The neural basis of empathy

Annual Review of Neuroscience

Volumn 35, Issue , 2012, Pages 1-23

  Bernhardt, Boris C ^a   Singer, Tania ^a  

^a MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

Author keywords

cingulate cortex; emotion; fMRI; insula; social neuroscience

Indexed keywords

ALEXITHYMIA; ANGER; ANTERIOR CINGULATE; ANTERIOR INSULA; ANXIETY; CELL ACTIVATION; CINGULATE GYRUS; COMPASSIONATE USE; DIFFUSION TENSOR IMAGING; EMOTION; EMPATHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMISPHERE; HOMEOSTASIS; HUMAN; INFERIOR FRONTAL GYRUS; NERVE CELL; NEUROIMAGING; NONHUMAN; PAIN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RETROSPLENIAL CORTEX; REVIEW; SOCIAL COGNITION; SOCIAL INTERACTION; TRANSCRANIAL MAGNETIC STIMULATION;

BRAIN MAPPING; CEREBRAL CORTEX; EMPATHY; GYRUS CINGULI; HUMANS; NEURAL PATHWAYS; PAIN; SOCIAL BEHAVIOR;

EID: 84862645807     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-062111-150536     Document Type: Review

References (160)

1. Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, et al. 2010. The von Economo neurons in the frontoinsular and anterior cingulate cortex. Ann. N. Y. Acad. Sci. 1225:59-71
2. Amaral DG, Price JL. 1984. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230:465-96 (Pubitemid 15183874)
3. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. 2005. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 9:463-84 (Pubitemid 40836040)
4. Augustine JR. 1996. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Brain Res. Rev. 22:229-44 (Pubitemid 26390178)
5. Avenanti A, Bueti D, Galati G, Aglioti SM. 2005. Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat. Neurosci. 8:955-60
6. Avenanti A, Minio-Paluello I, Bufalari I, Aglioti SM. 2006. Stimulus-driven modulation of motor-evoked potentials during observation of others' pain. Neuroimage 32:316-24
7. 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. 34:163-75 (Pubitemid 39023470)
8. Batson CD. 2009. These things called empathy. In The Social Neuroscience of Empathy, ed. J Decety, WIckes, pp. 16-31. Cambridge, MA: MIT Press
9. Batson CD, Eklund JH, Chermok VL, Hoyt JL, Ortiz BG. 2007. An additional antecedent of empathic concern: valuing the welfare of the person in need. J. Pers. Soc. Psychol. 93:65-74
10. Baumeister RF, Vohs KD. 2007. Encyclopedia of Social Psychology. Thousand Oaks, CA: Sage
11. Beckmann M, Johansen-Berg H, Rushworth MF. 2009. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 29:1175-90
12. Benuzzi F, Lui F, Duzzi D, Nichelli PF, Porro CA. 2008. Does it look painful or disgusting? Ask your parietal and cingulate cortex. J. Neurosci. 28:923-31 (Pubitemid 351159009)
13. Bingel U, Quante M, Knab R, Bromm B, Weiller C, Buchel C. 2003. Single trial fMRI reveals significant contralateral bias in responses to laser pain within thalamus and somatosensory cortices. Neuroimage 18:740-48 (Pubitemid 36349424)
14. Birbaumer N, Veit R, Lotze M, Erb M, Hermann C, et al. 2005. Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. Arch. Gen. Psychiatry 62:799-805 (Pubitemid 41002763)
15. Bird G, Silani G, Brindley R, White S, Frith U, Singer T. 2010. Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain 133:1515-25
16. Blair RJ. 2005. Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations. Conscious. Cogn. 14:698-718 (Pubitemid 41742032)
17. Blakemore SJ, Bristow D, Bird G, Frith C, Ward J. 2005. Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain 128:1571-83 (Pubitemid 41373676)
18. Boccardi M, GanzolaR, Rossi R, Sabattoli F, Laakso MP, et al. 2010. Abnormal hippocampal shape in offenders with psychopathy. Hum. Brain Mapp. 31:438-47
19. Botvinick M, Jha AP, Bylsma LM, Fabian SA, Solomon PE, Prkachin KM. 2005. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. Neuroimage 25:312-19 (Pubitemid 40289158)
20. Buchel C, Morris J, Dolan RJ, Friston KJ. 1998. Brain systems mediating aversive conditioning: an eventrelated fMRI study. Neuron 20:947-57 (Pubitemid 28247400)
21. Buckner RL, Carroll DC. 2007. Self-projection and the brain. Trends Cogn. Sci. 11:49-57 (Pubitemid 46176697)
22. Bullmore E, Sporns O. 2009. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10:186-98
23. Bushnell MC, Duncan GH, Hofbauer RK, Ha B, Chen JI, Carrier B. 1999. Pain perception: Is there a role for primary somatosensory cortex? Proc. Natl. Acad. Sci. USA 96:7705-9 (Pubitemid 29328344)
24. Caruana F, Jezzini A, Sbriscia-Fioretti B, Rizzolatti G, Gallese V. 2011. Emotional and social behaviors elicited by electrical stimulation of the insula in the macaque monkey. Curr. Biol. 21:195-99
25. Cauda F, D'Agata F, Sacco K, Duca S, Geminiani G, Vercelli A. 2011. Functional connectivity of the insula in the resting brain. Neuroimage 55:8-23
26. Cerliani L, Thomas R, Jbabdi S, Siero J, Nanetti L, et al. 2012. Probabilistic tractorgraphy recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex. Hum. Brain Mapp. doi: 10. 1002/hbm. 21338. In press
27. Cheng Y, Chen C, Lin CP, Chou KH, Decety J. 2010. Love hurts: an fMRI study. Neuroimage 51:923-29
28. Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW. 2009. Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proc. Natl. Acad. Sci. USA 106:8719-24
29. Corradi-Dell'Acqua C, Hofstetter C, Vuilleumier P. 2011. Felt and seen pain evoke the same local patterns of cortical activity in insula and cingulate cortex. J. Neurosci. 31(49):17996-8006
30. Craig AD. 2002. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3:655-66 (Pubitemid 135706673)
31. Craig AD. 2003. Pain mechanisms: labeled lines versus convergence in central processing. Annu. Rev. Neurosci. 26:1-30 (Pubitemid 37064926)
32. Craig AD. 2009. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10:59-70
33. Craig KD. 2004. Social communication of pain enhances protective functions: a comment on Deyo, Prkachin and Mercer 2004. Pain 107:5-6 (Pubitemid 38058692)
34. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. 2004. Neural systems supporting interoceptive awareness. Nat. Neurosci. 7:189-95 (Pubitemid 38129796)
35. Davis MH. 1983. Measuring individual differences in empathy: evidence for a multidimensional approach. J. Pers. Soc. Psychol. 44:113-26
36. de Gelder B, Snyder J, Greve D, Gerard G, Hadjikhani N. 2004. Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body. Proc. Natl. Acad. Sci. USA 101:16701-6 (Pubitemid 39557776)
37. de Greck M, Wang G, Yang X, Wang X, Northoff G, Han S. 2012. Neural substrates underlying intentional empathy. Soc. Cogn. Affect. Neurosci. doi: 10. 1093/scan/nsq093. In press
38. de Vignemont F, Singer T. 2006. The empathic brain: how, when and why? Trends Cogn. Sci. 10:435-41 (Pubitemid 44415572)
39. Decety J, Echols S, Correll J. 2009a. The blame game: the effect of responsibility and social stigma on empathy for pain. J. Cogn. Neurosci. 22:985-97
40. Decety J, Michalska KJ. 2010. Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev. Sci. 13:886-99
41. Decety J, Michalska KJ, Akitsuki Y, Lahey BB. 2009b. Atypical empathic responses in adolescents with aggressive conduct disorder: a functional MRI investigation. Biol. Psychol. 80:203-11
42. Deen B, Pitskel NB, Pelphrey KA. 2011. Three systems of insular functional connectivity identified with cluster analysis. Cereb. Cortex 21(7):1498-506
43. Derbyshire SW. 2000. Exploring the pain "neuromatrix". Curr. Rev. Pain 4:467-77
44. Devinsky O, Morrell MJ, Vogt BA. 1995. Contributions of anterior cingulate cortex to behaviour. Brain 118(Pt. 1):279-306
45. Duerden EG, Albanese M-C. 2012. Localization of pain-related brain activation: a meta-analysis of neuroimaging data. Hum. Brain Mapp. doi: 10. 1002/hbm. 21416. In press
46. Dum RP, Levinthal DJ, Strick PL. 2009. The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J. Neurosci. 29:14223-35
47. Ebisch SJ, Perrucci MG, Ferretti A, DelGratta C, Romani GL, Gallese V. 2008. The sense of touch: embodied simulation in a visuotactile mirroring mechanism for observed animate or inanimate touch. J. Cogn. Neurosci. 20:1611-23
48. Eisenberg N. 2000. Emotion, regulation, and moral development. Annu. Rev. Psychol. 51:665-97
49. Eisenberg N, Fabes RA. 1990. Empathy: conceptualization, measurement, and relation to prosocial behavior. Motiv. Emot. 14:131-49
50. Fan Y, Duncan NW, de Greck M, Northoff G. 2011. Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci. Biobehav. Rev. 35:903-11
51. Fehr E. 2008. Social preferences and the brain. In Neuroeconomics: Decision Making and the Brain, ed. PW Glimcher, E Fehr, C Camerer, A Rangel, RA Poldrack, pp. 215-35. London, UK: Academic/Elsevier
52. Frith CD, Frith U. 2006. The neural basis of mentalizing. Neuron 50:531-34
53. Frith U, Frith CD. 2003. Development and neurophysiology of mentalizing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358:459-73 (Pubitemid 36386247)
54. Fudge JL, Breitbart MA, Danish M, Pannoni V. 2005. Insular and gustatory inputs to the caudal ventral striatum in primates. J. Comp. Neurol. 490:101-18 (Pubitemid 41140983)
55. Gallay DS, Gallay MN, Jeanmonod D, Rouiller EM, Morel A. 2012. The insula of reil revisited: multiarchitectonic organization in macaque monkeys. Cereb. Cortex 22(1):175-90
56. Gallese V, Keysers C, Rizzolatti G. 2004. A unifying view of the basis of social cognition. Trends Cogn. Sci. 8:396-403 (Pubitemid 39179902)
57. Grill-Spector K, Malach R. 2001. fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol. (Amst. ) 107:293-321 (Pubitemid 33647324)
58. Grinband J, Hirsch J, Ferrera VP. 2006. A neural representation of categorization uncertainty in the human brain. Neuron 49:757-63 (Pubitemid 43290134)
59. Gu X, Han S. 2007. Attention and reality constraints on the neural processes of empathy for pain. Neuroimage 36:256-67 (Pubitemid 46617945)
60. Gu X, Liu X, Guise KG, Naidich TP, Hof PR, Fan J. 2010. Functional dissociation of the frontoinsular and anterior cingulate cortices in empathy for pain. J. Neurosci. 30:3739-44
61. Halifax J. 2010. The precious necessity of compassion. J. Pain Symptom Manag. 41(1):146-53
62. Hardy SG, Leichnetz GR. 1981. Cortical projections to the periaqueductal gray in the monkey: a retrograde and orthograde horseradish peroxidase study. Neurosci. Lett. 22:97-101 (Pubitemid 11157834)
63. Harrison NA, Singer T, Rotshtein P, Dolan RJ, Critchley HD. 2006. Pupillary contagion: central mechanisms engaged in sadness processing. Soc. Cogn. Affect. Neurosci. 1:5-17
64. 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 68:149-60
65. Henson RN, Rugg MD. 2003. Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia 41:263-70 (Pubitemid 35365956)
66. Hill E, Berthoz S, Frith U. 2004. Brief report: cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. J. Autism Dev. Disord. 34:229-35 (Pubitemid 39023476)
67. HoffmanML. 2000. Empathy andMoral Development: Implications for Caring and Justice. New York: Cambridge Univ. Press
68. Hojat M, Vergare MJ, Maxwell K, Brainard G, Herrine SK, et al. 2009. The devil is in the third year: a longitudinal study of erosion of empathy in medical school. Acad. Med. 84:1182-91
69. Huettel SA, Stowe CJ, Gordon EM, Warner BT, PlattML. 2006. Neural signatures of economic preferences for risk and ambiguity. Neuron 49:765-75 (Pubitemid 43290135)
70. Immordino-Yang MH, McColl A, Damasio H, Damasio A. 2009. Neural correlates of admiration and compassion. Proc. Natl. Acad. Sci. USA 106:8021-26
71. Jabbi M, Bastiaansen J, Keysers C. 2008. A common anterior insula representation of disgust observation, experience and imagination shows divergent functional connectivity pathways. PLoS One 3:e 2939
72. Jabbi M, Swart M, Keysers C. 2007. Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 34:1744-53 (Pubitemid 46187071)
73. 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 44:752-61 (Pubitemid 43327398)
74. Jackson PL, Meltzoff AN, Decety J. 2005. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 24:771-79 (Pubitemid 40094559)
75. Keysers C, Gazzola V. 2007. Integrating simulation and theory of mind: from self to social cognition. Trends Cogn. Sci. 11:194-96 (Pubitemid 46654819)
76. Keysers C, Kaas JH, Gazzola V. 2010. Somatosensation in social perception. Nat. Rev. Neurosci. 11:417-28
77. Keysers C, Wicker B, Gazzola V, Anton JL, Fogassi L, Gallese V. 2004. A touching sight: SII/PV activation during the observation and experience of touch. Neuron 42:335-46 (Pubitemid 38501654)
78. Kiehl KA, Smith AM, Hare RD, Mendrek A, Forster BB, et al. 2001. Limbic abnormalities in affective processing by criminal psychopaths as revealed by functionalmagnetic resonance imaging. Biol. Psychiatry 50:677-84 (Pubitemid 33043770)
79. Klimecki O, Leihberg S, Lamm C, Singer T. 2011. Neural and behavioral changes related to compassion training. Poster presented at "The Social Brain" workshop, Cambridge, UK
80. Klimecki O, Singer T. 2012. Empathic distress fatigue rather than compassion fatigue? Integrating findings from empathy research in psychology and neuroscience. In Pathological Altruism, ed. B Oakley, A Knafo, G Madhavan, DS Wilson, pp. 368-84. New York: Springer
81. Klingler J, Ludwig E. 1956. Atlas cerebri humani. Der innere Bau des Gehirns, dargestellt aufGrund makroskopischer Pr̈aparate/The Inner Structure of the Brain Demonstrated on the Basis of Macroscopical Preparations. Basel: Karger
82. 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 8:737-52
83. Kong J, Gollub RL, Polich G, Kirsch I, Laviolette P, et al. 2008. A functional magnetic resonance imaging study on the neural mechanisms of hyperalgesic nocebo effect. J. Neurosci. 28:13354-62
84. Krach S, Cohrs JC, de Echeverria Loebell NC, Kircher T, Sommer J, et al. 2011. Your flaws are my pain: linking empathy to vicarious embarrassment. PLoS One 6:e18675
85. Kuhnen CM, Knutson B. 2005. The neural basis of financial risk taking. Neuron 47:763-70 (Pubitemid 41208013)
86. Kunishio K, Haber SN. 1994. Primate cingulostriatal projection: limbic striatal versus sensorimotor striatal input. J. Comp. Neurol. 350:337-56 (Pubitemid 24356002)
87. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB. 2010. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 214:519-34
88. Lamm C, Batson CD, Decety J. 2007a. The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J. Cogn. Neurosci. 19:42-58 (Pubitemid 46106022)
89. Lamm C, Decety J, Singer T. 2011. Meta-analytic evidence forcommonand distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 54:2492-502
90. Lamm C, Nusbaum HC, Meltzoff AN, Decety J. 2007b. What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS One 2:e1292
91. Leiberg S, Klimecki O, Singer T. 2011. Short-term compassion training increases prosocial behavior in a newly developed prosocial game. PLoS One 6:e17798
92. Lutz A, Brefczynski-Lewis J, Johnstone T, Davidson RJ. 2008. Regulation of the neural circuitry of emotion by compassion meditation: effects of meditative expertise. PLoS One 3:e1897
93. Lutz A, Greischar LL, Perlman DM, Davidson RJ. 2009. BOLD signal in insula is differentially related to cardiac function during compassion meditation in experts versus novices. Neuroimage 47:1038-46
94. Maihofner C, Herzner B, Otto Handwerker H. 2006. Secondary somatosensory cortex is important for the sensory-discriminative dimension of pain: a functional MRI study. Eur. J. Neurosci. 23:1377-83
95. Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP. 2007. Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:579-88 (Pubitemid 47444255)
96. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN. 2007. Wandering minds: the default network and stimulus-independent thought. Science 315:393-95 (Pubitemid 46175523)
97. Masten CL, Morelli SA, Eisenberger NI. 2011. An fMRI investigation of empathy for 'social pain' and subsequent prosocial behavior. Neuroimage 55:381-88
98. Medford N, Critchley HD. 2010. Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct. Funct. 214:535-49
99. Mehrabian A. 1997. Relations among personality scales of aggression, violence, and empathy: validational evidence bearing on the risk of eruptive violence scale. Aggress. Behav. 23:433-45 (Pubitemid 127359401)
100. Mesulam MM, Mufson EJ. 1982a. Insula of the old world monkey. I. Architectonics in the insulo-orbitotemporal component of the paralimbic brain. J. Comp. Neurol. 212:1-22 (Pubitemid 13208306)
101. Mesulam MM, Mufson EJ. 1982b. Insula of the old worldmonkey. III: Efferent cortical output and comments on function. J. Comp. Neurol. 212:38-52 (Pubitemid 13208308)
102. Mitchell JP. 2009. Inferences about mental states. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 364:1309-16
103. Mobbs D, Yu R, Meyer M, Passamonti L, Seymour B, et al. 2009. A key role for similarity in vicarious reward. Science 324:900
104. Morecraft RJ, McNeal DW, Stilwell-Morecraft KS, Gedney M, Ge J, et al. 2007. Amygdala interconnections with the cingulate motor cortex in the rhesus monkey. J. Comp. Neurol. 500:134-65 (Pubitemid 44904306)
105. Morrison I, Downing PE. 2007. Organization of felt and seen pain responses in anterior cingulate cortex. Neuroimage 37:642-51 (Pubitemid 47444248)
106. 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. 4:270-78 (Pubitemid 39167169)
107. Mufson EJ, Mesulam MM. 1982. Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. J. Comp. Neurol. 212:23-37 (Pubitemid 13208307)
108. Nanetti L, Cerliani L, Gazzola V, Renken R, Keysers C. 2009. Group analyses of connectivity-based cortical parcellation using repeated k-means clustering. Neuroimage 47:1666-77
109. Nemiah JC. 1977. Alexithymia. Theoretical considerations. Psychother. Psychosom. 28:199-206
110. Norman KA, Polyn SM, Detre GJ, Haxby JV. 2006. Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn. Sci. 10:424-30 (Pubitemid 44308461)
111. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. 2004. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304:452-54 (Pubitemid 38495943)
112. Pandya DN, Van Hoesen GW, Mesulam MM. 1981. Efferent connections of the cingulate gyrus in the rhesus monkey. Exp. Brain Res. 42:319-30 (Pubitemid 11112361)
113. Paulus MP, Rogalsky C, Simmons A, Feinstein JS, Stein MB. 2003. Increased activation in the right insula during risk-taking decisionmaking is related to harm avoidance and neuroticism. Neuroimage 19:1439-48 (Pubitemid 37025843)
114. Paus T. 2001. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat. Rev. Neurosci. 2:417-24 (Pubitemid 33674798)
115. Peyron R, Laurent B, Garcia-Larrea L. 2000. Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol. Clin. 30:263-88
116. Phillips ML, Gregory LJ, Cullen S, Coen S, Ng V, et al. 2003. The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation. Brain 126:669-84 (Pubitemid 36240867)
117. Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, et al. 1999. Dissociating pain from its anticipation in the human brain. Science 284:1979-81 (Pubitemid 29309443)
118. Ploner M, Freund HJ, Schnitzler A. 1999. Pain affect without pain sensation in a patient with a postcentral lesion. Pain 81:211-14 (Pubitemid 29199918)
119. Porro CA, Baraldi P, Pagnoni G, Serafini M, Facchin P, et al. 2002. Does anticipation of pain affect cortical nociceptive systems? J. Neurosci. 22:3206-14 (Pubitemid 35379207)
120. Prehn-Kristensen A, Wiesner C, Bergmann TO, Wolff S, Jansen O, et al. 2009. Induction of empathy by the smell of anxiety. PLoS One 4:e5987
121. Preston SD, de Waal FB. 2002. Empathy: its ultimate and proximate bases. Behav. Brain Sci. 25:1-20; discussion-71 (Pubitemid 36150071)
122. Preuschoff K, Quartz SR, Bossaerts P. 2008. Human insula activation reflects risk prediction errors as well as risk. J. Neurosci. 28:2745-52 (Pubitemid 351398874)
123. Price DD. 2000. Psychological and neural mechanisms of the affective dimension of pain. Science 288:1769-72 (Pubitemid 30399009)
124. Prinz W. 1984. Modes of linkages between perception and actions. In Cognition and Motor Processes, ed. W Prinz, AF Sanders, pp. 185-93. Berlin: Springer
125. Prinz W. 2005. Experimental approaches to action. In Agency and Self-Awareness, ed. J Roessler, N Eilan, pp. 165-87. New York: Oxford Univ. Press
126. Rainville P. 2002. Brain mechanisms of pain affect and pain modulation. Curr. Opin. Neurobiol. 12:195-204 (Pubitemid 34518340)
127. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. 1997. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968-71 (Pubitemid 27366684)
128. Riem MM, Bakermans-Kranenburg MJ, Pieper S, Tops M, Boksem MA, et al. 2011. Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol. Psychiatry 70(3):291-7
129. Rizzolatti G, Fogassi L, Gallese V. 2001. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat. Rev. Neurosci. 2:661-70 (Pubitemid 33674057)
130. Rolls ET. 2004. The functions of the orbitofrontal cortex. Brain Cogn. 55:11-29 (Pubitemid 38591427)
131. 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 17:230-37 (Pubitemid 44973911)
132. Salminen JK, Saarijarvi S, Aarela E, Toikka T, Kauhanen J. 1999. Prevalence of alexithymia and its association with sociodemographic variables in the general population of Finland. J. Psychosom. Res. 46:75-82 (Pubitemid 29030512)
133. Saxe R, Kanwisher N. 2003. People thinking about people. The role of the temporo-parietal junction in "theory of mind". Neuroimage 19(4):1835-42 (Pubitemid 37025879)
134. Schooler JW, Smallwood J, Christoff K, Handy TC, Reichle ED, Sayette MA. 2011. Meta-awareness, perceptual decoupling and the wandering mind. Trends Cogn. Sci. 15(7):319-26
135. SchultzW. 2000. Multiple reward signals in the brain. Nat. Rev. Neurosci. 1:199-207
136. Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, et al. 2006. Early frontotemporal dementia targets neurons unique to apes and humans. Ann. Neurol. 60:660-67 (Pubitemid 46048483)
137. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, et al. 2007. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27:2349-56 (Pubitemid 46340968)
138. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ. 2011. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12:154-67
139. 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 132:617-27
140. Silani G, Bird G, Brindley R, Singer T, Frith C, Frith U. 2008. Levels of emotional awareness and autism: an fMRI study. Soc. Neurosci. 3:97-112
141. Singer T. 2006. The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neurosci. Biobehav. Rev. 30:855-63 (Pubitemid 44292288)
142. Singer T, Critchley HD, Preuschoff K. 2009. A common role of insula in feelings, empathy and uncertainty. Trends Cogn. Sci. 13:334-40
143. Singer T, Lamm C. 2009. The social neuroscience of empathy. Ann. N. Y. Acad. Sci. 1156:81-96
144. 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 303:1157-62 (Pubitemid 38233574)
145. 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 439:466-69 (Pubitemid 43152836)
146. Singer T, Snozzi R, Bird G, Petrovic P, Silani G, et al. 2008. Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Emotion 8:781-91
147. Singer T, SteinbeisN. 2009. Differential roles of fairness-and compassion-based motivations for cooperation, defection, and punishment. Ann. N. Y. Acad. Sci. 1167:41-50
148. Smallwood J, Schooler JW. 2006. The restless mind. Psychol. Bull. 132:946-58 (Pubitemid 44665373)
149. Sridharan D, Levitin DJ, Menon V. 2008. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc. Natl. Acad. Sci. USA 105:12569-74
150. Sterzer P, Stadler C, Poustka F, Kleinschmidt A. 2007. A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy. Neuroimage 37:335-42 (Pubitemid 47068977)
151. Taylor KS, Seminowicz DA, Davis KD. 2009. Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 30:2731-45
152. Tiihonen J, Rossi R, Laakso MP, Hodgins S, Testa C, et al. 2008. Brain anatomy of persistent violent offenders: more rather than less. Psychiatry Res. 163:201-12
153. Ture U, Yasargil DC, Al-Mefty O, Yasargil MG. 1999. Topographic anatomy of the insular region. J. Neurosurg. 90:720-33 (Pubitemid 29152861)
154. Van Overwalle F. 2009. Social cognition and the brain: a meta-analysis. Hum. Brain Mapp. 30:829-58
155. Vogt BA, Pandya DN. 1987. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J. Comp. Neurol. 262:271-89 (Pubitemid 17114121)
156. Vogt BA, Vogt L, Farber NB, Bush G. 2005. Architecture and neurocytology of monkey cingulate gyrus. J. Comp. Neurol. 485:218-39 (Pubitemid 40471300)
157. Von Economo C. 1926. Eine neue art spezialzellen des lobus cinguli und lobus insulae. Zschr. Ges. Neurol. Psychiat. 100:706-12
158. Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G. 2003. Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 40:655-64 (Pubitemid 37494712)
159. Wispe L. 1986. The distinction between sympathy and empathy: to call forth a concept, a word is needed. J. Pers. Soc. Psychol. 50:314-21
160. Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD. 2011. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 8(8):665-70