Journal of Autism and Developmental Disorders

, Volume 43, Issue 2, pp 272–285

Neural and Behavioral Responses During Self-Evaluative Processes Differ in Youth With and Without Autism

  • Jennifer H. Pfeifer
  • Junaid S. Merchant
  • Natalie L. Colich
  • Leanna M. Hernandez
  • Jeff D. Rudie
  • Mirella Dapretto
Original Paper

Abstract

This fMRI study investigated neural responses while making appraisals of self and other, across the social and academic domains, in children and adolescents with and without autism spectrum disorders (ASD). Compared to neurotypical youth, those with ASD exhibited hypoactivation of ventromedial prefrontal cortex during self-appraisals. Responses in middle cingulate cortex (MCC) and anterior insula (AI) also distinguished between groups. Stronger activity in MCC and AI during self-appraisals was associated with better social functioning in the ASD group. Although self-appraisals were significantly more positive in the neurotypical group, positivity was unrelated to brain activity in these regions. Together, these results suggest that multiple brain regions support making self-appraisals in neurotypical development, and function atypically in youth with ASD.

Keywords

Autism Self Ventral mPFC Anterior insula Middle cingulate cortex Development 

References

  1. Assaf, M., Jagannathan, K., Calhoun, V. D., Miller, L., Stevens, M. C., Sahl, R., et al. (2010). Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage, 53(1), 247–256. doi:10.1016/j.neuroimage.2010.05.067.PubMedCrossRefGoogle Scholar
  2. Berndt, T. J., & Burgy, L. (1996). Social self-concept. In B. A. Bracken (Ed.), Handbook of self-concept: Developmental, social, and clinical considerations (pp. 171–209). New York: Wiley.Google Scholar
  3. Bracken, B. (Ed.). (1996). Handbook of self-concept. New York: Wiley.Google Scholar
  4. Brown, J. D. (1986). Evaluations of self and others: Self-enhancement biases in social judgments. Social Cognition, 4, 353–376. doi:10.1521/soco.1986.4.4.353.CrossRefGoogle Scholar
  5. Bruck, M., London, K., Landa, R., & Goodman, J. (2007). Autobiographical memory and suggestibility in children with autism spectrum disorder. Development and Psychopathology, 19(1), 73–95. doi:10.1017/S0954579407070058.PubMedCrossRefGoogle Scholar
  6. Chen, A. C., Welsh, R. C., Liberzon, I., & Taylor, S. F. (2010). ‘Do I like this person?’ A network analysis of midline cortex during a social preference task. Neuroimage, 51(2), 930–939. doi:10.1016/j.neuroimage.2010.02.044.PubMedCrossRefGoogle Scholar
  7. Cherkassky, V. L., Kana, R. K., Keller, T. A., & Just, M. A. (2006). Functional connectivity in a baseline resting-state network in autism. NeuroReport, 17(16), 1687–1690. doi:10.1097/01.wnr.0000239956.45448.4c.PubMedCrossRefGoogle Scholar
  8. Chiu, P. H., Kayali, M. A., Kishida, K. T., Tomlin, D., Klinger, L. G., Klinger, M. R., et al. (2008). Self responses along cingulate cortex reveal quantitative neural phenotype for high-functioning autism. Neuron, 57(3), 463–473. doi:10.1016/j.neuron.2007.12.020.PubMedCrossRefGoogle Scholar
  9. Coie, J. D., & Cillessen, A. H. N. (1993). Peer rejection: Origins and effects on children’s development. Current Directions in Psychological Science, 2, 89–92.CrossRefGoogle Scholar
  10. Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., et al. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433. doi:10.1023/A:1025014929212.PubMedCrossRefGoogle Scholar
  11. Craig, A. D. (2009). How do you feel—now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10(1), 59–70. doi:10.1038/nrn2555.PubMedCrossRefGoogle Scholar
  12. Crane, L., & Goddard, L. (2008). Episodic and semantic autobiographical memory in adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 38(3), 498–506. doi:10.1007/s10803-007-0420-2.PubMedCrossRefGoogle Scholar
  13. Di Martino, A., Ross, K., Uddin, L. Q., Sklar, A. B., Castellanos, F. X., & Milham, M. P. (2009). Functional brain correlates of social and nonsocial processes in autism spectrum disorders: An activation likelihood estimation meta-analysis. Biological Psychiatry, 65(1), 63–74. doi:10.1016/j.biopsych.2008.09.022.PubMedCrossRefGoogle Scholar
  14. Friston, K. J., Holmes, A. P., Price, C. J., Buchel, C., & Worsley, K. J. (1999). Multisubject fMRI studies and conjunction analyses. Neuroimage, 10, 385–396.PubMedCrossRefGoogle Scholar
  15. Frith, C. D., & Frith, U. (1999). Interacting minds—a biological basis. Science, 286(5445), 1692. doi:10.1126/science.286.5445.1692.PubMedCrossRefGoogle Scholar
  16. Frith, C. D., & Frith, U. (2008). Implicit and explicit processes in social cognition. Neuron, 60(3), 503–510.PubMedCrossRefGoogle Scholar
  17. Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National academy of Sciences of the United States of America, 100(1), 253–258. doi:10.1073/pnas.0135058100.PubMedCrossRefGoogle Scholar
  18. Harter, S. (1999). The construction of the self: A developmental perspective. New York, NY: The Guilford Press.Google Scholar
  19. Heerey, E. A., Keltner, D., & Capps, L. M. (2003). Making sense of self-conscious emotion: Linking theory of mind and emotion in children with autism. Emotion (Washington, DC), 3(4), 394–400. doi:10.1037/1528-3542.3.4.394.CrossRefGoogle Scholar
  20. Henderson, H. A., Zahka, N. E., Kojkowski, N. M., Inge, A. P., Schwartz, C. B., Hileman, C. M., et al. (2009). Self-referenced memory, social cognition, and symptom presentation in autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 50(7), 853–861. doi:10.1111/j.1469-7610.2008.02059.x.CrossRefGoogle Scholar
  21. Hillier, A., & Allinson, L. (2002). Beyond expectations: Autism, understanding embarrassment, and the relationship with theory of mind. Autism: The International Journal of Research and Practice, 6(3), 299–314. doi:10.1177/1362361302006003007.CrossRefGoogle Scholar
  22. Hobson, P. R., Chidambi, G., Lee, A., & Meyer, J. (2006). Foundations for self-awareness: An exploration through autism. Monographs of the Society for Research in Child Development, 71(2), vii–166. doi:10.1111/j.1540-5834.2006.00387.x.PubMedCrossRefGoogle Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. Kennedy, D. P., & Courchesne, E. (2008a). Functional abnormalities of the default network during self- and other-reflection in autism. Social Cognitive and Affective Neuroscience, 3(2), 177–190. doi:10.1093/scan/nsn011.PubMedCrossRefGoogle Scholar
  25. Kennedy, D. P., & Courchesne, E. (2008b). The intrinsic functional organization of the brain is altered in autism. Neuroimage, 39(4), 1877–1885. doi:10.1016/j.neuroimage.2007.10.052.PubMedCrossRefGoogle Scholar
  26. Krienen, F. M., Tu, P., & Buckner, R. L. (2010). Clan mentality: Evidence that the medial prefrontal cortex responds to close others. The Journal of Neuroscience, 30(41), 13906–13915. doi:10.1523/JNEUROSCI.2180-10.2010.PubMedCrossRefGoogle Scholar
  27. Kwan, V. S., John, O. P., Robins, R. W., & Kuang, L. L. (2008). Conceptualizing and assessing self-enhancement bias: A componential approach. Journal of Personality and Social Psychology, 94(6), 1062–1077. doi:10.1037/0022-3514.94.6.1062.PubMedCrossRefGoogle Scholar
  28. Lamm, C., Batson, C. D., & Decety, J. (2007). The neural substrate of human empathy: Effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience, 19(1), 42–58.PubMedCrossRefGoogle Scholar
  29. Leary, M. R., & Tangney, J. P. (2003). The self as an organizing construct in the behavioral and social sciences. In Handbook of self and identity. (pp. 3–14). Guilford Press.Google Scholar
  30. Lee, A., & Hobson, R. P. (1998). On developing self-concepts: A controlled study of children and adolescents with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39(8), 1131–1144.CrossRefGoogle Scholar
  31. Lee, A., Hobson, R. P., & Chiat, S. (1994). I, you, me, and autism: An experimental study. Journal of Autism and Developmental Disorders, 24(2), 155–176.PubMedCrossRefGoogle Scholar
  32. Lind, S. E. (2010). Memory and the self in autism: A review and theoretical framework. Autism: The International Journal of Research and Practice, 14(5), 430–456. doi:10.1177/1362361309358700.CrossRefGoogle Scholar
  33. Lind, S. E., & Bowler, D. M. (2009a). Delayed self-recognition in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 39(4), 643–650. doi:10.1007/s10803-008-0670-7.PubMedCrossRefGoogle Scholar
  34. Lind, S. E., & Bowler, D. M. (2009b). Recognition memory, self-other source memory, and theory-of-mind in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 39(9), 1231–1239. doi:10.1007/s10803-009-0735-2.PubMedCrossRefGoogle Scholar
  35. Lombardo, M. V., Barnes, J. L., Wheelwright, S. J., & Baron-Cohen, S. (2007). Self-Referential cognition and empathy in autism. PLoS One, 2(9), e883. doi:10.1371/journal.pone.0000883.PubMedCrossRefGoogle Scholar
  36. Lombardo, M. V., & Baron-Cohen, S. (2011). The role of the self in mindblindness in autism. Consciousness and Cognition, 20(1), 130–140. doi:10.1016/j.concog.2010.09.006.PubMedCrossRefGoogle Scholar
  37. Lombardo, M. V., Charkrabarti, B., Bullmore, E. T., Sadek, S. A., Pasco, G., Wheelwright, S. J., et al. (2010). Atypical neural self-representation in autism. Brain, 133(2), 611–624. doi:10.1093/brain/awp306.PubMedCrossRefGoogle Scholar
  38. Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223. doi:10.1023/A:1005592401947.PubMedCrossRefGoogle Scholar
  39. Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24(5), 659–685.PubMedCrossRefGoogle Scholar
  40. Margulies, D. S., Vincent, J. L., Kelly, C., Lohmann, G., Uddin, L. Q., Biswal, B. B., et al. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proceedings of the National Academy of Sciences, 106(47), 20069–20074.Google Scholar
  41. Markus, H. (1977). Self-schemata and processing information about the self. Journal of Personality and Social Psychology, 35(2), 63–78.CrossRefGoogle Scholar
  42. Marsh, H. W. (1990). Causal ordering of academic self-concept and academic achievement: A multiwave, longitudinal panel analysis. Journal of Educational Psychology, 82, 646–656.CrossRefGoogle Scholar
  43. McConnell, S. R. (2002). Interventions to facilitate social interaction for young children with autism: Review of available research and recommendations for educational intervention and future research. Journal of Autism and Developmental Disorders, 32(5), 351–372. doi:10.1023/A:1020537805154.PubMedCrossRefGoogle Scholar
  44. Millward, C., Powell, S., Messer, D., & Jordan, R. (2000). Recall for self and other in autism: Children’s memory for events experienced by themselves and their peers. Journal of Autism and Developmental Disorders, 30(1), 15–28. doi:10.1023/A:1005455926727.PubMedCrossRefGoogle Scholar
  45. Mitchell, J. P. (2009). Inferences about other minds. Philosophical Transactions of the Royal Society B, 364, 1309–1316.CrossRefGoogle Scholar
  46. Modinos, G., Ormel, J., & Aleman, A. (2009). Activation of Anterior Insula during Self-Reflection. PLoS One, 4(2), e4618. doi:10.1371/journal.pone.0004618.PubMedCrossRefGoogle Scholar
  47. Monk, C. S., Peltier, S. J., Wiggins, J. L., Weng, S. J., Carrasco, M., Risi, S., et al. (2009). Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage, 47(2), 764–772. doi:10.1016/j.neuroimage.2009.04.069.PubMedCrossRefGoogle Scholar
  48. Moran, J. M., Macrae, C. N., Heatherton, T. F., Wyland, C. L., & Kelley, W. M. (2006). Neuroanatomical evidence for distinct cognitive and affective components of self. Journal of Cognitive Neuroscience, 18(9), 1586–1594.PubMedCrossRefGoogle Scholar
  49. Noles, S. W., Cash, T. F., & Winstead, B. A. (1985). Body image, physical attractiveness, and depression. Journal of Consulting and Clinical Psychology, 53, 88–94.PubMedCrossRefGoogle Scholar
  50. Northoff, G., & Bermpohl, F. (2004). Cortical midline structures and the self. Trends in Cognitive Sciences, 8(3), 102–107. doi:10.1016/j.tics.2004.01.004.PubMedCrossRefGoogle Scholar
  51. Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain–a meta-analysis of imaging studies on the self. Neuroimage, 31(1), 440–457. doi:10.1016/j.neuroimage.2005.12.002.PubMedCrossRefGoogle Scholar
  52. Northoff, G., Qin, P., & Feinberg, T. E. (2011). Brain imaging of the self—conceptual, anatomical, and methodological issues. Consciousness and Cognition, 20, 52–64. doi:10.1016/j.concog.2010.09.011.PubMedCrossRefGoogle Scholar
  53. 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. doi:10.1016/j.neuroimage.2005.06.069.PubMedCrossRefGoogle Scholar
  54. Pfeifer, J. H., Lieberman, M. D., & Dapretto, M. (2007). “I know you are but what am I?!”: Comparing the neural bases of self- and social knowledge retrieval in children and adults. Journal of Cognitive Neuroscience, 19, 1323–1337.PubMedCrossRefGoogle Scholar
  55. Pfeifer, J. H., Masten, C. L., Borofsky, L. A., Dapretto, M., Lieberman, M. D., & Fuligni, A. J. (2009). Neural correlates of direct and reflected self-appraisals in adolescents and adults: When social perspective-taking informs self-perception. Child Development, 80, 1016–1034.PubMedCrossRefGoogle Scholar
  56. Pfeifer, J. H., & Peake, S. J. (2012). Self-development: Integrating cognitive, social, and neuroimaging perspectives. Developmental Cognitive Neuroscience,. doi:10.1016/j.dcn.2011.07.012.PubMedGoogle Scholar
  57. Qin, P., Liu, Y., Shi, J., Wang, Y., Duncan, N., Gong, Q., et al. (2012). Dissociation between anterior and posterior cortical regions during self-specificity and familiarity: A combined fMRI-meta-analytic study. Human Brain Mapping, 33, 154–164. doi:10.1002/hbm.21201.PubMedCrossRefGoogle Scholar
  58. Raichle, M. E., & Snyder, A. Z. (2007). A default mode of brain function: A brief history of an evolving idea. Neuroimage, 37(4), 1083–1090; discussion 1097–1099. doi:10.1016/j.neuroimage.2007.02.041.
  59. Ray, R. D., Shelton, A. L., Hollon, N. G., Michel, B. D., Frankel, C. B., Gross, J. J., et al. (2009). Cognitive and neural development of individuated self-representation in children. Child Development, 80(4), 1232–1242. doi:10.1111/j.1467-8624.2009.01327.x.PubMedCrossRefGoogle Scholar
  60. Robins, R. W., Tracy, J. L., & Trzesniewski, K. H. (2008). Naturalizing the self. In Handbook of personality: Theory and research (3rd ed., pp. 375–398). Guilford Press.Google Scholar
  61. Saxe, R. (2010). The right temporo-parietal junction: A specific brain region for thinking about thoughts. In A. Leslie, & T. German (Eds.), Handbook of theory of mind.Google Scholar
  62. Schmitz, T. W., Kawahara-Baccus, T. N., & Johnson, S. C. (2004). Metacognitive evaluation, self-relevance, and the right prefrontal cortex. Neuroimage, 22, 941–947.PubMedCrossRefGoogle Scholar
  63. Schulte-Ruther, M., Greimel, E., Markowitsch, H. J., Kamp-Becker, I., Remschmidt, H., Fink, G. R., et al. (2011). Dysfunctions in brain networks supporting empathy: An fMRI study in adults with autism spectrum disorders. Social Neuroscience, 6, 1–21.PubMedCrossRefGoogle Scholar
  64. Sedikides, C., & Spencer, S. J. (Eds.) (2007). The self: Frontiers in social psychology. New York, NY: Psychology Press.Google Scholar
  65. Sedikides, C., & Gregg, A. P. (2008). Self-enhancement: Food for thought. Perspectives on Psychological Science, 3(2), 102. doi:10.1111/j.1745-6916.2008.00068.x.CrossRefGoogle Scholar
  66. Sigman, M., & Ruskin, E. (1999). Continuity and change in the social competence of children with autism, Down syndrome, and developmental delays. Monographs of the Society for Research in Child Development, 64, 1–130.PubMedCrossRefGoogle Scholar
  67. 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, 1157–1162.PubMedCrossRefGoogle Scholar
  68. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155. doi:10.1002/hbm.10062.PubMedCrossRefGoogle Scholar
  69. Summerfield, J. J., Hassabis, D., & Maguire, E. (2010). Differential engagement of brain regions within a ‘core’ network during scene construction. Neuropsychologia, 48, 1501–1509.PubMedCrossRefGoogle Scholar
  70. Svoboda, E., McKinnon, M. C., & Levine, B. (2006). The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia, 44, 2189–2208. doi:10.1016/j.neuropsychologia.2006.05.023.PubMedCrossRefGoogle Scholar
  71. Taylor, S. E., & Brown, J. D. (1988). Illusion and well-being: A social psychological perspective on mental health. Psychological Bulletin, 103, 193–210.PubMedCrossRefGoogle Scholar
  72. Toichi, M., Kamio, Y., Okada, T., Sakihama, M., Youngstrom, E. A., Findling, R. L., et al. (2002). A lack of self-consciousness in autism. The American Journal of Psychiatry, 159(8), 1422–1424. doi:10.1176/appi.ajp.159.8.1422.PubMedCrossRefGoogle Scholar
  73. Tomlin, D., Kayali, M. A., King-Casas, B., Anen, C., Camerer, C. F., Quartz, S. R., et al. (2006). Agent-Specific responses in the cingulate cortex during economic exchanges. Science (New York, NY), 312(5776), 1047–1050. doi:10.1126/science.1125596.CrossRefGoogle Scholar
  74. Uddin, L. Q. (2011). The self in autism: An emerging view from neuroimaging. Neurocase, 17(3), 201–208. doi:10.1080/13554794.2010.509320.PubMedCrossRefGoogle Scholar
  75. Uddin, L. Q., Supekar, K., & Menon, V. (2010). Typical and atypical development of functional human brain networks: Insights from resting-state FMRI. Frontiers in Systems Neuroscience, 4, 21. doi:10.3389/fnsys.2010.00021.PubMedGoogle Scholar
  76. Wechsler, D. (1991). WISC-III manual. New York: The Psychological Corporation.Google Scholar
  77. Wechsler, D. (1999). The Wechsler Abbreviated Scale of intelligence-UK. San Antonio, TX: The Psychological Corporation.Google Scholar
  78. Weng, S. J., Wiggins, J. L., Peltier, S. J., Carrasco, M., Risi, S., Lord, C., et al. (2010). Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Research, 1313, 202–214. doi:10.1016/j.brainres.2009.11.057.PubMedCrossRefGoogle Scholar
  79. Williams, D. M., & Happé, F. (2009). What did I say? Versus what did I think? Attributing false beliefs to self amongst children with and without autism. Journal of Autism and Developmental Disorders, 39(6), 865–873. doi:10.1007/s10803-009-0695-6.PubMedCrossRefGoogle Scholar
  80. Williams, D., & Happé, F. (2010). Recognising ‘social’ and ‘non-social’ emotions in self and others: A study of autism. Autism: The International Journal of Research and Practice, 14(4), 285–304. doi:10.1177/1362361309344849.CrossRefGoogle Scholar
  81. Yarkoni, T., Poldrack, R. A., Nichols, T. E., Van Essen, D. C., & Wager, T. D. (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 8, 665–670. doi:10.1038/nmeth.1635.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Jennifer H. Pfeifer
    • 1
  • Junaid S. Merchant
    • 1
  • Natalie L. Colich
    • 2
    • 3
  • Leanna M. Hernandez
    • 3
  • Jeff D. Rudie
    • 4
  • Mirella Dapretto
    • 3
    • 5
    • 6
    • 7
  1. 1.Department of Psychology1227 University of OregonEugeneUSA
  2. 2.Department of PsychologyStanford UniversityStanfordUSA
  3. 3.Ahmanson-Lovelace Brain Mapping Center, David Geffen School of MedicineUniversity of California, Los AngelesLos AngelesUSA
  4. 4.Neuroscience Interdepartmental Program, David Geffen School of MedicineUniversity of California, Los AngelesLos AngelesUSA
  5. 5.Center for Autism Research and Treatment, Semel Institute for Neuroscience and Human Behavior, David Geffen School of MedicineUniversity of California, Los AngelesLos AngelesUSA
  6. 6.Department of Psychiatry and Biobehavioral Sciences, David Geffen School of MedicineUniversity of California, Los AngelesLos AngelesUSA
  7. 7.FPR-UCLA Center for Culture, Brain, and DevelopmentUniversity of California, Los AngelesLos AngelesUSA

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