Selective impairment of cognitive empathy for moral judgment in adults with high functioning autism

Social Cognitive and Affective Neuroscience

Volumn 8, Issue 7, 2013, Pages 780-788

  Gleichgerrcht, Ezequiel ^a,b,c   Torralva, Teresa ^a,b   Rattazzi, Alexia ^a,b   Marenco, Victoria ^a   Roca, María ^a,b   Manes, Facundo ^a,b  

^a INSTITUTE OF COGNITIVE NEUROLOGY INECO   (Argentina)

^b FAVALORO UNIVERSITY   (Argentina)

^c UNIVERSIDAD DIEGO PORTALES   (Chile)

Author keywords

Asperger syndrome; Emotion; Moral judgment; Social cognition; Utilitarianism

Indexed keywords

ADULT; ARTICLE; ASPERGER SYNDROME; AUTISM; BEHAVIOR; COGNITION; DECISION MAKING; EMOTION; EMPATHY; FEMALE; HUMAN; MALE; MIDDLE AGED; MORAL JUDGMENT; MORALITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SOCIAL BEHAVIOR; SOCIAL COGNITION; UTILITARIANISM; YOUNG ADULT;

ASPERGER SYNDROME; EMOTION; MORAL JUDGMENT; SOCIAL COGNITION; UTILITARIANISM;

ADULT; AUTISTIC DISORDER; COGNITION; EMOTIONS; EMPATHY; FEMALE; HUMANS; INTENTION; JUDGMENT; MALE; MIDDLE AGED; MORALS; SOCIAL BEHAVIOR; YOUNG ADULT;

EID: 84885716432     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nss067     Document Type: Article

References (89)

1. Anderson, S.W., Barrash, J., Bechara, A., Tranel, D. (2006). Impairments of emotion and real-world complex behavior following childhood- or adult-onset damage to ventromedial prefrontal cortex. Journal of the International Neuropsychological Society, 12(2), 224-35.
2. Anderson, S.W., Bechara, A., Damasio, H., Tranel, D., Damasio, A.R. (1999). Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat Neurosci., 2(11), 1032-37.
3. Association, A.P. (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. DSM-IV-TR, 4th edn. Washington, DC: American Psychiatric Association.
4. Atkinson, A.P. (2009). Impaired recognition of emotions from body movements is associated with elevated motion coherence thresholds in autism spectrum disorders. Neuropsychologia, 47(13), 3023-9.
5. Baron-Cohen, S. (2005). Mindblindness: An Essay on Autism and Theory of Mind. Cambridge, MA: MIT Press.
6. Baron-Cohen, S., Jolliffe, T., Mortimore, C., Robertson, M. (1997). Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. Journal of Child Psychology and Psychiatry, 38(7), 813-22.
7. Baron-Cohen, S., Leslie, A.M., Frith, U. (1985). Does the autistic child have a "theory of mind". Cognition, 21(1), 37-46.
8. Baron-Cohen, S., O'Riordan, M., Stone, V., Jones, R., Plaisted, K. (1999). Recognition of faux pas by normally developing children and children with Asperger syndrome or high-functioning autism. Journal of Autism and Developmental Disorders, 29(5), 407-18.
9. Baron-Cohen, S., Wheelwright, S. (2004). The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34(2), 163-75.
10. Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., Plumb, I. (2001a). The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 42(2), 241-51.
11. Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., Clubley, E. (2001b). The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31(1), 5-17.
12. Batson, D.C. (2009). These things called empathy: eight related but distinct phenomena. In: Decety, J., Ickes, W.J., editors. The Social Neuroscience of Empathy. Cambridge, MA: The MIT Press.
13. Bird, G., Press, C., Richardson, D.C. (2011). The role of alexithymia in reduced eye-fixation in autism spectrum conditions. Journal of Autism and Developmental Disorders, 41(11), 1556-64.
14. 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(Pt 5), 1515-25.
15. Blair, R.J. (1995). A cognitive developmental approach to mortality: investigating the psychopath. Cognition, 57(1), 1-29.
16. Blair, R.J. (1996). Brief report: morality in the autistic child. Journal of Autism and Developmental Disorders, 26(5), 571-9.
17. Blair, R.J. (1999). Psychophysiological responsiveness to the distress ofothers in children with autism. Personality and Individual Differences, 26(3), 477-85.
18. Blair, R.J. (2008). Fine cuts of empathy and the amygdala: dissociable deficits in psychopathy and autism. Q J Exp Psychol (Hove), 61(1), 157-70.
19. Blair, R.J., Blair, K.S. (2009). Empathy, Morality, and Social Convention: Evidence from the Study of Psychopathy and Other Psychiatric Disorders. Cambridge: MIT Press, pp. 139-52.
20. Carter, C., Meckes, L., Pritchard, L., Swensen, S., Wittman, P.P., Velde, B. (2004). The Friendship Club: an after-school program for children with Asperger syndrome. Family and Community Health, 27(2), 143-50.
21. Cushman, F., Young, L., Hauser, M. (2006). The role of conscious reasoning and intuition in moral judgment: testing three principles of harm. Psychological Science, 17(12), 1082-9.
22. Davis, M.H. (1983). Measuring individual differences in empathy: evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44(1), 113-26.
23. de Waal, F.B. (2008). Putting the altruism back into altruism: the evolution of empathy. Annual Review of Psychology, 59, 279-300.
24. Decety, J., Michalska, K.J. (2010). Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev Sci, 13(6), 886-99.
25. Decety, J., Svetlova, M. (2012). Putting together phylogenetic and ontogenetic perspectives on empathy. Developmental Cognitive Neuroscience, 2(1), 1-24.
26. Dziobek, I., Rogers, K., Fleck, S., et al. (2008). Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the Multifaceted Empathy Test (MET). Journal of Autism and Developmental Disorders, 38(3), 464-73.
27. Eslinger, P.J., Grattan, L.M., Damasio, H., Damasio, A.R. (1992). Developmental consequences of childhood frontal lobe damage. Archives of Neurology, 49(7), 764-9.
28. Fitzgerald, M., Bellgrove, M.A. (2006). The overlap between alexithymia and Asperger's syndrome. Journal of Autism and Developmental Disorders, 36(4), 573-6.
29. Frith, U. (2004). Emanuel Miller lecture: confusions and controversies about Asperger syndrome. Journal of Child Psychology and Psychiatry, 45(4), 672-86.
30. Frith, U., Morton, J., Leslie, A.M. (1991). The cognitive basis of a biological disorder: autism. Trends in Neuroscience, 14(10), 433-8.
31. Gleichgerrcht, E., Torralva, T., Roca, M., Pose, M., Manes, F. (2010). The role of social cognition in moral judgment in frontotemporal dementia. Social Neuroscience, 6(2), 113-22.
32. Golan, O., Baron-Cohen, S. (2006). Systemizing empathy: teaching adults with Asperger syndrome or high-functioning autism to recognize complex emotions using interactive multimedia. Development and Psychopathology, 18(2), 591-617.
33. Grant, C.M., Boucher, J., Riggs, K.J., Grayson, A. (2005). Moral understanding in children with autism. Autism, 9(3), 317-31.
34. Gray, K., Jenkins, A.C., Heberlein, A.S., Wegner, D.M. (2011). Distortions of mind perception in psychopathology. Proc Natl Acad Sci, 108(2), 477-79.
35. Gray, K., Keating, C., Taffe, J., Bereton, A., Einfeld, S., Tonge, B. (2012). Trajectory of behavior and emotional problems in autism. American Journal on Intellectual and Developmental Disabilities, 117(2), 121-33.
36. Greene, J. (2003). From neural 'is' to moral 'ought': what are the moral implications of neuroscientific moral psychology. Nature Review Neuroscience, 4(10), 846-9.
37. Greene, J., Morelli, S.A., Lowenberg, K., Nystrom, L.E., Cohen, J.D. (2008). Cognitive load selectively interferes with utilitarian moral judgment. Cognition, 107(3), 1144-54.
38. Greene, J., Nystrom, L.E., Engell, A.D., Darley, J.M., Cohen, J.D. (2004). The neural bases of cognitive conflict and control in moral judgment. Neuron, 44(2), 389-400.
39. Greene, J., Sommerville, R.B., Nystrom, L.E., Darley, J.M., Cohen, J.D. (2001). An fMRI investigation of emotional engagement in moral judgment. Science, 293(5537), 2105.
40. Greenwald, A.G., Nosek, B.A., Banaji, M.R. (2003). Understanding and using the Implicit Association Test: I. An improved scoring algorithm. Journal of Personality and Social Psychology, 85(2), 197-216.
41. Haidt, J. (2001). The emotional dog and its rational tail: a social intuitionist approach to moral judgment. Psychological Review, 108(4), 814-34.
42. Haidt, J. (2003). The moral emotions. In: Davidson, R.J., Scherer, K.R., Goldsmith, H.H., editors. Handbook of Affective Sciences. Oxford: Oxford University Press.
43. Hatfield, E., Rapson, R.L., Yen-Chi, L. (2009). Emotional contagion and empathy. In: Decety, J., Ickes, W.J., editors. The Social Neuroscience of Empathy. Cambridge, MA: The MIT Press.
44. Hauser, M., Cushman, F., Young, L., Jin, R., Mikhail, J. (2007). A dissociation between moral judgments and justiEcations. Mind and Language, 22(1), 1-21.
45. Heaton, P., Reichenbacher, L., Sauter, D., Allen, R., Scott, S., Hill, E. (2012). Measuring the effects of alexithymia on perception of emotional vocalizations in autistic spectrum disorder and typical development. Psychological Medicine, 4, 1-7.
46. Heekeren, H.R., Wartenburger, I., Schmidt, H., Schwintowski, H.P., Villringer, A. (2003). An fMRI study of simple ethical decision-making. NeuroReport, 14(9), 1215-9.
47. Hurlemann, R., Patin, A., Onur, O.A., Cohen, M.X., Baumgartner, T., Metzler, S., et al. (2010). Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J Neurosci., 30(14), 4999-5007.
48. Ickes, W.J. (2009). Empathic accuracy: its links to clinical, cognitive, developmental, social, and physiological psychology. In: Decety, J., Ickes, W.J., editors. The Social Neuroscience of Empathy. Cambridge, MA: The MIT Press.
49. Kessler, J., Kalbe, E., Schlegel, M., et al. (2009). Dissociating cognitive from affective theory of mind: a TMS study. Cortex, 46(6), 769-80.
50. Koenigs, M., Young, L., Adolphs, R., et al. (2007). Damage to the prefrontal cortex increases utilitarian moral judgements. Nature, 446(7138), 908-11.
51. Kohlberg, L. (1981). The Philosophy of Moral Development 1. New York: Harper & Row.
52. Kuchinke, L., Schneider, D., Kotz, S.A., Jacobs, A.M. (2011). Spontaneous but not explicit processing of positive sentences impaired in Asperger's syndrome: pupillometric evidence. Neuropsychologia, 49(3), 331-338.
53. Leslie, A.M., Mallon, R., DiCorcia, J.A. (2006). Transgressors, victims, and cry babies: is basic moral judgment spared in autism. Social Neuroscience, 1(3-4), 270-83.
54. Luo, Q., Nakic, M., Wheatley, T., Richell, R., Martin, A., Blair, R.J. (2006). The neural basis of implicit moral attitude-an IAT study using event-related fMRI. NeuroImage, 30(4), 1449-57.
55. Mendez, M.F. (2006). What frontotemporal dementia reveals about the neurobiological basis of morality. Medical Hypotheses, 67(2), 411-8.
56. Mendez, M.F., Anderson, E., Shapira, J.S. (2005). An investigation of moral judgement in frontotemporal dementia. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology, 18(4), 193-7.
57. Miller, M.B., Sinnott-Armstrong, W., Young, L., et al. (2010). Abnormal moral reasoning in complete and partial callosotomy patients. Neuropsychologia, 48(7), 2215-20.
58. Moll, J., de Oliveira-Souza, R., Bramati, I.E., Grafman, J. (2002). Functional networks in emotional moral and nonmoral social judgments. NeuroImage, 16(3 Pt 1), 696-703.
59. Moll, J., de Oliveira-Souza, R., Garrido, G.J., et al. (2007). The self as a moral agent: linking the neural bases of social agency and moral sensitivity. Social Neuroscience, 2(3-4), 336-52.
60. Moran, J.M., Young, L., Saxe, R., et al. (2011). Impaired theory of mind for moral judgment in high-functioning autism. Proceedings of the National Academy of Sciences, 108, 2688-92.
61. Panksepp, J. (1998). Affective Neuroscience. New York: Oxford University Press.
62. Piaget, J. (1965). The Moral Judgment of the Child. New York: Free Press.
63. Preston, S.D., de Waal, F.B. (2002). Empathy: its ultimate and proximate bases. The Behavioral and Brain Sciences, 25(1), 1-20; discussion 20-71.
64. Rogers, K., Dziobek, I., Hassenstab, J., Wolf, O.T., Convit, A. (2007). Who cares? Revisiting empathy in Asperger syndrome. Journal of Autism and Developmental Disorders, 37(4), 709-15.
65. Scott, F.J., Baron-Cohen, S., Bolton, P., Brayne, C. (2002). The CAST (Childhood Asperger Syndrome Test): preliminary development of a UK screen for mainstream primary-school-age children. Autism, 6(1), 9-31.
66. Shamay-Tsoory, S.G. (2009). Empathic processing: its cognitive and affective dimensions and neuroanatomical basisCambridge: The Social Neuroscience of Empathy, pp. 215-32.
67. Shamay-Tsoory, S.G. (2011). The neural bases for empathy. Neuroscientist, 17(1), 18-24.
68. Shamay-Tsoory, S.G., Aharon-Peretz, J. (2007). Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia, 45(13), 3054-67.
69. Shamay-Tsoory, S.G., Shur, S., Barcai-Goodman, L., Medlovich, S., Harari, H., Levkovitz, Y. (2007). Dissociation of cognitive from affective components of theory of mind in schizophrenia. Psychiatry Research, 149(1-3), 11-23.
70. Shamay-Tsoory, S.G., Tomer, R., Berger, B.D., Goldsher, D., Aharon-Peretz, J. (2005). Impaired "affective theory of mind" is associated with right ventromedial prefrontal damage. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology, 18(1), 55-67.
71. Shamay-Tsoory, S.G., Tomer, R., Yaniv, S., Aharon-Peretz, J. (2002). Empathy deficits in Asperger syndrome: a cognitive profile. Neurocase, 8(3), 245-52.
72. Singer, T. (2006). The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neuroscience and Biobehavioral Reviews, 30(6), 855-63.
73. Stone, V.E., Baron-Cohen, S., Knight, R.T. (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience, 10(5), 640-56.
74. Tani, P., Lindberg, N., Joukamaa, M., et al. (2004). Asperger syndrome, alexithymia and perception of sleep. Neuropsychobiology, 49(2), 64-70.
75. Thomson, J.J., Parent, W. (1986). Rights, restitution, and risk: essays, in moral theory. Cambridge: Harvard University Press.
76. Uono, S., Sato, W., Toichi, M. (2011). The specific impairment of fearful expression recognition and its atypical development in pervasive developmental disorder. Social Neuroscience, 6(5-6), 452-63.
77. Valdesolo, P., DeSteno, D. (2006). Manipulations of emotional context shape moral judgment. Psychological Science, 17(6), 476-7.
78. Wechsler, D. (1997). Wechsler Adult Intelligence Scale 3rd edn. San Antonio: Pearson.
79. Wheatley, T., Haidt, J. (2005). Hypnotic disgust makes moral judgments more severe. Psychological Science, 16(10), 780-4.
80. Wheelwright, S., Baron-Cohen, S., Goldenfeld, N., et al. (2006). Predicting Autism Spectrum Quotient (AQ) from the Systemizing Quotient-Revised (SQ-R) and Empathy Quotient (EQ). Brain Research, 1079(1), 47-56.
81. Yang, H.H., Savosyanov, A.N., Tsai, A.C., Liou, M. (2011). Face recognition in Asperger syndrome: a study on EEG spectral power changes. Neuroscience Letters, 492(2), 84-8.
82. Yirmiya, N., Sigman, M.D., Kasari, C., Mundy, P. (1992). Empathy and cognition in high-functioning children with autism. Child Development, 63(1), 150-60.
83. Young, L., Bechara, A., Tranel, D., Damasio, H., Hauser, M., Damasio, A. (2010a). Damage to ventromedial prefrontal cortex impairs judgment of harmful intent. Neuron, 65(6), 845-51.
84. Young, L., Camprodon, J.A., Hauser, M., Pascual-Leone, A., Saxe, R. (2010b). Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proceedings of the National Academy of Sciences, 107(15), 6753-8.
85. Young, L., Cushman, F., Hauser, M., Saxe, R. (2007). The neural basis of the interaction between theory of mind and moral judgment. Proceedings of the National Academy of Sciences, 104(20), 8235-40.
86. Young, L., Dodell-Feder, D., Saxe, R. (2010). What gets the attention of the temporoparietal junction? An fMRI investigation of attention and theory of mind. Neuropsychologia, 48(9), 2658-64.
87. Young, L., Koenigs, M. (2007). Investigating emotion in moral cognition: a review of evidence from functional neuroimaging and neuropsychology. British Medical Bulletin, 84, 69-79.
88. Young, L., Saxe, R. (2008). The neural basis of belief encoding and integration in moral judgment. NeuroImage, 40(4), 1912-20.
89. Zalla, T., Barlassina, L., Buon, M., Leboyer, M. (2011). Moral judgment in adults with autism spectrum disorders. Cognition, 121(1), 115-26.