Empathy for social exclusion involves the sensory-discriminative component of pain: A within-subject fMRI study

Social Cognitive and Affective Neuroscience

Volumn 10, Issue 2, 2015, Pages 153-164

  Novembre, Giovanni ^a   Zanon, Marco ^a   Silani, Giorgia ^a  

^a SISSA   (Italy)

Author keywords

Empathy; FMRI; Physical pain; Social exclusion; Somatosensory cortex

Indexed keywords

ADOLESCENT; BRAIN MAPPING; CINGULATE GYRUS; EMPATHY; FEMALE; HUMAN; MALE; NERVE CELL NETWORK; NOCICEPTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PAIN THRESHOLD; PATHOPHYSIOLOGY; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; PSYCHOLOGY; SENSATION; SOCIAL DISTANCE; SOMATOSENSORY CORTEX; YOUNG ADULT;

ADOLESCENT; BRAIN MAPPING; DISCRIMINATION (PSYCHOLOGY); EMPATHY; FEMALE; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PAIN; PAIN PERCEPTION; PAIN THRESHOLD; SENSATION; SOCIAL DISTANCE; SOMATOSENSORY CORTEX; YOUNG ADULT;

EID: 84983157139     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nsu038     Document Type: Article

References (61)

1. Amodio, D., Frith, C. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7(4), 268-77.
2. Avenanti, A., Bueti, D., Galati, G., Aglioti, S.M. (2005). Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nature Neuroscience, 8(7), 955-60.
3. Bastiaansen, J.A., Thioux, M., Keysers, C. (2009). Evidence for mirror systems in emotions. Philosophical Transactions of the Royal Society B: Biological Science, 364(1528), 2391-404.
4. Beeney, J.E., Franklin, R.G., Jr, Levy, K.N., Adams, R.B., Jr. (2011). I feel your pain: emotional closeness modulates neural responses to empathically experienced rejection. Social Neuroscience, 6(4), 369-76.
5. Bolling, D.Z., Pitskel, N.B., Deen, B., et al. (2011). Dissociable brain mechanisms for processing social exclusion and rule violation. NeuroImage, 54(3), 2462-71.
6. Bolling, D.Z., Pelphrey, K.A., Vander Wyk, B.C. (2012). Differential brain responses to social exclusion by one's own versus opposite-gender peers. Social Neuroscience, 7(4), 331-46.
7. Bowlby, J. (1999). Attachment and loss. Attachment (vol.1) (2nd ed.). New York: Basic Books.
8. Craig, A.D. (2009). How do you feel_now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10(1), 59-70.
9. Davis, K.D. (2000). The neural circuitry of pain as explored with functional MRI. Neurological Research, 22(3), 313-7.
10. Davis, M.H. (1980). A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology, 10, 85.
11. de Vignemont, F., Singer, T. (2006). The empathic brain: how, when and why? Trends in Cognitive Sciences, 10(10), 435-41.
12. Decety, J. (2011). The neuroevolution of empathy. Annals of the New York Academy of Sciences, 1231, 35-45.
13. Decety, J., Lamm, C. (2006). Human empathy through the lens of social neuroscience. ScientificWorldJournal, 6, 1146-63.
14. Dewall, C.N., Macdonald, G., Webster, G.D. et al. (2010). Acetaminophen reduces social pain: behavioral and neural evidence. Psychological Science, 21(7), 931-7.
15. Drevets, W.C., Savitz, J., Trimble, M. (2008). The subgenual anterior cingulate cortex in mood disorders. CNS Spectrums, 13(8), 663-81.
16. Eickhoff, S.B., Stephan, K.E., Mohlberg, H., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage, 25, 1325-35.
17. Eisenberger, N.I. (2012). The pain of social disconnection: examining the shared neural underpinnings of physical and social pain. Nature Reviews. Neuroscience, 13(6), 421-34.
18. Eisenberger, N.I., Lieberman, M.D., Williams, K.D. (2003). Does rejection hurt? An FMRI study of social exclusion. Science, 302(5643), 290-2.
19. 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), 903-11.
20. Fisher, H.E., Brown, L.L., Aron, A., Strong, G., Mashek, D. (2010). Reward, addiction, and emotion regulation systems associated with rejection in love. Journal of Neurophysiology, 104(1), 51-60.
21. Frith, C.D., Frith, U. (2006). The neural basis of mentalizing. Neuron, 50(4), 531-4.
22. Han, S., Jiang, Y., Humphreys, G.W., Zhou, T., Cai, P. (2005). Distinct neural substrates for the perception of real and virtual visual worlds. NeuroImage, 24(3), 928-35.
23. Hein, G., Singer, T. (2008). I feel how you feel but not always: the empathic brain and its modulation. Current Opinion in Neurobiology, 18(2), 153-8.
24. Iannetti, G.D., Mouraux, A. (2010). From the neuromatrix to the pain matrix (and back). Experimental Brain Research, 205(1), 1-12.
25. Jackson, P., Meltzoff, A., Decety, J. (2005). How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage, 24(3), 771-9.
26. Kelly, C., Toro, R., Di Martino, A., et al. (2012). A convergent functional architecture of the insula emerges across imaging modalities. NeuroImage, 61(4), 1129-42.
27. Kersting, A., Ohrmann, P., Pedersen, A., et al. (2009). Neural activation underlying acute grief in women after the loss of an unborn child. The American Journal of Psychiatry, 166(12), 1402-10.
28. Keysers, C., Kaas, J.H., Gazzola, V. (2010). Somatosensation in social perception. Nature Reviews Neuroscience, 11(6), 417-28.
29. Kingstone, A., Smilek, D., Eastwood, J.D. (2008). Cognitive Ethology: a new approach for studying human cognition. British Journal of Psychology, 99(Pt 3), 317-40.
30. Krill, A., Platek, S.M. (2009). In-group and out-group membership mediates anterior cingulate activation to social exclusion. Frontiers in Evolutionary Neuroscience, 1, 1.
31. Kross, E., Berman, M.G., Mischel, W., Smith, E.E., Wager, T.D. (2011). Social rejection shares somatosensory representations with physical pain. Proceedings of the National Academy of Sciences of the United States of America, 108(15), 6270-5.
32. Kurth, F., Zilles, K., Fox, P.T., Laird, A.R., Eickhoff, S.B. (2010). A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Structure and Function, 214(5-6), 519-34.
33. 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), 2492-502.
34. Mar, R.A., Kelley, W.M., Heatherton, T.F., Macrae, C.N. (2007). Detecting agency from the biological motion of veridical vs animated agents. Social Cognitive and Affective Neuroscience, 2(3), 199-205.
35. Masten, C.L., Eisenberger, N.I., Borofsky, L.A., et al. (2009). Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. Social Cognitive and Affective Neuroscience, 4(2), 143-57.
36. Masten, C.L., Colich, N.L., Rudie, J.D., Bookheimer, S.Y., Eisenberger, N.I., Dapretto, M. (2011a). An fMRI investigation of responses to peer rejection in adolescents with autism spectrum disorders. Developmental Cognitive Neuroscience, 1(3), 260-70.
37. Masten, C.L., Morelli, S.A., Eisenberger, N.I. (2011b). An fMRI investigation of empathy for 'social pain' and subsequent prosocial behavior. NeuroImage, 55(1), 381-8.
38. Masten, C.L., Telzer, E.H., Fuligni, A.J., Lieberman, M.D., Eisenberger, N.I. (2012). Time spent with friends in adolescence relates to less neural sensitivity to later peer rejection. Social Cognitive and Affective Neuroscience, 7(1), 106-14.
39. Mayberg, H.S., Liotti, M., Brannan, S.K., et al. (1999). Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. The American Journal of Psychiatry, 156(5), 675-82.
40. Meyer, M.L., Masten, C.L., Ma, Y., et al. (2012). Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. Social Cognitive and Affective Neuroscience, 8(4), 446-454.
41. Mitchell, J.P., Banaji, M.R., Macrae, C.N. (2005). General and specific contributions of the medial prefrontal cortex to knowledge about mental states. NeuroImage, 28(4), 757-62.
42. Moor, B.G., Guroglu, B., Op de Macks, Z.A., Rombouts, S.A., Van der Molen, M.W., Crone, E.A. (2012). Social exclusion and punishment of excluders: neural correlates and developmental trajectories. NeuroImage, 59(1), 708-17.
43. Mutschler, I., Wieckhorst, B., Kowalevski, S., et al. (2009). Functional organization of the human anterior insular cortex. Neuroscience Letters, 457(2), 66-70.
44. Nichols, T., Brett, M., Andersson, J., Wager, T., Poline, J.B. (2005). Valid conjunction inference with the minimum statistic. NeuroImage, 25(3), 653-60.
45. Onoda, K., Okamoto, Y., Nakashima, K., Nittono, H., Ura, M., Yamawaki, S. (2009). Decreased ventral anterior cingulate cortex activity is associated with reduced social pain during emotional support. Society for Neuroscience, 4(5), 443-54.
46. Penny, W.D., Holmes, A. (2004). Random-effects analysis. In: Penny, W., Holmes, A., Friston, K.J., editors. Human Brain Function. San Diego, CA: Elsevier, pp. 843-50.
47. Perl, E.R. (2007). Ideas about pain, a historical view. Nature Reviews Neuroscience, 8(1), 71-80.
48. Peyron, R., Laurent, B., Garcia-Larrea, L. (2000). Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiologie Clinique, 30, 263-88.
49. Phan, K.L., Wager, T., Taylor, S.F., Liberzon, I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16(2), 331-48.
50. Premkumar, P. (2012). Are you being rejected or excluded? Insights from neuroimaging studies using different rejection paradigms. Clinical Psychopharmacology and Neuroscience, 10(3), 144-54.
51. Preston, S.D., de Waal, F.B.M. (2002). Empathy: its ultimate and proximate bases. Journal of Behavioral and Brain Science, 25, 1-72.
52. Risko, E.F., Laidlaw, K., Freeth, M., Foulsham, T., Kingstone, A. (2012). Social attention with real versus reel stimuli: toward an empirical approach to concerns about ecological validity. Frontiers in Human Neuroscience, 6, 143.
53. Shackman, A.J., Salomons, T.V., Slagter, H.A., Fox, A.S., Winter, J.J., Davidson, R.J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience, 12(3), 154-67.
54. Singer, T., Lamm, C. (2009). The social neuroscience of empathy. Annals of the New York Academy of Sciences, 1156, 81-96.
55. Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R.J., Frith, C.D. (2004). Empathy for pain involves the affective but not the sensory components of pain. Science, 303, 1157-61.
56. Torta, D.M., Cauda, F. (2011). Different functions in the cingulate cortex, a meta-analytic connectivity modeling study. NeuroImage, 56(4), 2157-72.
57. Vogt, B.A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience, 6, 533-44.
58. Vorst, H., Bermond, B. (2001). Validity and reliability of the Bermond-Vorst alexithymia questionnaire. Personality and Individual Differences, 30(3), 413-34.
59. Williams, A.C. (2002). Facial expression of pain: an evolutionary account. Behavioral and Brain Sciences, 25(4), 439-55 discussion 455-88.
60. Williams, K.D., Cheung, C.K., Choi, W. (2000). Cyberostracism: effects of being ignored over the Internet. Journal of Personality and Social Psychology, 79(5), 748-62.
61. Zaki, J., Ochsner, K. (2012). The neuroscience of empathy: progress, pitfalls and promise. Nature Neuroscience, 15(5), 675-80.