doi:

DOI: 10.3724/SP.J.1042.2018.00442

Advances in Psychological Science (心理科学进展) 2018/26:3 PP.442-453

The effects of oxytocin on empathic response and its mechanisms


Abstract:
Oxytocin is a prosocial hormone that also has an important influence on human beings' empathic responses. It can promote emotion recognition, enhance the empathic concern regarding others' unfortunate experiences, and weaken the level of personal distress. With reference to the mechanisms, oxytocin may influence an individual's empathic response by promoting his/her embodied-simulation ability, weakening the tendency of self-centeredness, and regulating the emotional representation mechanism. Future studies could focus on the effects of oxytocin on the different types of empathic responses, the effects of oxytocin on gender differences in empathic responses, and actively using oxytocin in clinical interventions for empathy deficits.

Key words:oxytocin,empathic response,embodied-simulation,self-projection,emotional representation

ReleaseDate:2018-03-29 16:57:01



刘金婷, 蔡强, 王若菡, 吴寅. (2011). 催产素与人类社会行为. 心理科学进展, 19(10), 1480-1492.

岳童, 黄希庭, 刘光远. (2017). 催产素影响人类社会认知的性别差异. 心理科学进展, 25(12), 2146-2157.

岳童. (2016). 积极共情的认知神经机制研究(博士学位论文). 西南大学, 重庆.

岳童, 黄希庭. (2014). 共情的神经网络. 西南大学学报(社会科学版), 40(5), 87-94.

岳童, 黄希庭. (2016a). 共情特质的神经生物学基础. 心理科学进展, 24(9), 1368-1376.

岳童, 黄希庭. (2016b).认知神经研究中的积极共情. 心理科学进展, 24(9), 402-409.

Abu-Akel, A., Palgi, S., Klein, E., Decety, J., & Shamay-Tsoory, S. (2015). Oxytocin increases empathy to pain when adopting the other-but not the self-perspective. Social Neuroscience, 10(1), 7-15.

Anagnostou, E., Soorya, L., Brian, J., Dupuis, A., Mankad, D., Smile, S., & Jacob, S. (2014). Intranasal oxytocin in the treatment of autism spectrum disorders:A review of literature and early safety and efficacy data in youth. Brain Research, 1580, 188-198.

Averbeck, B. B., Bobin, T., Evans, S., & Shergill, S. S. (2012). Emotion recognition and oxytocin in patients with schizophrenia. Psychological Medicine, 42(2), 259-266.

Barraza, J. A., & Zak, P. J. (2009). Empathy toward strangers triggers oxytocin release and subsequent generosity. Annals of the New York Academy of Sciences, 1167(1), 182-189.

Bastiaansen, J. A., Thioux, M., & Keysers, C. (2009). Evidence for mirror systems in emotions. Philosophical Transactions of the Royal Society of London B:Biological Sciences, 364(1528), 2391-2404.

Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008). Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron, 58(4), 639-650.

Bernhardt, B. C., & Singer, T. (2012). The neural basis of empathy. Annual Review of Neuroscience, 35, 1-23.

Bertsch, K., Gamer, M., Schmidt, B., Schmidinger, I., Walther, S., Kästel, T.,... Herpertz, S. C. (2013). Oxytocin and reduction of social threat hypersensitivity in women with borderline personality disorder. The American Journal of Psychiatry, 170(10), 1169-1177.

Bos, P. A., Montoya, E. R., Hermans, E. J., Keysers, C., & van Honk, J. (2015). Oxytocin reduces neural activity in the pain circuitry when seeing pain in others. NeuroImage, 113, 217-224.

Cardoso, C., Ellenbogen, M. A., Orlando, M. A., Bacon, S. L., & Joober, R. (2013). Intranasal oxytocin attenuates the cortisol response to physical stress:A dose-response study. Psychoneuroendocrinology, 38(3), 399-407.

Carr, L., Iacoboni, M., Dubeau, M.-C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans:A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences of the United States of America, 100(9), 5497-5502.

Cikara, M., & Fiske, S. T. (2011). Bounded empathy:Neural responses to outgroup targets' (mis) fortunes. Journal of Cognitive Neuroscience, 23(12), 3791-3803.

Colonnello, V., Chen, F. S., Panksepp, J., & Heinrichs, M. (2013). Oxytocin sharpens self-other perceptual boundary. Psychoneuroendocrinology, 38(12), 2996-3002.

de Vignemont, F., & Singer, T. (2006). The empathic brain:How, when and why? Trends in Cognitive Sciences, 10(10), 435-441.

de Waal, F. B. (2008). Putting the altruism back into altruism:The evolution of empathy. Annual Review of Psychology, 59, 279-300.

Ditzen, B., Nater, U. M., Schaer, M., La Marca, R., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2013). Sex-specific effects of intranasal oxytocin on autonomic nervous system and emotional responses to couple conflict. Social Cognitive and Affective Neuroscience, 8(8), 897-902.

Domes, G., Heinrichs, M., Gläscher, J., Büchel, C., Braus, D. F., & Herpertz, S. C. (2007a). Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biological Psychiatry, 62(10), 1187-1190.

Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007b). Oxytocin improves "mind-reading" in humans. Biological Psychiatry, 61(6), 731-733.

Domes, G., Steiner, A., Porges, S. W., & Heinrichs, M. (2013). Oxytocin differentially modulates eye gaze to naturalistic social signals of happiness and anger. Psychoneuroendocrinology, 38(7), 1198-1202.

Eckstein, M., Becker, B., Scheele, D., Scholz, C., Preckel, K., Schlaepfer, T. E.,... Hurlemann, R. (2015). Oxytocin facilitates the extinction of conditioned fear in humans. Biological Psychiatry, 78(3), 194-202.

Fan, Y., Duncan, N. W., de Greck, M., & Northoff, G. (2011). Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neuroscience and Biobehavioral Reviews, 35(3), 903-911.

Frith, C. D., & Singer, T. (2008). The role of social cognition in decision making. Philosophical Transactions of the Royal Society B:Biological Sciences, 363(1511), 3875-3886.

Gamer, M., Zurowski, B., & Buchel, C. (2010). Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proceedings of the National Academy of Sciences of the United States of America, 107(20), 9400-9405.

Gao, S., Becker, B., Luo, L. Z., Geng, Y. Y., Zhao, W. H., Yin, Y.,... Kendrick, K. M. (2016). Oxytocin, the peptide that bonds the sexes also divides them. Proceedings of the National Academy of Sciences of the United States of America, 113(27), 7650-7654.

Grimm, S., Pestke, K., Feeser, M., Aust, S., Weigand, A., Wang, J.,... Bajbouj, M. (2014). Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress. Social Cognitive and Affective Neuroscience, 9(11), 1828-1835.

Hoge, E. A., Anderson, E., Lawson, E. A., Bui, E., Fischer, L. E., Khadge, S. D.,... Simon, N. M. (2014). Gender moderates the effect of oxytocin on social judgments. Human Psychopharmacology:Clinical and Experimental, 29(3), 299-304.

Jabbi, M., & Keysers, C. (2008). Inferior frontal gyrus activity triggers anterior insula response to emotional facial expressions. Emotion, 8(6), 775-780.

Jackson, P. L., Meltzoff, A. N., & Decety, J. (2005). How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage, 24(3), 771-779.

Kanat, M., Heinrichs, M., Mader, I., van Elst, L. T., & Domes, G. (2015a). Oxytocin modulates amygdala reactivity to masked fearful eyes. Neuropsychopharmacology, 40(11), 2632-2638.

Kanat, M., Heinrichs, M., Schwarzwald, R., & Domes, G. (2015b). Oxytocin attenuates neural reactivity to masked threat cues from the eyes. Neuropsychopharmacology, 40(2), 287-295.

Klimecki, O. M., Leiberg, S., Lamm, C., & Singer, T. (2012). Functional neural plasticity and associated changes in positive affect after compassion training. Cerebral Cortex, 23(7), 1552-1561.

Klimecki, O. M., Leiberg, S., Ricard, M., & Singer, T. (2014). Differential pattern of functional brain plasticity after compassion and empathy training. Social Cognitive and Affective Neuroscience, 9(6), 873-879.

Korb, S., Malsert, J., Strathearn, L., Vuilleumier, P., & Niedenthal, P. (2016). Sniff and mimic-Intranasal oxytocin increases facial mimicry in a sample of men. Hormones and Behavior, 84, 64-74.

Labuschagne, I., Phan, K. L., Wood, A., Angstadt, M., Chua, P., Heinrichs, M.,... Nathan, P. J. (2011). Medial frontal hyperactivity to sad faces in generalized social anxiety disorder and modulation by oxytocin. International Journal of Neuropsychopharmacology, 15(7), 883-896.

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.

Lischke, A., Berger, C., Prehn, K., Heinrichs, M., Herpertz, S. C., & Domes, G. (2012). Intranasal oxytocin enhances emotion recognition from dynamic facial expressions and leaves eye-gaze unaffected. Psychoneuroendocrinology, 37(4), 475-481.

Liu, Y., Sheng, F., Woodcock, K. A., & Han, S. H. (2013). Oxytocin effects on neural correlates of self-referential processing. Biological Psychology, 94(2), 380-387.

Ma, Y. N., Shamay-Tsoory, S., Han, S. H., & Zink, C. F. (2016). Oxytocin and social adaptation:Insights from neuroimaging studies of healthy and clinical populations. Trends in Cognitive Sciences, 20(2), 133-145.

MacDonald, E., Dadds, M. R., Brennan, J. L., Williams, K., Levy, F., & Cauchi, A. J. (2011). A review of safety, side-effects and subjective reactions to intranasal oxytocin in human research. Psychoneuroendocrinology, 36(8), 1114-1126.

MacDonald, K., & MacDonald, T. M. (2010). The peptide that binds:A systematic review of oxytocin and its prosocial effects in humans. Harvard Review Of Psychiatry, 18(1), 1-21.

MacKinnon, A. L., Gold, I., Feeley, N., Hayton, B., Carter, C. S., & Zelkowitz, P. (2014). The role of oxytocin in mothers' theory of mind and interactive behavior during the perinatal period. Psychoneuroendocrinology, 48, 52-63.

Meyer, M. L., Masten, C. L., Ma, Y. N., Wang, C. B., Shi, Z. H., Eisenberger, N. I., & Han, S. H. (2013). Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. Social Cognitive and Affective Neuroscience, 8(4), 446-454.

Mezzacappa, E. S., & Katkin, E. S. (2002). Breast-feeding is associated with reduced perceived stress and negative mood in mothers. Health Psychology, 21(2), 187-193.

Molenberghs, P., Cunnington, R., & Mattingley, J. B. (2012). Brain regions with mirror properties:A meta-analysis of 125 human fMRI studies. Neuroscience & Biobehavioral Reviews, 36(1), 341-349.

Morelli, S. A., Lieberman, M. D., & Zaki, J. (2015). The emerging study of positive empathy. Social and Personality Psychology Compass, 9(2), 57-68.

Morelli, S. A., Rameson, L. T., & Lieberman, M. D. (2014). The neural components of empathy:Predicting daily prosocial behavior. Social Cognitive and Affective Neuroscience, 9(1), 39-47.

Palgi, S., Klein, E., & Shamay-Tsoory, S. G. (2015). Intranasal administration of oxytocin increases compassion toward women. Social Cognitive and Affective Neuroscience, 10(3), 311-317.

Palgi, S., Klein, E., & Shamay-Tsoory, S. G. (2016). Oxytocin improves compassion toward women among patients with PTSD. Psychoneuroendocrinology, 64, 143-149.

Perry, A., Bentin, S., Shalev, I., Israel, S., Uzefovsky, F., Bar-On, D., & Ebstein, R. P. (2010). Intranasal oxytocin modulates EEG mu/alpha and beta rhythms during perception of biological motion. Psychoneuroendocrinology, 35(10), 1446-1453.

Perry, D., Hendler, T., & Shamay-Tsoory, S. G. (2012). Can we share the joy of others? Empathic neural responses to distress vs joy. Social Cognitive and Affective Neuroscience, 7(8), 909-916.

Petrovic, P., Kalisch, R., Singer, T., & Dolan, R. J. (2008). Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. Journal of Neuroscience, 28(26), 6607-6615.

Pfeifer, J. H., Iacoboni, M., Mazziotta, J. C., & Dapretto, M. (2008). Mirroring others' emotions relates to empathy and interpersonal competence in children. NeuroImage, 39(4), 2076-2085.

Preston, S. D., & De Waal, F. B. (2002). Empathy:Its ultimate and proximate bases. Behavioral and brain sciences, 25(1), 1-20.

Pineda, J. A. (2005). The functional significance of mu rhythms:Translating "seeing" and "hearing" into "doing". Brain Research Reviews, 50(1), 57-68.

Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M.,... Rombouts, S. A. R. B. (2011). Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying:A randomized controlled trial. Biological Psychiatry, 70(3), 291-297.

Riem, M. M. E. (2012). No laughing matter:intranasal oxytocin administration changes functional brain connectivity during exposure to infant laughter.. Neuropsychopharmacology, 37(5), 1257-1266.

Rilling, J. K., DeMarco, A. C., Hackett, P. D., Thompson, R., Ditzen, B., Patel, R., & Pagnoni, G. (2012). Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology, 37(4), 447-461.

Rupp, H. A., James, T. W., Ketterson, E. D., Sengelaub, D. R., Ditzen, B., & Heiman, J. R. (2014). Amygdala response to negative images in postpartum vs nulliparous women and intranasal oxytocin. Social Cognitive and Affective Neuroscience, 9(1), 48-54.

Sallquist, J., Eisenberg, N., Spinrad, T. L., Eggum, N. D., & Gaertner, B. M. (2009). Assessment of preschoolers' positive empathy:Concurrent and longitudinal relations with positive emotion, social competence, and sympathy. The Journal of Positive Psychology, 4(3), 223-233.

Sauer, C., Montag, C., Reuter, M., & Kirsch, P. (2013). Imaging oxytocin×dopamine interactions:an epistasis effect of CD38 and COMT gene variants influences the impact of oxytocin on amygdala activation to social stimuli. Frontiers in Neuroscience, 7, 45.

Scheele, D., Kendrick, K. M., Khouri, C., Kretzer, E., Schläpfer, T. E., Stoffel-Wagner, B.,... Hurlemann, R. (2014a). An oxytocin-induced facilitation of neural and emotional responses to social touch correlates inversely with autism traits. Neuropsychopharmacology, 39(9), 2078-2085.

Scheele, D., Striepens, N., Kendrick, K. M., Schwering, C., Noelle, J., Wille, A.,... Hurlemann, R. (2014b). Opposing effects of oxytocin on moral judgment in males and females. Human Brain Mapping, 35(12), 6067-6076.

Scheele, D., Wille, A., Kendrick, K. M., Stoffel-Wagner, B., Becker, B., Gunturkun, O.,... Hurlemann, R. (2013). Oxytocin enhances brain reward system responses in men viewing the face of their female partner. Proceedings of the National Academy of Sciences of the United States of America, 110(50), 20308-20313.

Schulte-Rüther, M., & Greimel, E. (2011). Brain networks supporting empathy. In R. Ebstein, S. Shamay-Tsoory, & S. H. Chew (Eds.), From DNA to social cognition (pp. 47-61). Hoboken, NJ:John Wiley & Sons.

Singer, T., & Klimecki, O. M. (2014). Empathy and compassion. Current Biology, 24(18), R875-R878.

Singer, T., Snozzi, R., Bird, G., Petrovic, P., Silani, G., Heinrichs, M., & Dolan, R. J. (2008). Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Emotion, 8(6), 781-791.

Singh, F., Nunag, J., Muldoon, G., Cadenhead, K. S., Pineda, J. A., & Feifel, D. (2016). Effects of intranasal oxytocin on neural processing within a socially relevant neural circuit. European Neuropsychopharmacology, 26(3), 626-630.

Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology, 34(13), 2655-2666.

Theodoridou, A., Rowe, A. C., & Mohr, C. (2013). Men perform comparably to women in a perspective taking task after administration of intranasal oxytocin but not after placebo. Frontiers in Human Neuroscience, 7, 197.

van Overwalle, F., & Baetens, K. (2009). Understanding others' actions and goals by mirror and mentalizing systems:A meta-analysis. NeuroImage, 48(3), 564-584.

Warren, J. E., Sauter, D. A., Eisner, F., Wiland, J., Dresner, M. A., Wise, R. J.,... Scott, S. K. (2006). Positive emotions preferentially engage an auditory-motor "mirror" system. The Journal of Neuroscience, 26(50), 13067-13075.

Walter, H. (2012). Social cognitive neuroscience of empathy:concepts, circuits, and genes. Emotion Review, 4(1), 9-17.

Wicker, B., Keysers, C., Plailly, J., Royet, J.-P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in my insula:The common neural basis of seeing and feeling disgust. Neuron, 40(3), 655-664.

Wittfoth-Schardt, D., Gründing, J., Wittfoth, M., Lanfermann, H., Heinrichs, M., Domes, G.,... Waller, C. (2012). Oxytocin modulates neural reactivity to children's faces as a function of social salience. Neuropsychopharmacology, 37(8), 1799-1807.

Yue, T., Pan, W. G., & Huang, X. T. (2016). The relationship between trait positive empathy and brain structure:A voxel-based morphometry study. NeuroReport, 27(6), 422-426.

Zhao, W. H., Yao, S. X., Li, Q., Geng, Y. Y., Ma, X. L., Luo, L. Z.,... Kendrick, K. M. (2016). Oxytocin blurs the self-other distinction during trait judgments and reduces medial prefrontal cortex responses. Human Brain Mapping, 37(7), 2512-2527.

Zunhammer, M., Geis, S., Busch, V., Greenlee, M. W., & Eichhammer, P. (2015). Effects of intranasal oxytocin on thermal pain in healthy men:A randomized functional magnetic resonance imaging study. Psychosomatic Medicine, 77(2), 156-166.