Abstract
Prior studies have emphasized the contribution of aberrant amygdala structure and function in social aspects of autism. However, it remains largely unknown whether amygdala dysfunction directly impairs visual attention and exploration as has been observed in people with autism spectrum disorders (ASD). Here, gaze patterns were directly compared between a rare amygdala lesion patient and adults with ASD when they freely viewed static images of complex natural scenes. The amygdala lesion patient showed a gaze pattern that was more similar to controls rather than that of the ASD group, which was independent of image content (social vs. objects) or complexity. This finding was further corroborated by analysis of temporal aspects of the gaze patterns and semantic category analysis. Together, the present results suggest that abnormal visual exploration observed in people with ASD is not likely primarily attributed to the amygdala.
References
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.
Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31, 137–145.
Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30, 52–73.
Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. R. (2000). The amygdala theory of autism. Neuroscience and Biobehavioral Reviews, 24, 355–364.
Bauman, M., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35, 866–874.
Becker, B., Mihov, Y., Scheele, D., Kendrick, K. M., Feinstein, J. S., et al. (2012). Fear processing and social networking in the absence of a functional amygdala. Biological Psychiatry, 72, 70–77.
Birmingham, E., Cerf, M., & Adolphs, R. (2011). Comparing social attention in autism and amygdala lesions: effects of stimulus and task condition. Social Neuroscience, 6, 420–435.
Chawarska, K., Macari, S., & Shic, F. (2013). Decreased spontaneous attention to social scenes in 6-month-old infants later diagnosed with autism spectrum disorders. Biological Psychiatry, 74, 195–203.
Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., et al. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8, 519–526.
Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27, 403–424.
Ecker, C., Suckling, J., Deoni, S. C., Lombardo, M. V., Bullmore, E. T., et al. (2012). Brain anatomy and its relationship to behavior in adults with autism spectrum disorder: A multicenter magnetic resonance imaging study. Archives of General Psychiatry, 69, 195–209.
Feinstein, J. S., Adolphs, R., & Tranel, D. (2016). A tale of survival from the world of patient SM. In D. G. Amaral & R. Adolphs (Eds.), Living without an amygdala (pp. 1–38). New York: Guilford Press.
Gotts, S. J., Simmons, W. K., Milbury, L. A., Wallace, G. L., Cox, R. W., & Martin, A. (2012). Fractionation of social brain circuits in autism spectrum disorders. Brain, 135, 2711–2725.
Hamann, S. B., Stefanacci, L., Squire, L. R., Adolphs, R., Tranel, D., et al. (1996). Recognizing facial emotion. Nature, 379, 497.
Happe, F., Ronald, A., & Plomin, R. (2006). Time to give up on a single explanation for autism. Nature Neuroscience, 9, 1218–1220.
Hofer, P. A. (1973). Urbach-Wiethe disease (lipoglycoproteinosis; lipoid proteinosis; hyalinosis cutis et mucosae). A review. Acta Derm Venereol Suppl (Stockh), 53, 1–52.
Kennedy, D. P., D’Onofrio, B. M., Quinn, P. D., Bölte, S., Lichtenstein, P., & Falck-Ytter, T. (2017). Genetic influence on eye movements to complex scenes at short timescales. Current Biology, 27, 3554–3560.
Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., & Heekeren, H. R. (2012). The role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders. The Journal of Neuroscience, 32, 9469–9476.
Lord, C., Rutter, M., Goode, S., Heemsbergen, J., Jordan, H., & Mawhood, L. (1989). Autism diagnostic observation schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185–212.
Osterling, J., & Dawson, G. (1994). Early recognition of children with autism: A study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24, 247–257.
Patin, A., & Hurlemann, R. (2016). Behavioral consequences and compensatory adaptations after early bilateral amygdala damage in monozygotic twins. In D. G. Amaral & R. Adolphs (Eds.), Living without an amygdala (pp. 306–333). New York: The Guilford Press.
Paul, L., Corsello, C., Tranel, D., & Adolphs, R. (2010). Does bilateral damage to the human amygdala produce autistic symptoms? Journal of Neurodevelopmental Disorders, 2, 165–173.
Philip, R. C. M., Dauvermann, M. R., Whalley, H. C., Baynham, K., Lawrie, S. M., & Stanfield, A. C. (2012). A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neuroscience and Biobehavioral Reviews, 36, 901–942.
Rice, K., Moriuchi, J. M., Jones, W., & Klin, A. (2012). Parsing heterogeneity in autism spectrum disorders: visual scanning of dynamic social scenes in school-aged children. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 238–248.
Rutishauser, U., Tudusciuc, O., Wang, S., Mamelak, A. N., Ross, I. B., & Adolphs, R. (2013). Single-neuron correlates of atypical face processing in autism. Neuron, 80, 887–899.
Santos, A., Chaminade, T., Da Fonseca, D., Silva, C., Rosset, D., & Deruelle, C. (2012). Just another social scene: evidence for decreased attention to negative social scenes in high-functioning autism. Journal of Autism and Developmental Disorders, 42, 1790–1798.
Sasson, N. J., Elison, J. T., Turner-Brown, L. M., Dichter, G. S., & Bodfish, J. W. (2011). Brief Report: Circumscribed attention in young children with autism. Journal of Autism and Developmental Disorders, 41, 242–247.
Sasson, N. J., Turner-Brown, L. M., Holtzclaw, T. N., Lam, K. S. L., & Bodfish, J. W. (2008). Children with autism demonstrate circumscribed attention during passive viewing of complex social and nonsocial picture arrays. Autism Research, 1, 31–42.
Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. The Journal of Neuroscience, 26, 7674–7679.
Schumann, C. M., Bauman, M. D., & Amaral, D. G. (2011). Abnormal structure or function of the amygdala is a common component of neurodevelopmental disorders. Neuropsychologia, 49, 745–759.
Schumann, C. M., Hamstra, J., Goodlin-Jones, B. L., Lotspeich, L. J., Kwon, H., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. The Journal of Neuroscience, 24, 6392–6401.
Shic, F., Bradshaw, J., Klin, A., Scassellati, B., & Chawarska, K. (2011). Limited activity monitoring in toddlers with autism spectrum disorder. Brain Research, 1380, 246–254.
Terburg, D., Morgan, B. E., Montoya, E. R., Hooge, I. T., Thornton, H. B., et al. (2012). Hypervigilance for fear after basolateral amygdala damage in humans. Transl Psychiatry, 2, e115.
van Honk, J., Terburg, D., Thornton, H., Stein, D. J., & Morgan, B. (2016). Consequences of selective bilateral lesions to the basolateral amygdala in humans. In D. G. Amaral & R. Adolphs (Eds.), Living without an Amygdala (pp. 334–363). New York: Guilford Press.
Wang, S., & Adolphs, R. (2017). Social saliency. In Q. Zhao (Ed.), Computational and cognitive neuroscience of vision (pp. 171–193). Singapore: Springer.
Wang, S., Jiang, M., Duchesne, X. M., Laugeson Elizabeth, A., Kennedy, D. P., et al. (2015a). Atypical visual saliency in autism spectrum disorder quantified through model-based eye tracking. Neuron, 88, 604–616.
Wang, S., Tsuchiya, N., New, J., Hurlemann, R., & Adolphs, R. (2015b). Preferential attention to animals and people is independent of the amygdala. Social Cognitive and Affective Neuroscience, 10, 371–380.
Wang, S., Yu, R., Tyszka, J. M., Zhen, S., Kovach, C., et al. (2017). The human amygdala parametrically encodes the intensity of specific facial emotions and their categorical ambiguity. Nature Communications, 8, 14821.
Xu, J., Jiang, M., Wang, S., Kankanhalli, M. S., & Zhao, Q. (2014). Predicting human gaze beyond pixels. Journal of Vision, 14, 28.
Acknowledgments
The author thank Tim Armstrong for collecting the data, Rene Hurlemann for contributing the amygdala lesion patient, and Ralph Adolphs and Paula Webster for valuable comments. This research was supported by the West Virginia University and the Dana Foundation.
Author information
Authors and Affiliations
Contributions
SW designed experiments, performed research, analyzed data, and wrote the paper.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, S. Brief Report: Atypical Visual Exploration in Autism Spectrum Disorder Cannot be Attributed to the Amygdala. J Autism Dev Disord 49, 2605–2611 (2019). https://doi.org/10.1007/s10803-019-04009-w
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-019-04009-w