J, Perry D (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132(3):617–627. https://doi.org/10.1093/brain/awn279
Singer T, Lamm C (2009) The social neuroscience of empathy. Ann N Y Acad Sci 1156:81–96. https://doi.org/10.1111/j.1749-6632.2009.04418.x
Singer T, Seymour B, O’Doherty JP, Stephan KE, Dolan RJ, Frith CD (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature 439(7075):466–469. https://doi.org/10.1038/nature04271
Topcu C, Erdur-Baker O (2012) Affective and cognitive empathy as mediators of gender differences in cyber and traditional bullying. Sch Psychol Int 33(5):550–561
Vromen JM, Lipp OV, Remington RW (2015) The spider does not always win the fight for attention: disengagement from threat is modulated by goal set. Cogn Emot 29(7):1185–1196. https://doi.org/10.1080/02699931.2014.969198
Wen G, Bo C, Shiguang S, Xilin C, Delong Z, Xiaohua Z et al (2008) The CAS-PEAL large-scale Chinese face database and baseline evaluations. IEEE Trans Syst Man Cybern A Syst Hum 38(1):149–161. https://doi.org/10.1109/tsmca.2007.909557
Williford A, Boulton AJ, Forrestbank SS, Bender K, Dieterich WA, Jenson JM (2016) The effect of bullying and victimization on cognitive empathy development during the transition to middle school. Child Youth Care Forum 45(4):525–541. https://doi.org/10.1007/s10566-015-9343-9
Wölfer R, Cortina KS, Baumert J (2012) Embeddedness and empathy: how the social network shapes adolescents’ social understanding. J Adolesc 35(5):1295–1305. https://doi.org/10.1016/j.adolescence.2012.04.015
World Medical Organization (1999) Declaration of Helsinki (1964). Br Med J 313:1448–1449
Xiang Y, Wang Y, Gao S, Zhang X, Cui R (2018) Neural mechanisms with respect to different paradigms and relevant regulatory factors in empathy for pain. Front Neurosci 12:507. https://doi.org/10.3389/fnins.2018.00507
Yamada M, Lamm C, Decety J (2011) Pleasing frowns, disappointing smiles: an ERP investigation of counter-empathy. Emotion 11(6):1336–1345. https://doi.org/10.1037/a0023854
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant no. 31771218), the Major Program of the National Social Science Foundation of China (Grant no. 14ZDB259), and the Educational Science Project during the Twelfth Five-year Plan Period of Hainan, China (Grant no. QJY1251505).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Ethical approval
All procedures involving human participants were in accordance with the ethical standards of the Ethics Committee of South China Normal University and with the 1964 Helsinki Declaration and its later amendments.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jie, J., Luo, P., Zhuang, M. et al. Gender differences in empathic responses to others’ economic payoffs: an event-related potentials study. Exp Brain Res 237, 1347–1359 (2019). https://doi.org/10.1007/s00221-019-05518-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-019-05518-x