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Gaze fixation and the neural circuitry of face processing in autism

Nature Neuroscience volume 8, pages 519–526 (2005)Cite this article

Abstract

Diminished gaze fixation is one of the core features of autism and has been proposed to be associated with abnormalities in the neural circuitry of affect. We tested this hypothesis in two separate studies using eye tracking while measuring functional brain activity during facial discrimination tasks in individuals with autism and in typically developing individuals. Activation in the fusiform gyrus and amygdala was strongly and positively correlated with the time spent fixating the eyes in the autistic group in both studies, suggesting that diminished gaze fixation may account for the fusiform hypoactivation to faces commonly reported in autism. In addition, variation in eye fixation within autistic individuals was strongly and positively associated with amygdala activation across both studies, suggesting a heightened emotional response associated with gaze fixation in autism.

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Figure 1: Study designs and exemplar stimuli.
Figure 2: Average fixation durations.
Figure 3: Brain clusters with significant group differences in brain activation across all faces in Study I.
Figure 4: Brain clusters with significant group differences in brain activation across all faces in Study II.
Figure 5: Brain clusters associated with significant Group × Familiarity interactions in brain activation in Study II.
Figure 6: Brain activation clusters associated with average eye fixation time for the autistic and control groups, Study I.
Figure 7: Brain activation clusters associated with average eye fixation time for the autistic and control groups, Study II.
Figure 8: Clusters in the left amygdala associated with group differences in activation as a function of amount of eye fixation within subjects.

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References

  1. Diagnostic and Statistical Manual of Mental Disorders 4th edn. (American Psychiatric Association, Washington DC, 1994).

  2. Lord, C., Cook, E.H., Leventhal, B. & Amaral, D.G. Autism spectrum disorders. Neuron 28, 355–363 (2000).

    Article  CAS  Google Scholar 

  3. Klin, A., Jones, W., Schultz, R.T., Volkmar, F.R. & Cohen, D.J. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch. Gen. Psychiatry 59, 809–816 (2002).

    Article  Google Scholar 

  4. Ellis, H.D. & Young, A.W. Faces in their social and biological context. in Face and Mind (ed. Young, A.W.) 67–95 (Oxford Univ. Press, London, 1998).

    Chapter  Google Scholar 

  5. Farah, M.J., Wilson, K.D., Drain, M. & Tanaka, J.N. What is 'special' about face perception? Psychol. Rev. 105, 482 (1998).

    Article  CAS  Google Scholar 

  6. Schultz, R.T. et al. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch. Gen. Psychiatry 57, 331–340 (2000).

    Article  CAS  Google Scholar 

  7. Adolphs, R., Sears, L. & Piven, J. Abnormal processing of social information from faces in autism. J. Cogn. Neurosci. 13, 232–240 (2001).

    Article  CAS  Google Scholar 

  8. Joseph, R.M. & Tanaka, J.N. Holistic and part-based face recognition in children with autism. J. Child Psychol. Psychiatry 44, 529–542 (2003).

    Article  Google Scholar 

  9. Osterling, J. & Dawson, G. Early recognition of children with autism: a study of first birthday home videotapes. J. Autism Dev. Disord. 24, 247–257 (1994).

    Article  CAS  Google Scholar 

  10. Osterling, J.A., Dawson, G. & Munson, J.A. Early recognition of 1-year-old infants with autism spectrum disorder versus mental retardation. Dev. Psychopathol. 14, 239–251 (2002).

    Article  Google Scholar 

  11. Mundy, P., Sigman, M. & Kasari, C. Theory of mind and joint-attention deficits in autism. in Understanding Other Minds: Perspectives from Autism (eds. Baron-Cohen, S., Tager-Flusberg, H. & Cohen, D.) 181–203 (Oxford Univ. Press, London, 1994).

    Google Scholar 

  12. Joseph, R.M. & Tager-Flusberg, H. An investigation of attention and affect in children with autism and Down syndrome. J. Autism Dev. Disord. 27, 385–395 (1997).

    Article  CAS  Google Scholar 

  13. Critchley, H.D. et al. The functional neuroanatomy of social behaviour. Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 123, 2203–2212 (2000).

    Article  Google Scholar 

  14. Pierce, K., Muller, R.A., Ambrose, J., Allen, G. & Courchesne, E. Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. Brain 124, 2059–2073 (2001).

    Article  CAS  Google Scholar 

  15. Puce, A., Allison, T., Gore, J.C. & McCarthy, G. Face-sensitive regions in human extrastriate cortex studied by functional MRI. J. Neurophysiol. 74, 1192–1199 (1995).

    Article  CAS  Google Scholar 

  16. Ogai, M. et al. fMRI study of recognition of facial expressions in high-functioning autistic patients. Neuroreport 14, 559–563 (2003).

    Article  Google Scholar 

  17. George, N. et al. Contrast polarity and face recognition in the human fusiform gyrus. Nat. Neurosci. 2, 547–580 (1999).

    Article  Google Scholar 

  18. Lehmann, C. et al. Dissociation between overt and unconscious face processing in fusiform face area. Neuroimage 21, 75–83 (2004).

    Article  Google Scholar 

  19. Lord, C., Rutter, M. & LeCouteur, A. Autism diagnostic interview—revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J. Autism Dev. Disord. 24, 659–685 (1994).

    Article  CAS  Google Scholar 

  20. Glutting, J., Adams, W. & Sheslow, D. Wide Range Intelligence Test (Wide Range, Wilmington, Delaware, USA, 2000).

    Google Scholar 

  21. Lundqvist, D., Flykt, A. & Ohman, A. Karolinska Directed Emotional Faces (Department of Neurosciences, Karolinska Hospital, Stockholm, Sweden, 1998).

    Google Scholar 

  22. Cox, R.W. Analyses of functional neuroimages software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173 (1996).

    Article  CAS  Google Scholar 

  23. Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain: 3-dimensional Proportional System: An Approach to Cerebral Imaging (Thieme Medical, New York, 1988).

    Google Scholar 

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Acknowledgements

We thank all the individuals and families who participated in this research, M. Anderle and R. Fisher for technical assistance in data acquisition, and faculty and staff at the Waisman Center and Waisman Laboratory for Brain Imaging and Behavior for administrative and technical support. This work was supported by a US National Institute of Mental Health (NIMH) Studies to Advance Autism Research and Treatment (STAART) grant U54MH066398 Project IV (R.J.D.), a National Alliance for Research on Schizophrenia and Affective Disorders (NARSAD) Distinguished Investigator Award to R.J.D., a National Institutes of Health core grant P30 HD03352 (M.M. Seltzer) and a National Institutes of Child Health and Human Development training grant T32 HD07489 (L. Abbeduto).

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Authors and Affiliations

  1. Waisman Center, University of Wisconsin, 1500 Highland Avenue, Madison, 53705-2280, Wisconsin, USA

    Kim M Dalton, Morton Ann Gernsbacher, H H Goldsmith, Andrew L Alexander & Richard J Davidson

  2. Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, 1500 Highland Avenue, Madison, 53705-2280, Wisconsin, USA

    Kim M Dalton, Brendon M Nacewicz, Tom Johnstone, Hillary S Schaefer, Andrew L Alexander & Richard J Davidson

  3. Psychology Department, University of Wisconsin, 1202 West Johnson Street, Madison, 53706-1696, Wisconsin, USA

    Morton Ann Gernsbacher, H H Goldsmith & Richard J Davidson

  4. Psychiatry Department, University of Wisconsin, 6001 Research Park Boulevard, Madison, 53719, Wisconsin, USA

    Andrew L Alexander & Richard J Davidson

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Correspondence to Kim M Dalton or Richard J Davidson.

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Dalton, K., Nacewicz, B., Johnstone, T. et al. Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 8, 519–526 (2005). https://doi.org/10.1038/nn1421

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