Age-dependent changes in the neural substrates of empathy in autism spectrum disorder

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 8, 2014, Pages 1118-1126

  Schulte Rüther, Martin ^a,b,c   Greimel, Ellen ^a,b,c   Piefke, Martina ^b,d   Kamp Becker, Inge ^e   Remschmidt, Helmut ^e   Fink, Gereon R ^b,f   Herpertz Dahlmann, Beate ^a,c   Konrad, Kerstin ^a,b,c  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d UNIVERSITY OF WITTEN HERDECKE   (Germany)

^e PHILIPPS UNIVERSITY MARBURG   (Germany)

^f UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Developmental trajectories; Facial emotion; Medial prefrontal cortex; Social cognition; Theory of mind

Indexed keywords

ADOLESCENT; ADULT; AUTISM; BRAIN; CHILD; CHILD DEVELOPMENT; DECISION MAKING; EMPATHY; FACIAL EXPRESSION; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALE; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN; CHILD; CHILD DEVELOPMENT; CHILD DEVELOPMENT DISORDERS, PERVASIVE; EMPATHY; FACIAL EXPRESSION; HUMANS; JUDGMENT; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; YOUNG ADULT;

EID: 84905921813     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst088     Document Type: Article

References (77)

1. Baron-Cohen, S., Frith, U., Leslie, A.M. (1985). Does the autistic child have a "theory of mind"? Cognition, 21, 37-46.
2. 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 highfunctioning autism. Journal of Autism and Developmental Disorders, 29, 407-18.
3. Baron-Cohen, S., Tager-Flusberg, H., Cohen, D. (2000). Understanding Other Minds: Perspectives from Autism and Developmental Cognitive Neuroscience. Oxford: Oxford University Press.
4. 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, 163-75.
5. Bastiaansen, J.A., Thioux, M., Keysers, C. (2009). Evidence for mirror systems in emotions. Philosophical Transactions of the Royal Society of London Series B Biological Sciences, 364, 2391-404.
6. Bird, G., Silani, G., Brindley, R., White, S.J., Frith, U., Singer, T. (2010). Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain, 133, 1515-25.
7. Blakemore, S.-J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9, 267-77.
8. Blakemore, S.-J., Den Ouden, H., Choudhury, S., Frith, C.D. (2007). Adolescent development of the neural circuitry for thinking about intentions. Social Cognitive and Affective Neuroscience, 2, 130-9.
9. Blasi, G., Goldberg, T.E., Weickert, T., et al. (2006). Brain regions underlying response inhibition and interference monitoring and suppression. The European Journal of Neuroscience, 23, 1658-64.
10. Bock, M.A. (2001). SODA strategy: enhancing the social interaction skills of youngsters with Asperger syndrome. Intervention in School and Clinic, 36, 272-8.
11. Bowler, D.M. (1992). "Theory of mind" in Asperger's syndrome. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 33, 877-93.
12. Brieber, S., Herpertz-Dahlmann, B., Fink, G.R., Kamp-Becker, I., Remschmidt, H., Konrad, K. (2010). Coherent motion processing in autism spectrum disorder (ASD): an fMRI study. Neuropsychologia, 48, 1644-51.
13. Bryant, B.K. (1982). An index of empathy for children and adolescents. Child Development, 53, 413.
14. Bunge, S.A., Dudukovic, N.M., Thomason, M.E., Vaidya, C.J., Gabrieli, J.D.E. (2002). Immature frontal lobe contributions to cognitive control in children evidence from fMRI. Neuron, 33, 301-11.
15. 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 Sciences of the United States of America, 100, 5497-502.
16. Casey, B.J., Tottenham, N., Liston, C., Durston, S. (2005). Imaging the developing brain: what have we learned about cognitive development? Trends in Cognitive Sciences, 9, 104-10.
17. Castelli, F., Frith, C.D., Happé, F., Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125, 1839-49.
18. Castelli, F., Happé, F., Frith, U., Frith, C.D. (2000). Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. NeuroImage, 12, 314-25.
19. Ciaramelli, E., Bernardi, F., Moscovitch, M. (2013). Individualized theory of mind (iToM): when memory modulates empathy. Frontiers in Psychology, 4, 4.
20. Craig, A.D.B. (2009). How do you feel-now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 59-70.
21. Dadds, M.R., Hunter, K., Hawes, D.J., et al. (2008). A measure of cognitive and affective empathy in children using parent ratings. Child Psychiatry and Human Development, 39, 111-22.
22. Davis, M.H. (1980). A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology, 10, 85.
23. Decety, J., Jackson, P.L. (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews, 3, 71-100.
24. Decety, J., Michalska, K.J. (2010). Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Developmental Science, 13, 886-99.
25. Decety, J., Michalska, K.J., Akitsuki, Y. (2008). Who caused the pain? An fMRI investigation of empathy and intentionality in children. Neuropsychologia, 46, 2607-2614.
26. Decety, J., Sommerville, J.A. (2003). Shared representations between self and other: a social cognitive neuroscience view. Trends in Cognitive Sciences, 7, 527-33.
27. Diamond, A. (2002). Normal development of prefrontal cortex from birth to young adulthood: cognitive functions, anatomy, and biochemistry. In: Stuss, D.T., Knight, R.T., editors. Principles of Frontal Lobe Function. Oxford: Oxford University Press, pp. 466-503.
28. Dondi, M., Simion, F., Caltran, G. (1999). Can newborns discriminate between their own cry and the cry of another newborn infant? Developmental Psychology, 35, 418-26.
29. Döpfner, M., Schmeck, K., Berner, W. (1994). Handbuch: Elternfragebogen über das Verhalten von Kindern und Jugendlichen: Forschungsergebnisse zur deutschen Fassung der Child Behavior Checklist (CBCL)Köln: Arbeitsgruppe Kinder-, Jugendund Familiendiagnostik.
30. Durston, S., Davidson, M.C., Tottenham, N., et al. (2006). A shift from diffuse to focal cortical activity with development. Developmental Science, 9, 1-8.
31. 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, 464-73.
32. Farley, M.A., McMahon, W.M., Fombonne, E., et al. (2009). Twenty-year outcome for individuals with autism and average or near-average cognitive abilities. Autism Research, 2, 109-18.
33. Franke, G.H. (2000). Brief symptom inventory von L.R. Derogatis (Kurzform der SCL-90-R). Deutsche VersionGöttingen, Germany: Beltz.
34. Frith, C.D., Amodio, D.M. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7, 268-77.
35. Frith, C.D., Frith, U. (2008). Implicit and explicit processes in social cognition. Neuron, 60, 503-10.
36. Frith, U., Frith, C.D. (2003). Development and neurophysiology of mentalizing. Philosophical Transactions of the Royal Society of London Series B Biological Sciences, 358, 459-73.
37. Gallagher, H.L., Frith, C.D. (2003). Functional imaging of "theory of mind". Trends in Cognitive Sciences, 7, 77-83.
38. Greimel, E., Schulte-Rüther, M., Fink, G.R., Piefke, M., Herpertz-Dahlmann, B., Konrad, K. (2010a). Development of neural correlates of empathy from childhood to early adulthood: an fMRI study in boys and adult men. Journal of Neural Transmission, 117, 781-91.
39. Greimel, E., Schulte-Rüther, M., Kircher, T., et al. (2010b). Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. NeuroImage, 49, 1055-65.
40. Moor, B.G., Macks, Z.A., Güroglu, B., Rombouts, S.A., Molen, M.W., Crone, E.A. (2011). Neurodevelopmental changes of reading the mind in the eyes. Social Cognitive and Affective Neuroscience, 7, 44-52.
41. Happé, F. (1994). An advanced test of theory of mind: understanding of story characters' thoughts and feelings by able autistic, mentally handicapped, and normal children and adults. Journal of Autism and Developmental Disorders, 24, 129-54.
42. Happé, F., Ehlers, S., Fletcher, P., et al. (1996). "Theory of mind" in the brain. Evidence from a PET scan study of Asperger syndrome. Neuroreport, 8, 197-201.
43. Hutman, T., Rozga, A., DeLaurentis, A.D., Barnwell, J.M., Sugar, C.A., Sigman, M. (2010). Response to distress in infants at risk for autism: a prospective longitudinal study. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 51, 1010-20.
44. Iacoboni, M., Dapretto, M. (2006). The mirror neuron system and the consequences of its dysfunction. Nature Reviews Neuroscience, 7, 942-51.
45. Kobayashi, C., Glover, G.H., Temple, E. (2008). Switching language switches mind: linguistic effects on developmental neural bases of 'Theory of Mind'. Social Cognitive and Affective Neuroscience, 3, 62.
46. Lawrence, E.J., Shaw, P., Baker, D., Baron-Cohen, S., David, A.S. (2004). Measuring empathy: reliability and validity of the empathy quotient. Psychological Medicine, 34, 911-9.
47. Light, S.N., Coan, J.A., Zahn-Waxler, C., Frye, C., Goldsmith, H.H., Davidson, R.J. (2009). Empathy is associated with dynamic change in prefrontal brain electrical activity during positive emotion in children. Child Development, 80, 1210-31.
48. Lombardo, M.V., Barnes, J.L., Wheelwright, S., Baron-Cohen, S. (2007). Self-referential cognition and empathy in autism. PloS One, 2, e883.
49. Lombardo, M.V., Chakrabarti, B., Bullmore, E.T., et al. (2010). Atypical neural self-representation in autism. Brain, 133, 611-24.
50. Lou, H.C., Luber, B., Crupain, M., et al. (2004). Parietal cortex and representation of the mental self. Proceedings of National Academy of Science U S A, 101, 6827-32.
51. Luna, B., Sweeney, J.A. (2001). Studies of brain and cognitive maturation through childhood and adolescence: a strategy for testing neurodevelopmental hypotheses. Schizophrenia Bulletin, 27, 443-55.
52. Manjaly, Z.M., Bruning, N., Neufang, S., et al. (2007). Neurophysiological correlates of relatively enhanced local visual search in autistic adolescents. Neuroimage, 35, 283-91.
53. Pfeifer, J.H., Dapretto, M., Iacoboni, M., Mazziotta John, C. (2008). Mirroring others' emotions relates to empathy and interpersonal competence in children. NeuroImage, 39, 2076-85.
54. Pfeifer, J.H., Lieberman, M.D., Dapretto, M. (2007). "I know you are but what am I?!": Neural bases of self- and social knowledge retrieval in children and adults. Journal of Cognitive Neuroscience, 19, 1323-37.
55. Premack, D., Woodruff, G. (1978). Does the chimpanzee have a theory of mind. Behavioral and Brain Sciences, 1, 515-26.
56. Ridderinkhof, K.R., Ullsperger, M., Crone, E.A., Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306, 443-7.
57. Scambler, D.J., Hepburn, S., Rutherford, M.D., Wehner, E.A., Rogers, S.J. (2007). Emotional responsivity in children with autism, children with other developmental disabilities, and children with typical development. Journal of Autism and Developmental Disorders, 37, 553-63.
58. Schulte-Rüther, M., Fink, G.R., Markowitsch, H.J., Piefke, M. (2007). Mirror neuron and theory of mind mechanisms involved in face-to-face interactions: a functional magnetic resonance imaging approach to empathy. Journal of Cognitive Neuroscience, 19, 1354-72.
59. Schulte-Rüther, M., Fink, G.R., Markowitsch, H.J., Shah, N.J., Piefke, M. (2008). Gender differences in brain networks supporting empathy. NeuroImage, 42, 393-403.
60. Schulte-Rüther, M., Greimel, E. (2011). Brain networks supporting empathy. In: Ebstein, R.P., Shamay-Tsoory, S.G., Chew, S.H., editors. From DNA to Social Cognition. Hoboken, NJ: John Wiley&Sons, pp. 47-61.
61. Schulte-Rüther, M., Greimel, E., Markowitsch, H.J., et al. (2011). Dysfunctions in brain networks supporting empathy: an fMRI study in adults with autism spectrum disorders. Social Neuroscience, 6, 1-21.
62. Schwenck, C., Mergenthaler, J., Keller, K., et al. (2011). Empathy in children with autism and conduct disorder: group-specific profiles and developmental aspects. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 53, 651-9.
63. Shattuck, P.T., Seltzer, M.M., Greenberg, J.S., et al. (2007). Change in autism symptoms and maladaptive behaviors in adolescents and adults with an autism spectrum disorder. Journal of Autism and Developmental Disorders, 37, 1735-47.
64. Silani, G., Bird, G., Brindley, R., Singer, T., Frith, C.D., Frith, U. (2008). Levels of emotional awareness and autism: an fMRI study. Social Neuroscience, 3, 97-112.
65. Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R.J., Frith, C.D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303, 1157-62.
66. Strayer, J. (1993). Children's concordant emotions and cognitions in response to observed emotions. Child Development, 64, 188-201.
67. Tamm, L., Menon, V., Reiss, A.L. (2002). Maturation of brain function associated with response inhibition. Journal of American Academy of Child and Adolescent Psychiatry, 41, 1231.
68. Thompson, R. (1987). Empathy and emotional understanding: the early development of empathy. In: Eisenberger, N., Strayer, J., editors. Empathy and its Development. Cambridge: Cambridge University Press, pp. 119-45.
69. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15, 273-89.
70. Uddin, L.Q., Molnar-Szakacs, I., Kaplan, J.T., Zaidel, E., Iacoboni, M. (2005). Self-face recognition activates a frontoparietal "mirror" network in the right hemisphere: an event-related fMRI study. NeuroImage, 25, 926-35.
71. Vogeley, K., Bussfeld, P., Newen, A., et al. (2001). Mind reading: neural mechanisms of theory of mind and self-perspective. Neuroimage, 14, 170-81.
72. Vogeley, K., Fink, G.R. (2003). Neural correlates of the first-person-perspective. Trends in Cognitive Sciences, 7, 38-42.
73. Wang, A.T., Lee, S.S., Sigman, M., Dapretto, M. (2006). Developmental changes in the neural basis of interpreting communicative intent. Social Cognitive and Affective Neuroscience, 1, 107-21.
74. Wellman, H.M., Liu, D. (2004). Scaling of theory-of-mind tasks. Child Development, 75, 523-41.
75. White, S.J., Coniston, D., Rogers, R., Frith, U. (2011). Developing the Frith-Happé animations: a quick and objective test of theory of mind for adults with autism. Autism Research, 4, 149-54.
76. Wicker, B., Keysers, C., Plailly, J., Royet, J.P., 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.
77. Zahn-Waxler, C., Radke-Yarrow, M. (1990). The origins of empathic concern. Motivation and Emotion, 14, 107-30.