An fmri study of caring vs self-focus during induced compassion and pride

Social Cognitive and Affective Neuroscience

Volumn 7, Issue 6, 2012, Pages 635-648

  Simon thomas, Emiliana R ^a   Godzik, Jakub ^b   Castle, Elizabeth ^c   Antonenko, Olga ^d   Ponz, Aurelie ^d   Kogan, Aleksander ^d   Keltner, Dacher J ^d  

^a STANFORD UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Caregiving; Midbrain periaqueductal gray; Nurturing; Posterior medial cortex; Self focus

Indexed keywords

OXYGEN;

ANALYSIS OF VARIANCE; ARTICLE; BLOOD; BRAIN; BRAIN MAPPING; EMPATHY; FEMALE; HUMAN; IMAGE PROCESSING; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; REGRESSION ANALYSIS; SELF REPORT; SOCIAL BEHAVIOR; VASCULARIZATION;

ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; EMPATHY; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PHOTIC STIMULATION; REGRESSION ANALYSIS; SELF REPORT; SOCIAL BEHAVIOR;

EID: 84865774717     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nsr045     Document Type: Article

References (97)

1. Badre, D., Wagner, A.D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia, 45(13), 2883-901.
2. Bartels, A., Zeki, S. (2004). The neural correlates of maternal and romantic love. Neuroimage, 21(3), 1155-66.
3. Batson, C.D., Shaw, L. (1991). Evidence for Altruism: toward a pluralism of prosocial motives. Psychological Inquiry, 2, 107-22.
4. 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), 639-50.
5. Beauregard, M., Courtemanche, J., Paquette, V., St-Pierre, E.L. (2009). The neural basis of unconditional love. Psychiatry Research, 172(2), 93-8.
6. Bennett, C.M., Wolford, G.L., Miller, M.B. (2009). The principled control of false positives in neuroimaging. Social Cognitive and Affective Neuroscience, 4(4), 417-22.
7. Berkman, E.T., Lieberman, M.D. (2009). Using neuroscience to broaden emotion regulation: theoretical and methodological considerations. Social and Personality Psychology Compass, 3, 475-93.
8. Blakemore, S.J., Frith, C. (2003). Self-awareness and action. Current Opinion in Neurobiology, 13(2), 219-24.
9. 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 Science, 100(9), 5497-502.
10. Carter, C.S., Grippo, A.J., Pournajafi-Nazarloo, H., Ruscio, M.G., Porges, S.W. (2008). Oxytocin, vasopressin and sociality. Progress in Brain Research, 170, 331-6.
11. Cheng, Y., Chen, C., Lin, C.P., Chou, K.H., Decety, J. (2010). Love hurts: an fMRI study. Neuroimage, 51(2), 923-9.
12. Coan, J.A., Allen, J.J., editors. (2007). Handbook of Emotion Elicitation and Assessment. New York: Oxford University Press.
13. D'Argembeau, A., Feyers, D., Majerus, S., et al. (2008). Self-reflection across time: cortical midline structures differentiate between present and past selves. Social Cognitive and Affective Neuroscience, 3(3), 244-52.
14. D'Argembeau, A., Ruby, P., Collette, F., et al. (2007). Distinct regions of the medial prefrontal cortex are associated with self-referential processing and perspective taking. Journal of Cognitive Neuroscience, 19(6), 935-44.
15. D'Argembeau, A., Stawarczyk, D., Majerus, S., et al. (2009). The neural basis of personal goal processing when envisioning future events. Journal of Cognitive Neuroscience, 22(8), 1701-13.
16. D'Esposito, M. (2000). Functional neuroimaging of cognition. Seminars in Neurology, 20(4), 487-98.
17. Damasio, A. (2003). Feelings of emotion and the self. Annual New York Academy of Science, 1001, 253-61.
18. Damasio, A., Grabowski, T., Bechara, A., et al. (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience, 3(10), 1049-56.
19. Daselaar, S.M., Rice, H.J., Greenberg, D.L., Cabeza, R., LaBar, K.S., Rubin, D.C. (2008). The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving. Cerebral Cortex, 18(1), 217-29.
20. Daselaar, S.M., Rombouts, S.A., Veltman, D.J., Raaijmakers, J.G., Lazeron, R.H., Jonker, C. (2001). Parahippocampal activation during successful recognition of words: a self-paced event-related fMRI study. Neuroimage, 13(6), 1113-20.
21. Decety, J., Echols, S., Correll, J. (2009). The blame game: The effect of responsibility and social stigma on empathy for pain. Journal of Cognitive Neuroscience, 22(5), 985-97.
22. Decety, J., Jackson, P.L. (2004). The functional architecture of human empathy. Behavioral Cognitive Neuroscience Review, 3(2), 71-100.
23. Eisenberg, N., Fabes, R.A., Miller, P.A., Fultz, J., Shell, R., Mathy, R.M. (1989). Relation of sympathy and personal distress to prosocial behavior: a multimethod study. Journal of Personality and Social Psychology, 57, 55-66.
24. Eisenberg, N., Guthrie, I.K., Cumberland, A., et al. (2002). Prosocial development in early adulthood: a longitudinal study. Journal of Personality & Social Psychology, 82, 993-1006.
25. Figueira, R.J., Peabody, M.F., Lonstein, J.S. (2008). Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. Behavioral Neuroscience, 122(3), 618-28.
26. Fossati, P., Hevenor, S.J., Graham, S.J., et al. (2003). In search of the emotional self: an FMRI study using positive and negative emotional words. American Journal of Psychiatry, 160(11), 1938-45.
27. Goetz, J., Keltner, D., Simon-Thomas, E.R. (2010). Is compassion a distinct emotion? An integrated review of four hypotheses. Psychological Bulletin, 136(3), 351-74.
28. Gordon, I., Zagoory-Sharon, O., Leckman, J.F., Feldman, R. (2010). Oxytocin and the development of parenting in humans. Biological Psychiatry, 68(4), 377-82.
29. Gross, J.J., Sutton, S.K., Ketalaar, T. (1998). Relations between affect and personality: support for the affect-level and affective-reactivity views. Personality and Social Psychology Bulletin, 24(3), 279.
30. Harris, L.T., McClure, S.M., van den Bos, W., Cohen, J.D., Fiske, S.T. (2007). Regions of the MPFC differentially tuned to social and nonsocial affective evaluation. Cognitive Affective and Behavioral Neuroscience, 7(4), 309-16.
31. Heatherton, T.F., Wyland, C.L., Macrae, C.N., Demos, K.E., Denny, B.T., Kelley, W.M. (2006). Medial prefrontal activity differentiates self from close others. Social Cognitive and Affective Neuroscience, 1(1), 18-25.
32. Heinricher, M.M., Tavares, I., Leith, J.L., Lumb, B.M. (2009). Descending control of nociception: specificity, recruitment and plasticity. Brain Research Review, 60(1), 214-25.
33. Hertenstein, M., Keltner, D., App, B., Bulleit, B.A., Jaskolka, A.R. (2006). Touch communicates discrete emotions. Emotion, 6(3), 528-33.
34. Hooker, C., Verosky, S., Germine, L., Knight, R., D'Esposito, M. (2010). Neural activity during social signal perception correlates with self-reported empathy. Brain Research, 1308, 100-13.
35. Hooker, C.I., Verosky, S.C., Germine, L.T., Knight, R.T., D'Esposito, M. (2008). Mentalizing about emotion and its relationship to empathy. Social Cognitive and Affective Neuroscience, 3, 204-17.
36. Hutcherson, C.A., Goldin, P.R., Ochsner, K.N., Gabrieli, J.D., Barrett, L.F., Gross, J.J. (2005). Attention and emotion: does rating emotion alter neural responses to amusing and sad films? Neuroimage, 27(3), 656-68.
37. Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J.C., Rizzolatti, G. (2005). Grasping the intentions of others with one's own mirror neuron system. Public Library of Science: Biology, 3(3), 529-35.
38. Immordino-Yang, M.H., McColl, A., Damasio, H., Damasio, A. (2009). Neural correlates of admiration and compassion. Proceedings of the National Academy of Science, 106(19), 8021-6.
39. Insel, T.R., Gingrich, B.S., Young, L.J. (2001). Oxytocin: who needs it? Progress in Brain Research, 133, 59-66.
40. Johnson, M.K., Raye, C.L., Mitchell, K.J., Touryan, S.R., Greene, E.J., Nolen-Hoeksema, S. (2006). Dissociating medial frontal and posterior cingulate activity during self-reflection. Social Cognitive and Affective Neuroscience, 1(1), 56-64.
41. Kelley, W.M., Macrae, C.N., Wyland, C.L., Caglar, S., Inati, S., Heatherton, T.F. (2002). Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience, 14(5), 785-94.
42. Keltner, D., Lerner, J.S. (2010). Emotion. In: Gilbert, D.T., Fiske, S.T., Lindsay, G., editors. The Handbook of Social Psychology 5 edn. New York: McGraw, pp. 312-47.
43. Kim, J.W., Kim, S.-E., Kim, J.-J., et al. (2009). Compassionate attitude towards others' suffering activates the mesolimbic neural system. Neuropsychologia, 47(10), 2073-81.
44. Kjaer, T.W., Nowak, M., Lou, H.C. (2002). Reflective self-awareness and conscious states: PET evidence for a common midline parietofrontal core. Neuroimage, 17(2), 1080-6.
45. Lamm, C., Batson, C.D., Decety, J. (2007). The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience, 19(1), 42-58.
46. Lang, P.J. (1999). The International Affective Picture System. Gainesville, FL: University of Florida.
47. Lazarus, R.S. (1991). Emotion and Adaptation. New York: Oxford University Press.
48. Lerner, J.S., Keltner, D. (2001). Fear, anger, and risk. Journal of Personality and Social Psychology, 81(1), 146-59.
49. Lieberman, M.D., Cunningham, W.A. (2009). Type I and Type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience, 4(4), 423-8.
50. Lieberman, M.D., Jarcho, J.M., Satpute, A.B. (2004). Evidence-based and intuition-based self-knowledge: an FMRI study. Journal of Personality and Social Psychology, 87(4), 421-35.
51. Lonstein, J.S., De Vries, G.J. (2000). Maternal behaviour in lactating rats stimulates c-fos in glutamate decarboxylase-synthesizing neurons of the medial preoptic area, ventral bed nucleus of the stria terminalis, and ventrocaudal periaqueductal gray. Neuroscience, 100(3), 557-68.
52. Lonstein, J.S., Stern, J.M. (1997). Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c-fos and electrolytic lesion studies in lactating rats. Journal of Neuroscience, 17(9), 3364-78.
53. Lovick, T.A., Adamec, R. (2009). The Periaqueductal Gray (PAG). Neural Plasticity, 2009, 360907.
54. Macrae, C.N., Moran, J.M., Heatherton, T.F., Banfield, J.F., Kelley, W.M. (2004). Medial prefrontal activity predicts memory for self. Cerebral Cortex, 14(6), 647-54.
55. Maddock, R.J., Garrett, A.S., Buonocore, M.H. (2001). Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval. Neuroscience, 104(3), 667-76.
56. Maddock, R.J., Garrett, A.S., Buonocore, M.H. (2003). Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Human Brain Mapping, 18(1), 30-41.
57. Mathur, V.A., Harada, T., Lipke, T., Chiao, J.Y. (2010). Neural basis of extraordinary empathy and altruistic motivation. Neuroimage, 51(4), 1468-75.
58. Mikulincer, M., Shaver, P.R., Gillath, O., Nitzberg, R.A. (2005). Attachment, caregiving, and altruism: boosting attachment security increases compassion and helping. Journal of Personality and Social Psychology, 89, 817-39.
59. Mitchell, J.P., Banaji, M.R., Macrae, C.N. (2005a). General and specific contributions of the medial prefrontal cortex to knowledge about mental states. Neuroimage, 28(4), 757-62.
60. Mitchell, J.P., Banaji, M.R., Macrae, C.N. (2005b). The link between social cognition and self-referential thought in the medial prefrontal cortex. Journal of Cognitive Neuroscience, 17(8), 1306-15.
61. Montague, P.R., King-Casas, B., Cohen, J.D. (2006). Imaging valuation models in human choice. Annual Review of Neuroscience, 29, 417-48.
62. Nitschke, J.B., Nelson, E.E., Rusch, B.D., Fox, A.S., Oakes, T.R., Davidson, R.J. (2004). Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. Neuroimage, 21(2), 583-92.
63. Noriuchi, M., Kikuchi, Y., Senoo, A. (2008). The functional neuroanatomy of maternal love: mother's response to infant's attachment behaviors. Biological Psychiatry, 63(4), 415-23.
64. Northoff, G., Heinzel, A., Bermpohl, F., et al. (2004). Reciprocal modulation and attenuation in the prefrontal cortex: an fMRI study on emotional-cognitive interaction. Human Brain Mapping, 21(3), 202-12.
65. Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., Panksepp, J. (2006). Self-referential processing in our brain-a meta-analysis of imaging studies on the self. Neuroimage, 31(1), 440-57.
66. Numan, M., Numan, M.J. (1997). Projection sites of medial preoptic area and ventral bed nucleus of the stria terminalis neurons that express Fos during maternal behavior in female rats. Journal of Neuroendocrinology, 9(5), 369-84.
67. Ochsner, K.N., Knierim, K., Ludlow, D.H., et al. (2004). Reflecting upon feelings: an fMRI study of neural systems supporting the attribution of emotion to self and other. Journal of Cognitive Neuroscience, 16(10), 1746-72.
68. Oveis, C., Cohen, A.B., Gruber, J., Shiota, L., Haidt, J., Keltner, D. (2009). Resting respiratory sinus arrhythmia is associated with tonic positive emotionality. Emotion, 9, 265-70.
69. Oveis, C., Horberg, E.J., Keltner, D. (2010). Compassion, pride, and social intuitions of self-other similarity. Journal of Personality and Social Psychology, 98(4), 618-30.
70. Pelphrey, K.A., Morris, J.P., Michelich, C.R., Allison, T., McCarthy, G. (2005). Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. Cerebral Cortex, 15(12), 1866-76.
71. 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), 2076-85.
72. Reniers, R.L., Corcoran, R., Drake, R., Shryane, N.M., Vollm, B.A. (2011). The QCAE: a Questionnaire of Cognitive and Affective Empathy. Journal of Personality Assessment, 93(1), 84-95.
73. Rodrigues, S.M., Saslow, L.R., Garcia, N., John, O.P., Keltner, D. (2009). Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proceedings of the National Academy of Science USA, 106(50), 21437-41.
74. Rosen, G.J., de Vries, G.J., Goldman, S.L., Goldman, B.D., Forger, N.G. (2008). Distribution of oxytocin in the brain of a eusocial rodent. Neuroscience, 155(3), 809-17.
75. Rudebeck, P.H., Bannerman, D.M., Rushworth, M.F. (2008). The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making. Cognitive Affective and Behavioral Neuroscience, 8(4), 485-97.
76. Saarela, M.V., Hlushchuk, Y., Williams, A.C., Schurmann, M., Kalso, E., Hari, R. (2007). The compassionate brain: humans detect intensity of pain from another's face. Cerebral Cortex, 17(1), 230-7.
77. Saxe, R., Powell, L.J. (2006). It's the thought that counts: specific brain regions for one component of theory of mind. Psychological Science, 17(8), 692-9.
78. Saxe, R., Wexler, A. (2005). Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia, 43(10), 1391-9.
79. Shahrokh, D.K., Zhang, T.Y., Diorio, J., Gratton, A., Meaney, M.J. (2010). Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology, 151(5), 2276-86.
80. Shamay-Tsoory, S.G., 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(Pt 3), 617-27.
81. Simon-Thomas, E.R., Keltner, D., Sauter, D.A., Sinicropi-Yao, L., Abramson, A. (2009). The voice conveys specific emotions: evidence from vocal burst displays. Emotion, 9(6), 838-46.
82. Singer, T. (2006). The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neuroscience Biobehavioral Review, 30(6), 855-63.
83. Singer, T., Frith, C. (2005). The painful side of empathy. Nature Neuroscience, 8(7), 845-6.
84. Singer, T., Lamm, C. (2009). The social neuroscience of empathy. Annual New York Academy of Science, 1156, 81-96.
85. Smith, C.A., Ellsworth, P.C. (1985). Patterns of cognitive appraisal in emotion. Journal of Personality and Social Psychology, 48, 813-38.
86. Stack, E.C., Balakrishnan, R., Numan, M.J., Numan, M. (2002). A functional neuroanatomical investigation of the role of the medial preoptic area in neural circuits regulating maternal behavior. Behavioral Brain Research, 131(1-2), 17-36.
87. Sturgis, J.D., Bridges, R.S. (1997). N-methyl-DL-aspartic acid lesions of the medial preoptic area disrupt ongoing parental behavior in male rats. Physiology of Behavior, 62(2), 305-10.
88. Sugiura, M., Shah, N.J., Zilles, K., Fink, G.R. (2005a). Cortical representations of personally familiar objects and places: functional organization of the human posterior cingulate cortex. Journal of Cognitive Neuroscience, 17(2), 183-98.
89. Sugiura, M., Watanabe, J., Maeda, Y., Matsue, Y., Fukuda, H., Kawashima, R. (2005b). Cortical mechanisms of visual self-recognition. Neuroimage, 24(1), 143-9.
90. Swain, J.E. (2008). Baby stimuli and the parent brain: functional neuroimaging of the neural substrates of parent-infant attachment. Psychiatry, 5(8), 28-36.
91. Swain, J.E. (2010). The human parental brain: In vivo neuroimaging. Progress in Neuropsychopharmacology Biological Psychiatry, 35, 1242-54.
92. Takahashi, H., Matsuura, M., Koeda, M., et al. (2008). Brain activations during judgments of positive self-conscious emotion and positive basic emotion: pride and joy. Cerebral Cortex, 18(4), 898-903.
93. Tracy, J.L., Robins, R.W. (2004). Show your pride: evidence for a discrete emotion expression. Psychological Science, 15(3), 194-7.
94. Tracy, J.L., Robins, R.W. (2007). The psychological structure of pride: a tale of two facets. Journal of Personality and Social Psychology, 92(3), 506-25.
95. Tracy, J.L., Robins, R.W., Tangney, J.P. (2007). The Self-Conscious Emotions: Theory and Research. New York: Guilford Press.
96. Worsley, K.J., Friston, K.J. (1995). Analysis of fMRI time-series revisited -again. NeuroImage, 2, 173-81.
97. Zahn, R., Moll, J., Krueger, F., Huey, E.D., Garrido, G., Grafman, J. (2007). Social concepts are represented in the superior anterior temporal cortex. Proceedings of the National Academy of Science USA, 104(15), 6430-5.