Response to Smith’s Letter to the Editor ‘Emotional Empathy in Autism Spectrum Conditions: Weak, Intact, or Heightened?’

  • Ilaria Minio-Paluello
  • Michael V. Lombardo
  • Bhismadev Chakrabarti
  • Sally Wheelwright
  • Simon Baron-Cohen
Letter to the Editor

References

  1. Ashwin, C., Chapman, E., Colle, L., & Baron-Cohen, S. (2006). Impaired recognition of negative basic emotions in autism: A test of the amygdala theory. Social Neuroscience, 1(3–4), 349–363.CrossRefPubMedGoogle Scholar
  2. Bacon, A. L., Fein, D., Morris, R., Waterhouse, L., & Allen, D. (1998). The responses of autistic children to the distress of others. Journal of Autism and Developmental Disorders, 28, 129–142.CrossRefPubMedGoogle Scholar
  3. Baron-Cohen, S., & Wheelwright, S. (2004). The empathy quotient (EQ). An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34, 163–175.CrossRefPubMedGoogle Scholar
  4. Batson, C. D. (1991). The altruism question: Towards a social-psychological answer. Mahwah, NJ: Erlbaum.Google Scholar
  5. Beall, P. M., Moody, E. J., McIntosh, D. N., Hepburn, S. L., & Reed, C. L. (2008). Rapid facial reactions to emotional facial expressions in typically developing children and children with autism spectrum disorder. Journal of Experimental Child Psychology, 101(3), 206–223. [Epub 2008 Jun 17].CrossRefPubMedGoogle Scholar
  6. Becchio, C., Pierno, A., Mari, M., Lusher, D., & Castiello, U. (2007). Motor contagion from gaze: The case of autism. Brain, 130(Pt 9), 2401–2411.CrossRefPubMedGoogle Scholar
  7. Behrmann, M., Thomas, C., & Humphreys, K. (2006). Seeing it differently: Visual processing in autism. Trends in cognitive sciences, 10(6), 258–264. [Epub 2006 May 19. Review].CrossRefPubMedGoogle Scholar
  8. Ben Shalom, D., Mostofsky, S. H., Hazlett, R. L., Goldberg, M. C., Landa, R. J., Faran, Y., et al. (2006). Normal physiological emotions but differences in expression of conscious feelings in children with high-functioning autism. Journal of Autism and Developmental Disorders, 36, 395–400.CrossRefPubMedGoogle Scholar
  9. Bernier, R., Dawson, G., Panagiotides, H., & Webb, S. (2005). Individuals with autism spectrum disorder show normal responses to a fear potential startle paradigm. Journal of Autism and Developmental Disorders, 35, 575–583.CrossRefPubMedGoogle Scholar
  10. Berthoz, S., & Hill, E. L. (2005). The validity of using self-reports to assess emotion regulation abilities in adults with autism spectrum disorder. European Psychiatry, 20, 291–298.CrossRefPubMedGoogle Scholar
  11. Bird, G., Leighton, J., Press, C., & Heyes, C. (2007). Intact automatic imitation of human and robot actions in autism spectrum disorders. Proceedings of the Royal Society B, 274, 3027–3031.CrossRefPubMedGoogle Scholar
  12. Blair, R. J. (1999). Psychophysiological responsiveness to the distress of others in children with autism. Personality and Individual Differences, 26, 477–485.CrossRefGoogle Scholar
  13. Blakemore, S. J., 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(Pt 7), 1571–1583.CrossRefPubMedGoogle Scholar
  14. Bölte, S., Feineis-Matthews, S., & Poustka, F. (2008). Brief report: Emotional processing in high-functioning autism–physiological reactivity and affective report. Journal of Autism and Developmental Disorders, 38(4), 776–781. [Epub 2007 Sep 20].CrossRefPubMedGoogle Scholar
  15. Brian, J., Bryson, S. E., Garon, N., Roberts, W., Smith, I. M., Szatmari, P., et al. (2008). Clinical assessment of autism in high-risk 18-month-olds. Autism, 12(5), 433–456.CrossRefPubMedGoogle Scholar
  16. Bryson, S. E., Zwaigenbaum, L., Brian, J., Roberts, W., Szatmari, P., Rombough, V., et al. (2007). A prospective case series of high-risk infants who developed autism. Journal of Autism and Developmental Disorders, 37(1), 12–24. [Epub 2007 Jan 9].CrossRefPubMedGoogle Scholar
  17. Bufalari, I., Aprile, T., Avenanti, A., Di Russo, F., & Aglioti, S. M. (2007). Empathy for pain and touch in the human somatosensory cortex. Cerebral Cortex, 17(11), 2553–2561.CrossRefPubMedGoogle Scholar
  18. Capps, L., Kasari, C., Yirmiya, N., & Sigman, M. (1993). Parental perception of emotional expressiveness in children with autism. Journal of Consulting and Clinical Psychology, 61, 475–484.CrossRefPubMedGoogle Scholar
  19. Cattaneo, L., Fabbri-Destro, M., Boria, S., Pieraccini, C., Monti, A., Cossu, G., et al. (2007). Impairment of actions chains in autism and its possible role in intention understanding. Proceedings of the National Academy of Sciences of the United States of America, 104(45), 17825–17830. [Epub 2007 Oct 26].CrossRefPubMedGoogle Scholar
  20. Charman, T., Swettenham, J., Baron-Cohen, S., Cox, A., Baird, G., & Drew, A. (1997). Infants with autism: An investigation of empathy, pretend play, joint attention, and imitation. Developmental psychology, 33(5), 781–789.CrossRefPubMedGoogle Scholar
  21. Corona, R., Dissanayake, C., Arbelle, S., Wellington, P., & Sigman, M. (1998). Is affect aversive to young children with autism? Behavioral and cardiac responses to experimenter distress. Child Development, 69(6), 1494–1502.PubMedGoogle Scholar
  22. Davis, M. H. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44, 113–126.CrossRefGoogle Scholar
  23. Davis, M. H. (1996). Empathy: A social psychological approach. Boulder, CO: Westview.Google Scholar
  24. Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998). Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders, 28(6), 479–485.CrossRefPubMedGoogle Scholar
  25. Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., et al. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental psychology, 40(2), 271–283.CrossRefPubMedGoogle Scholar
  26. Dziobek, I., Rogers, K., Fleck, S., Bahnemann, M., Heekeren, H. R., Wolf, O. T., 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, 464–473.CrossRefPubMedGoogle Scholar
  27. Eisenberg, N. (2007). Empathy-related responding and prosocial behaviour. Novartis Foundation Symposium, 278, 71–80.CrossRefPubMedGoogle Scholar
  28. Frith, U. (2004). Emanuel Miller lecture: Confusions and controversies about Asperger syndrome. Journal of Child Psychology and Psychiatry, 45(4), 672–686. [Review].CrossRefPubMedGoogle Scholar
  29. Frith, U., & de Vignemont, F. (2005). Egocentrism, allocentrism, and Asperger syndrome. Consciousness and Cognition, 14, 719–738.CrossRefPubMedGoogle Scholar
  30. Gallese, V. (2007). Before and below ‘theory of mind’: Embodied simulation and the neural correlates of social cognition. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 362(1480), 659–669. [Review].CrossRefPubMedGoogle Scholar
  31. Garon, N., Bryson, S. E., Zwaigenbaum, L., Smith, I. M., Brian, J., Roberts, W., et al. (2009). Temperament and its relationship to autistic symptoms in a high-risk infant sib cohort. Journal of Abnormal Child Psychology, 37(1), 59–78.CrossRefPubMedGoogle Scholar
  32. Gazzola, V., & Keysers, C. (2009). The observation and execution of actions share motor and somatosensory voxels in all tested subjects: Single-subject analyses of unsmoothed fMRI data. Cerebral Cortex, 19(6), 1239–1255.CrossRefPubMedGoogle Scholar
  33. Hadjikhani, N., Joseph, R. M., Manoach, D. S., Naik, P., Snyder, J., Dominick, K., et al. (2009). Body expressions of emotion do not trigger fear contagion in autism spectrum disorder. Social cognitive and affective neuroscience, 4(1), 70–78. [Epub 2009 Jan 17].CrossRefPubMedGoogle Scholar
  34. Hermans, E. J., Putman, P., & van Honk, J. (2006). Testosterone administration reduces empathetic behavior: A facial mimicry study. Psychoneuroendocrinology, 31(7), 859–866.CrossRefPubMedGoogle Scholar
  35. Hermans, E. J., van Wingen, G., Bos, P. A., Putman, P., & van Honk, J. (2009). Reduced spontaneous facial mimicry in women with autistic traits. Biological Psychology, 80(3), 348–353. [Epub 2008 Dec 24].CrossRefPubMedGoogle Scholar
  36. Hill, E., Berthoz, S., & Frith, U. (2004). Brief report: Cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. Journal of Autism and Developmental Disorders, 34, 229–235.CrossRefPubMedGoogle Scholar
  37. Hirstein, W., Iversen, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings. Biological sciences, 268(1479), 1883–1888.CrossRefGoogle Scholar
  38. Humphreys, K., Minshew, N., Leonard, G. L., & Behrmann, M. (2007). A finegrained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45, 685–695.CrossRefPubMedGoogle Scholar
  39. Jackson, P. L., Brunet, E., Meltzoff, A. N., & Decety, J. (2006). Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia, 44(5), 752–761.CrossRefPubMedGoogle Scholar
  40. Keysers, C., Wicker, B., Gazzola, V., Anton, J. L., Fogassi, L., & Gallese, V. (2004). A touching sight: SII/PV activation during the observation and experience of touch. Neuron, 42, 335–346.CrossRefPubMedGoogle Scholar
  41. Kuusikko, S., Haapsamo, H., Jansson-Verkasalo, E., Hurtig, T., Mattila, M. L., Ebeling, H., et al. (2009). Emotion recognition in children and adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(6), 938–945.CrossRefPubMedGoogle Scholar
  42. Kylliäinen, A., & Hietanen, J. K. (2006). Skin conductance responses to another person’s gaze in children with autism. Journal of Autism and Developmental Disorders, 36(4), 517–525.CrossRefPubMedGoogle Scholar
  43. Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry, 45(6), 1115–1122.CrossRefPubMedGoogle Scholar
  44. Lane, R. D., Ahern, G. L., Schwartz, G. E., & Kaszniak, A. W. (1997). Is alexithymia the emotional equivalent of blindsight? Biological Psychiatry, 42(9), 834–844. [Review].CrossRefPubMedGoogle Scholar
  45. Lombardo, M. V., Barnes, J. L., Wheelwright, S. J., & Baron-Cohen, S. (2007). Self-referential cognition and empathy in autism. PLoS One, 2, e883.CrossRefPubMedGoogle Scholar
  46. Lombardo, M. V., Chakrabarti, B., Bullmore, E. T., Wheelwright, S. J., Sadek, S. A., Suckling, J., Baron-Cohen, S., & MRC AIMS Consortium. (2009). Shared neural circuits for mentalizing about the self and others. Journal of Cognitive Neuroscience, in press.Google Scholar
  47. Magnee, M. J. C. M., de Gelder, B., van Engeland, H., & Kemner, C. (2007). Facial electromyographic responses to emotional information from faces and voices in individuals with pervasive developmental disorder. Journal of Child Psychology and Psychiatry, 48, 1122–1130.CrossRefPubMedGoogle Scholar
  48. McIntosh, D. N., Reichmann-Decker, A., Winkielman, P., & Wilbarger, J. L. (2006). When the social mirror breaks: Deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. Developmental Science, 9(3), 295–302.CrossRefPubMedGoogle Scholar
  49. Minio-Paluello, I., Baron-Cohen, S., Avenanti, A., Walsh, V., & Aglioti, S. M. (2009). Absence of embodied empathy during pain observation in Asperger syndrome. Biological Psychiatry, 65(1), 55–62. [Epub 2008 Sep 23].CrossRefPubMedGoogle Scholar
  50. Mitchell, J. P., Macrae, C. N., & Banaji, M. R. (2006). Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron, 50, 655–663.CrossRefPubMedGoogle Scholar
  51. Niedenthal, P. M. (2007). Embodying emotion. Science, 316, 1002–1005.CrossRefPubMedGoogle Scholar
  52. Nummenmaa, L., Hirvonen, J., Parkkola, R., & Hietanen, J. K. (2008). Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy. NeuroImage, 43, 571–580.CrossRefPubMedGoogle Scholar
  53. Oberman, L. M., Winkielman, P., Ramachandran, V. S. (2009). Slow echo: Facial EMG evidence for the delay of spontaneaous, but not voluntary emotional mimicry in children with autism spectrum disorders. Developmental Science, 12(4), 510–520.CrossRefPubMedGoogle Scholar
  54. Ochsner, K. N., Knierim, K., Ludlow, D. H., Hanelin, J., Ramachandran, T., Glover, G., 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), 1746–1772.CrossRefPubMedGoogle Scholar
  55. Ochsner, K. N., Beer, J. S., Robertson, E. R., Cooper, J. C., Gabrieli, J. D., Kihsltrom, J. F., et al. (2005). The neural correlates of direct and reflected self-knowledge. Neuroimage, 28(4), 797–814.CrossRefPubMedGoogle Scholar
  56. Pierno, A. C., Mari, M., Lusher, D., & Castiello, U. (2008). Robotic movement elicits visuomotor priming in children with autism. Neuropsychologia, 46(2), 448–454. [Epub 2007 Sep 1].CrossRefPubMedGoogle Scholar
  57. Posner, M. I., & Rothbart, M. K. (1998). Attention, self-regulation and consciousness. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 353(1377), 1915–1927. [Review].CrossRefPubMedGoogle Scholar
  58. 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].PubMedGoogle Scholar
  59. Proverbio, A. M., Riva, F., & Zani, A. (2009). Observation of static pictures of dynamicactions enhances the activity of movement-related brain areas. PLoS One, 4(5), e5389.CrossRefPubMedGoogle Scholar
  60. Rheingold, H., Hay, D., & West, M. (1976). Sharing in the second year of life. Child Development, 47, 1148–1158.CrossRefGoogle Scholar
  61. 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), 709–715.CrossRefPubMedGoogle Scholar
  62. Rothbart, M. K., & Ahadi, S. A. (1994). Temperament and the development of personality. Journal of Abnormal Psychology, 103(1), 55–66. [Review].CrossRefPubMedGoogle Scholar
  63. Sagi, A., & Hoffman, M. L. (1976). Empathic distress in the newborn. Developmental Psychology, 12, 175–176.CrossRefGoogle Scholar
  64. Saxe, R., Moran, J. M., Scholz, J., & Gabrieli, J. D. (2006). Overlapping and nonoverlapping brain regions for theory of mind and self reflection in individual subjects. Soc Cogn Aff Neurosci, 1, 229–234.CrossRefGoogle Scholar
  65. 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(3), 553–563.CrossRefPubMedGoogle Scholar
  66. Senju et al (2008 Aug). J Autism Dev Disord, 38(7):1250–1258. Epub 2008 Feb 22.Google Scholar
  67. Sheese, B. E., Rothbart, M. K., Posner, M. I., White, L. K., & Fraundorf, S. H. (2008). Executive attention and self-regulation in infancy. Infant Behavior & Development, 31(3), 501–510. [Epub 2008 Apr 11].CrossRefGoogle Scholar
  68. Sigman, M. D., Kasari, C., Kwon, J. H., & Yirmiya, N. (1992). Responses to the negative emotions of others by autistic, mentally retarded, and normal children. Child Development, 63(4), 796–807.CrossRefPubMedGoogle Scholar
  69. Silani, G., Bird, G., Brindley, R., Singer, T., Frith, C., & Frith, U. (2008). Levels of emotional awareness and autism: An fMRI study. Social Neuroscience, 3(2), 97–112.CrossRefPubMedGoogle Scholar
  70. 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(5661), 1157–1162.CrossRefPubMedGoogle Scholar
  71. Smith A. (2009). Emotional empathy in autism spectrum conditions: Weak intact or heightened? JADD, (This issue).Google Scholar
  72. Spezio, M. L., Adolphs, A., Hurley, R. S. E., & Piven, J. (2007). Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorders, 37, 929–939.CrossRefPubMedGoogle Scholar
  73. Stel, M., van den Heuvel, C., Smeets, R. C. (2008). Facial feedback mechanisms in autistic spectrum disorders. Journal of Autism and Developmental Disorders, 38(7), 1250–1258.CrossRefPubMedGoogle Scholar
  74. Szatmari, P., Georgiades, S., Duku, E., Zwaigenbaum, L., Goldberg, J., & Bennett, T. (2008). Alexithymia in parents of children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 38(10), 1859–1865. [Epub 2008 May 13].CrossRefPubMedGoogle Scholar
  75. Tani, P., Lindberg, N., Joukamaa, M., Nieminen-von Wendt, T., von Wendt, L., Appelberg, B., et al. (2004). Asperger syndrome, alexithymia and perception of sleep. Neuropsychobiology, 49, 64–70.CrossRefPubMedGoogle Scholar
  76. Théoret, H., Halligan, E., Kobayashi, M., Fregni, F., Tager-Flusberg, H., & Pascual-Leone, A. (2005). Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Current Biology, 15(3), R84–R85.CrossRefPubMedGoogle Scholar
  77. Ungerer, J. A. (1990). The early development of empathy: Self-regulation and individual differences in the first year. Motivation and Emotion, 14, 93–106.CrossRefGoogle Scholar
  78. Urgesi, C., Moro, V., Candidi, M., & Aglioti, S. M. (2006). Mapping implied body actions in the human motor system. Journal of Neuroscience, 26, 7942–7949.CrossRefPubMedGoogle Scholar
  79. Welsh, T. N., Ray, M. C., Weeks, D. J., Dewey, D., & Elliott, D. (2009). Does Joe influence Fred’s action? Not if Fred has autism spectrum disorder. Brain Research, 1248, 141–148. [Epub 2008 Nov 12].CrossRefPubMedGoogle Scholar
  80. 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, 655–664.CrossRefPubMedGoogle Scholar
  81. Willemsen-Swinkels, S. H., Bakermans-Kranenburg, M. J., Buitelaar, J. K., van IJzendoorn, M. H., & van Engeland, H. (2000). Insecure and disorganised attachment in children with a pervasive developmental disorder: Relationship with social interaction and heart rate. Journal of Child Psychology and Psychiatry, 41, 759–767.CrossRefPubMedGoogle Scholar
  82. Williams, J. H. G. (2008). Self–other relations in social development and autism: Multiple roles for mirror neurons and other brain bases. Autism Research, 1, 73–90.CrossRefPubMedGoogle Scholar
  83. Yirmiya, N., Sigman, M. D., Kasari, C., & Mundy, P. (1992). Empathy and cognition in high-functioning children with autism. Child Development, 63(1), 150–160.CrossRefPubMedGoogle Scholar
  84. Zahn-Waxler, C., & Radke-Yarrow, M. (1982). The development of altruism: Alternative research strategies. In N. Eisenberg (Ed.), The development of prosocial behavior. New York: Academic Press.Google Scholar
  85. Zahn-Waxler, C., Friedman, S. L., & Cummings, E. M. (1983). Children’s emotions and behaviors in response to infants’ cries. Child Development, 54, 1522–1528.CrossRefPubMedGoogle Scholar
  86. Zahn-Waxler, C., Radke-Yarrow, M., Wagner, E., & Chapman, M. (1992). Development of concern for others. Developmental Psychology, 28, 126–136.CrossRefGoogle Scholar
  87. Zaki, J., Bolger, N., Weber, J., & Ochsner, K. N. (2009). The neural bases of empathic accuracy. Proceedings of the National Academy of Sciences. [Epub ahead of print Jun 23].Google Scholar
  88. Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience, 23(2-3), 143–152.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Ilaria Minio-Paluello
    • 1
  • Michael V. Lombardo
    • 2
  • Bhismadev Chakrabarti
    • 2
    • 3
  • Sally Wheelwright
    • 2
  • Simon Baron-Cohen
    • 2
  1. 1.Dipartimento di Psicologia La SapienzaUniversita’ di RomaRomeItaly
  2. 2.Department of Psychiatry, Autism Research CentreCambridge UniversityCambridgeUK
  3. 3.School of Psychology and Clinical Language SciencesUniversity of ReadingReadingUK

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