Empathic brain responses in insula are modulated by levels of alexithymia but not autism

Brain

Volumn 133, Issue 5, 2010, Pages 1515-1525

  Bird, Geoffrey ^a,b   Silani, Giorgia ^c   Brindley, Rachel ^b   White, Sarah ^b   Frith, Uta ^b   Singer, Tania ^c  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Alexithymia; Anterior insula; Autism; Empathy; Interoception; Mentalizing; Theory of mind

Indexed keywords

ADULT; ALEXITHYMIA; ARTICLE; ATTENTION; AUTISM; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EMPATHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEALTH SURVEY; HUMAN; INSULA; MALE; PRIORITY JOURNAL; RECOGNITION;

ADULT; AFFECTIVE SYMPTOMS; ANALYSIS OF VARIANCE; AUTISTIC DISORDER; CEREBRAL CORTEX; ELECTRIC STIMULATION; EMPATHY; HAND; HUMANS; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; PAIN MEASUREMENT; PAIN THRESHOLD; QUESTIONNAIRES; YOUNG ADULT;

EID: 77951908301     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq060     Document Type: Article

References (94)

1. Adolphs R. Looking at other people: mechanisms for social perception revealed in subjects with focal amygdala damage. Novartis Found Symp 2007; 278: 146-159
2. Adolphs R, Sears L, Piven J. Abnormal processing of social information from faces in autism. J Cognitive Neurosci 2001; 13: 232-240
3. Adolphs R, Spezio ML, Parlier M, Piven J. Distinct face processing strategies in parents of autistic children. Curr Biol 2008; 18: 1090-1093
4. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. Washington, D.C.: Author; 1994.
5. Bagby RM, Parker JD, Taylor GJ. The Twenty-item Toronto Alexithymia Scale-II. Convergent, discriminant, and concurrent validity. J Psychosom Res 1994; 38: 33-40.
6. Baron-Cohen S. Autism: the empathizing-systemizing (E-S) theory. Ann NY Acad Sci 2009; 1156: 68-80.
7. Baron-Cohen S, Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord 2004; 34: 163-175
8. Baron-Cohen S, Wheelwright S, Jolliffe T. Is there a "language of the eyes"? Evidence from normal adults, and adults with autism or Asperger syndrome. Visual Cognition 1997; 4: 311-331 (Pubitemid 127700185)
9. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The "reading the mind in the eyes" test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 2001; 42: 241-251
10. Baron-Cohen S, Riviere A, Fukushima M, French D, Hadwin J, Cross P, et al. Reading the mind in the face: a cross-cultural and developmental study. Visual Cognition 1996; 3: 39-59.
11. Berscheid E, Snyder M, Ornoto AM. The Relationship Closeness Inventory: assessing the closeness of interpersonal relationships. J Pers Soc Psychol 1989; 57: 792-807.
12. Berthoz S, Hill EL. Reliability of the Bermond-Vorst Alexithymia Questionnaire: data from adults with autism spectrum disorder, their relatives and normal controls. Eur Psychiat 2005; 20: 291-298
13. Blair RJ. Neurobiological basis of psychopathy. Br J Psychiatry 2003; 182: 5-7.
14. Blair RJ. Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations. Conscious Cogn 2005; 14: 698-718.
15. Blair RJ, Frith U, Smith N, Abell F, Cipolotti L. Fractionation of visual memory: agency detection and its impairment in autism. Neuropsychologia 2002; 40: 108-118
16. Blair RJR. Fine cuts of empathy and the amygdala: dissociable deficits in psychopathy and autism. Q J Exp Psychol 2008; 61: 157-170
17. Boucher J, Lewis V. Unfamiliar face recognition in relatively able autistic children. J Child Psychol Psychiat 1992; 33: 843-859
18. Brett M, Anton JL, Valabregue R, Poline JB. Region of interest analysis using the MarsBar toolbox for SPM 99. Neuroimage 2002; 16: S497.
19. Carr L, Iacoboni M, Dubeau MC, Mazziotta JC, Lenzi GL. 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 USA 2003; 100: 5497-5502
20. Cheng Y, Lin CP, Liu HL, Hsu YY, Lim KE, et al. Expertise modulates the perception of pain in others. Curr Bioly 2007; 17: 1708-1713
21. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 2002; 3: 655-666
22. Craig AD. Interoception: the sense of the physiological condition of the body. Curr Opin Neurol 2003; 13: 500-505
23. Craig AD. How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 2009; 10: 70.
24. Critchley HD. Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 2005; 493: 154-166
25. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. Neural system supporting interoceptive awareness. Nat Neurosci 2004; 7: 189-195
26. Damasio AR. Descartes' error and the future of human life. Sci Am 1994; 271: 144.
27. Davis MH. A multidimensional approach to individual differences in empathy. JSAS Catalogue of Selected Documents in Psychology 1980; 10: 85.
28. de Vignemont F, Singer T. The empathic brain: how, when and why? Trends Cogn Sci 2006; 10: 435-441
29. Decety J, Grè zes J. The power of simulation: Imagining one's own and other's behavior. Brain Res 2006; 1079: 4-14.
30. Decety J, Jackson PL. The functional architecture of human empathy. Behav Cogn Neurosci Rev 2004; 3: 71-100.
31. Decety J, Lamm C. Human empathy through the lens of social neu-roscience. Sci World J 2006; 6: 1146-1163
32. Deichmann R, Josephs O, Hutton C, Corfield DR, Turner R. Compensation of susceptibility-induced BOLD sensitivity losses in echoplanar fMRI imaging. Neuroimage 2002; 15: 120-135
33. Dziobek I, Rogers K, Fleck S, Bahnemann M, Heekeren HR, Wolf OT, et al. Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the Multifaceted Empathy Test (MET). J Autism Dev Disord 2008; 38: 464-473
34. Eisenberg N. Emotion, regulation, and moral development. Ann Rev Psychol 2000; 51: 665-697
35. Eisenberg N, Fabes RA. Empathy: conceptualization, measurement, and relation to prosocial behavior. Motiv Emotion 1990; 14: 131-149
36. Eisenberg N, Strayer JA. Empathy and its development. Cambridge, MA: Cambridge University Press; 1987.
37. Friston KJ, Ashburner J, Frith CD, Poline J-B, Heather JD, Frackowiack RSJ. Spatial registration and normalization of images. Hum Brain Mapp 1995a; 3: 165-189.
38. Friston KJ, Holmes AP, Worsley KJ, Poline J-B, Frith CD, Frackowiack RS. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995b; 2: 189-210.
39. Frith CD, Frith U. The neural basis of mentalizing. Neuron 2006; 50: 531-534
40. Frith U, Frith CD. Development and neurophysiology of mentalizing. Philos Trans R Soc Lond B Biol Sci 2003; 358: 459-473
41. Frith U, Happé F. Autism spectrum disorder. Curr Biol 2005; 15: R786-90.
42. Gillberg CL. The Emanuel Miller memorial lecture 1991: autism and autistic-like conditions: Subclasses among disorders of empathy. J Child Psychol Psychiat 1992; 33: 813-842
43. Gu X, Han S. Attention and reality constraints on the neural processes of empathy for pain. Neuroimage 2007; 36: 256-267
44. Hein G, Singer T. I feel how you feel but not always: the empathic brain and its modulation. Curr Opin Neurobiol 2008; 18: 153-158
45. Hill E, Berthoz S, Frith U. Brief report: cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. J Autism Dev Disord 2004; 34: 229-235
46. Hoffman ML. Empathy and moral development: implications for caring and justice. Cambridge, MA: Cambridge University Press; 2000.
47. Howard MA, Cowell PE, Boucher J, Broks P, Mayes A, Farrant A, et al. Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport 2000; 11: 1931-1935
48. Humphreys K, Minshew N, Leonard GL, Behrmann M. A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia 2007; 45: 685-695
49. Jabbi M, Swart M, Keysers C. Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 2007; 34: 1744-1753
50. Jackson PL, Meltzoff AN, Decety J. How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 2005; 24: 771-779
51. Jackson PL, Brunet E, Meltzoff AN, Decety J. Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia 2006; 44: 752-761
52. Johnson SA, Filliter JH, Murphy RR. Discrepancies between self-and parent-perceptions of autistic traits and empathy in high functioning children and adolescents on the autism spectrum. J Autism Dev Disord 2009; 39: 1706-1714
53. Keysers C, Gazzola V. Integrating simulation and theory of mind: from self to social cognition. Trends Cogn Sci 2007; 11: 194-196
54. Keysers C, Wicker B, Gazzola V, Anton JL, Fogassi L, Gallese V. A touching sight: SII/PV activation during the observation and experience of touch. Neuron 2004; 42: 335-346
55. Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch Gen Psychiat 2002; 59: 809-816
56. Klin A, Sparrow SS, de Bildt A, Cicchetti DV, Cohen DJ, Volkmar FR. A normed study of face recognition in autism and related disorders. J Autism Dev Disord 1999; 29: 499-508.
57. Lamm C, Batson CD, Decety J. The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. J Cogn Neurosci 2007a; 19: 42-58.
58. Lamm C, Nusbaum HC, Meltzoff AN, Decety J. What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS ONE 2007b; 2: e1292.
59. Linden W, Wen F, Paulhus DL. Measuring alexithymia: Reliability, validity, and prevalence. In: Butcher J, Spielberger C, editors. Advances in personality assessment. Hillsdale, NJ: Erlbaum; 1995. p. 51-95.
60. Lombardo MV, Barnes JL, Wheelwright SJ, Baron-Cohen S. Self-referential cognition and empathy in autism. PLoS ONE 2007; 2: e883.
61. Lord C, Risi S, Lambrecht L, EHJr Cook, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 2000; 30: 205-223
62. McIntosh DN, Reichmann-Decker A, Winkielman P, Wilbarger JL. When the social mirror breaks: deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. Dev Sci 2006; 9: 295-302.
63. Minio-Paluello I, Baron-Cohen S, Avenanti A, Walsh V, Aglioti SM. Absence of embodied empathy during pain observation in Asperger syndrome. Biol Psychiatry 2009; 65: 55-62.
64. Mitchell JP. Activity in right temporo-parietal junction is not selective for theory-of-mind. Cerebral Cortex 2008; 18: 262-271
65. Mitchell JP, Heatherton TF, Macrae CN. Distinct neural systems subserve person and object knowledge. Proc Natl Acad Sci USA 2002; 99: 15238-15243
66. Morrison I, Peelen MV, Downing PE. The sight of others' pain modulates motor processing in human cingulate cortex. Cereb Cortex 2007; 17: 2214-2222
67. Morrison I, Lloyd D, di Pellegrino G, Roberts N. Vicarious responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cogn Affect Behav Neurosci 2004; 4: 270-278
68. Nemiah JC, Freyberger H, Sifneos PE. Alexithymia: a view of the psychosomatic process. In: Hill OW, editor. Modern trends in psychosomatic medicine. London: Butterworths; 1976. p. 430-439
69. Pellicano E, Maybery M, Durkin K, Maley A. Multiple cognitive capabilities/deficits in children with an autism spectrum disorder: "Weak" central coherence and its relationship to theory of mind and executive control. Dev Psychopathol 2006; 18: 77-98.
70. Potthoff RF. Statistical aspects of the problem of biases in psychological tests (Institute of Statistics Mimeo Series No. 479). Chapel Hill, NC: University of North Carolina, Department of Statistics; 1966.
71. Premack D, Woodruff G. Does the chimpanzee have a theory of mind? Behav Brain Sci 1978; 1: 515-526
72. Preston SD, de Waal FBM. Empathy: its ultimate and proximate bases. Behav Brain Sci 2002; 25: 1-72.
73. Rogers K, Dziobek I, Hassenstab J, Wolf OT, Convit A. Who cares? Revisiting empathy in Asperger syndrome. J Autism Dev Disord 2007; 37: 709-715
74. Saarela MV, Hluschuk Y, Williams ACdC, Schü rmann M, Kalso E, Hari R. The compassionate brain: humans detect intensity of pain from another's face. Cereb Cortex 2007; 17: 230-237
75. Salminen JK, Saarijarvi S, Aarela E, Toikka T, Kauhanen J. Prevalence of alexithymia and its association with sociodemographic variables in the general population of Finland. J Psychosom Res 1999; 46: 75-82.
76. Saxe R. Uniquely human social cognition. Curr Opin Neurobiol 2006; 16: 235-239
77. Saxe R, Baron-Cohen S. The neuroscience of theory of mind. Soc Neurosci 2006; 1: i-ix.
78. Shamay-Tsoory SG, Tomer R, Yaniv S, Aharon-Peretz J. Empathy deficits in Asperger syndrome: a cognitive profile. Neurocase 2002; 8: 252.
79. Silani G, Bird G, Brindley R, Singer T, Frith C, Frith U. Levels of emotional awareness and autism: An fMRI study. Soc Neurosci 2008; 3: 97-112.
80. Singer T. The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neurosci Biobehav Rev 2006; 30: 855-863
81. Singer T, Lamm C. The social neuroscience of empathy. Year Cogn Neurosci 2009: Ann NY Acad Sci 2009; 1156: 81-96.
82. Singer T, Critchley HD, Preuschoff K. A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 2009; 13: 334-340
83. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science 2004; 303: 1157-1162
84. Singer T, Seymour B, O'Doherty JP, Stephan KE, Dolan RJ, Frith CD. Empathic neural responses are modulated by the perceived fairness of others. Nature 2006; 439: 466-469
85. Singer T, Snozzi R, Bird G, Petrovic P, Silani G, Heinrichs M, et al. Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Emotion 2008; 8: 781-791
86. Tani P, Lindberg N, Joukamaa M, Nieminen-von Wendt T, von Wendt L, Appelberg B, et al. Asperger syndrome, alexithymia and perception of sleep. Neuropsychobiology 2004; 49: 64-70. (Pubitemid 38253130)
87. Vorst HCM, Bermond B. Validity and reliability of the Bermond-Vorst Alexithymia Questionnaire. Pers Indiv Diff 2001; 30: 413-434
88. Wechsler D. Wechsler Adult Intelligence Scale-3rd UK Edition (WAIS®-III UK). London: The Psychological Corporation; 1999.
89. White S, O'Reilly H, Frith U. Big heads, small details and autism. Neuropsychologia 2009b; 47: 1274-1281
90. White S, Hill E, Happé F, Frith U. Revisiting the strange stories: revealing mentalizing impairments in autism. Child Development 2009a; 80: 1097-1117
91. Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G. Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 2003; 40: 655-664
92. Wispé L. The distinction between sympathy and empathy: to call forth a concept, a word is needed. J Pers Soc Psychol 1986; 50: 314-321
93. Worsley KJ, Friston KJ. Analysis of fMRI time-series revisited-again. Neuroimage 1995; 2: 173-181
94. Yirmiya N, Sigman MD, Kasari C, Mundy P. Empathy and cognition in high-functioning children with autism. Child Development 1992; 63: 150-160