Journal of Autism and Developmental Disorders

, Volume 38, Issue 6, pp 1072–1080 | Cite as

Emotional Modulation of Perception in Asperger’s Syndrome

Original Paper


Using an attentional blink paradigm, we show that the typical enhancement of perception for emotionally arousing events is significantly reduced in Asperger’s syndrome (AS) at short inter-target intervals. Control experiments demonstrate that this finding cannot be attributed to differences in the perceived arousal of the stimuli, or to a global impairment affecting any type of modulation of perceptual encoding. Because a functioning amygdala is critical for emotional modulation of the attentional blink, the findings support a role for the amygdala in the pathophysiology of AS. More specifically, they suggest there is a fundamental failure of the amygdala to modulate processing in cortex, a concept at the heart of some recent theories of amygdala involvement in the aetiology of autistic-spectrum disorders.


Social cognition Amygdala Autism Fear Attentional blink Emotion 



The authors were supported by a grant from the Wellcome Trust.


  1. Abell, F., Krams, M., Ashburner, J., Passingham, R., Friston, K., Frackowiak, R., et al. (1999). The neuroanatomy of autism: A voxel-based whole brain analysis of structural scans. Neuroreport, 10, 1647–1651.PubMedCrossRefGoogle Scholar
  2. Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience, 14, 1264–1274.PubMedCrossRefGoogle Scholar
  3. Adolphs, R., Gosselin, F., Buchanan, T. W., Tranel, D., Schyns, P., & Damasio, A. R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433, 68–72.PubMedCrossRefGoogle Scholar
  4. Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669–672.PubMedCrossRefGoogle Scholar
  5. American Psychiatry Association. (1994). Diagnostic and statistical manual. (4th ed.). Washington: APA Press.Google Scholar
  6. Anderson, A. K. (2005). Affective influences on the attentional dynamics supporting awareness. Journal of Experimental Psychology-General, 134, 258–281.PubMedCrossRefGoogle Scholar
  7. Anderson, A. K., & Phelps, E. A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305–309.PubMedCrossRefGoogle Scholar
  8. Arend, I., & Botella, J. (2002). Emotional stimuli reduce the attentional blink in sub-clinical anxious subjects. Psicothema, 14, 209–214.Google Scholar
  9. Aylward, E. H., Minshew, N. J., Goldstein, G., Honeycutt, N. A., Augustine, A. M., Yates, K. O., et al. (1999). MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology, 53, 2145–2150.PubMedGoogle Scholar
  10. Baron-Cohen, S., Ring, H. A., Wheelwright, S., Bullmore, E. T., Brammer, M. J., Simmons, A., et al. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11, 1891–1898.PubMedCrossRefGoogle Scholar
  11. 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, 241–251.CrossRefGoogle Scholar
  12. 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, 5–17.PubMedCrossRefGoogle Scholar
  13. Baron-Cohen, S., Wheelwright, S., & Jolliffe, T. (1997). Is there a ‘‘language of the eyes’’? Evidence from normal adults, and adults with autism or Asperger Syndrome. Visual Cognition, 4, 311–331.CrossRefGoogle Scholar
  14. Boraston, Z., Blakemore, S. J., Chilvers, R., & Skuse, D. (2007). Impaired sadness recognition is linked to social interaction deficit in autism. Neuropsychologia, 45, 1501–1510.PubMedCrossRefGoogle Scholar
  15. Castelli, F., Frith, C., Happe, F., & Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125, 1839–1849.PubMedCrossRefGoogle Scholar
  16. 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, 427–433.PubMedCrossRefGoogle Scholar
  17. Corden, B., Chilvers, R. & Skuse, D. (2007). Avoidance of emotionally arousing stimuli predicts social-perceptual impairment in Asperger’s syndrome. Neuropsychologia, e-pub ahead of print.Google Scholar
  18. Corden, B., Critchley, H. D., Skuse, D., & Dolan, R. J. (2006). Fear recognition ability predicts differences in social cognitive and neural functioning in men. Journal of Cognitive Neuroscience, 18, 889–897.PubMedCrossRefGoogle Scholar
  19. Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C. R., Van Amelsvoort, T., Robertson, D. M., et al. (2000). The functional neuroanatomy of social behaviour—changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain, 123, 2203–2212.PubMedCrossRefGoogle Scholar
  20. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8, 526.Google Scholar
  21. Dawson, M. E., Schell, A. M., & Filion, D. L. (2000). The electrodermal system. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of Psychophysiology (2nd ed.). Cambridge University Press.Google Scholar
  22. Dolan, R. J. (2002). Emotion, cognition, and behavior. Science, 298, 1191–1194.PubMedCrossRefGoogle Scholar
  23. Dziobek, I., Fleck, S., Rogers, K., Wolf, O. T., & Convit, A. (2006). The ‘amygdala theory of autism’ revisited: Linking structure to behavior. Neuropsychologia, 44(10), 1891–1899.PubMedCrossRefGoogle Scholar
  24. Ekman, P., & Friesen, W. (1976). Pictures of facial affect. Palo Alto: Consulting Psychologists Press.Google Scholar
  25. Grelotti, D. J., Gauthier, I., & Schultz, R. T. (2002). Social interest and the development of cortical face specialization: What autism teaches us about face processing. Developmental Psychobiology, 40, 213–225.PubMedCrossRefGoogle Scholar
  26. Happe, F. (1994). An advanced test of theory of mind: understanding of story characters’ feelings and thoughts by able autistic, mentally handicapped, and normal children and adults. Journal of Autism and Developmental Disorders, 24, 129–154.PubMedCrossRefGoogle Scholar
  27. Haznedar, M. M., Buchsbaum, M. S., Wei, T. C., Hof, P. R., Cartwright, C., Bienstock, C. A., et al. (2000). Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging. American Journal of Psychiatry, 157, 1994–2001.PubMedCrossRefGoogle Scholar
  28. Heberlein, A. S., & Adolphs, R. (2004). Impaired spontaneous anthropomorphizing despite intact perception and social knowledge. Proceedings of the National Academy of Sciences of the United States of America, 101, 7487–7491.PubMedCrossRefGoogle Scholar
  29. Howard, M. A., Cowell, P. E., Boucher, J., Broks, P., Mayes, A., Farrant, A., et al. (2000). Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport, 11, 2931–2935.PubMedCrossRefGoogle Scholar
  30. Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59, 809–816.PubMedCrossRefGoogle Scholar
  31. 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, 205–223.PubMedCrossRefGoogle Scholar
  32. Lord, C., Rutter, M., & Lecouteur, 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, 659–685.PubMedCrossRefGoogle Scholar
  33. Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., et al. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature, 383, 812–815.PubMedCrossRefGoogle Scholar
  34. Munson, J., Dawson, G., Abbott, R., Faja, S., Webb, S. J., Friedman, S. D., et al. (2006). Amygdalar volume and behavioral development in autism. Archives of General Psychiatry, 63, 686–693.PubMedCrossRefGoogle Scholar
  35. Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., Alexander, A. L., & Davidson, R. J. (2006). Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Archives of General Psychiatry, 63(12), 1417–1428.PubMedCrossRefGoogle Scholar
  36. Ogawa, T., & Suzuki, N. (2004). On the saliency of negative stimuli: Evidence from attentional blink. Japanese Psychological Research, 46, 20–30.CrossRefGoogle Scholar
  37. Palmen, S. J. M. C., Durston, S., Nederveen, H., & van Engeland, H. (2006). No evidence of preferential involvement of medial temporal lobe structures in high-functioning autism. Psychological Medicine, 36, 827–834.PubMedCrossRefGoogle Scholar
  38. Pelphrey, K. A., Sasson, N. J., Reznick, J. S., Paul, G., Goldman, B. D., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32, 249–261.PubMedCrossRefGoogle Scholar
  39. Phelps, E. A., & Le Doux, J. E. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48, 175–187.PubMedCrossRefGoogle Scholar
  40. Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the fusiform ‘face area’ in autism: evidence from functional MRI. Brain, 124, 2059–2073.PubMedCrossRefGoogle Scholar
  41. Raymond, J. E., Shapiro, K. L., & Arnell, K. M. (1992). Temporary suppression of visual processing in an Rsvp Task—an attentional blink. Journal of Experimental Psychology-Human Perception and Performance, 18, 849–860.PubMedCrossRefGoogle Scholar
  42. Ristic, J., Mottron, L., Friesen, C. K., Iarocci, G., Burack, J. A., & Kingstone, A. (2005). Eyes are special but not for everyone: the case of autism. Cognitive Brain Research, 24, 715–718.PubMedCrossRefGoogle Scholar
  43. Rojas, D. C., Smith, J. A., Benkers, T. L., Camou, S. L., Reite, M. L., & Rogers, S. J. (2004). Hippocampus and amygdala volumes in parents of children with autistic disorder. American Journal of Psychiatry, 161, 2038–2044.PubMedCrossRefGoogle Scholar
  44. Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303–316.PubMedGoogle Scholar
  45. Schultz, R. T. (2005). Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23, 125–141.PubMedCrossRefGoogle Scholar
  46. Schultz, R. T., Romanski, L., & Tsatsanis, K. (2000). Neurofunctional models of autistic disorder and Asperger syndrome: Clues from neuroimaging. In A. Klin, F. Volkmar, & S. S. Sparrow (Eds.), Asperger syndrome (pp. 179–209). New York: Plenum Press.Google Scholar
  47. Shapiro, K., Arnell, K. M., & Raymond, J. E. (1997). The attentional blink. Trends in Cognitive Sciences, 1, 291–296.CrossRefGoogle Scholar
  48. Skuse, D., Warrington, R., Bishop, D., Chowdhury, U., Lau, J., Mandy, W., et al. (2004). The developmental, dimensional and diagnostic interview (3di): A novel computerized assessment for autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 43, 548–558.PubMedCrossRefGoogle Scholar
  49. Spezio, M. L., Adolphs, R., Hurley, R. S., & Piven, J. (2006). Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorders, online publication, 37(5), 929–939.Google Scholar
  50. Volkmar, F. R., Klin, A., Siegel, B., Szatmari, P., Lord, C., Campbell, M., et al. (1994). Field trial for autistic disorder in DSM-IV. American Journal of Psychiatry, 151, 1361–1367.PubMedGoogle Scholar
  51. Volkmar, F. R., Lord, C., Bailey, A., Schultz, R. T., & Klin, A. (2004). Autism and pervasive developmental disorders. Journal of Child Psychology and Psychiatry, 45, 135–170.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Behavioural and Brain Sciences Unit, Institute of Child HealthUniversity College LondonLondonUK
  2. 2.Wolfson CollegeCambridgeUK

Personalised recommendations