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Gepubliceerd in: Journal of Autism and Developmental Disorders 6/2019

10-04-2019 | Brief Report

Brief Report: Atypical Visual Exploration in Autism Spectrum Disorder Cannot be Attributed to the Amygdala

Auteur: Shuo Wang

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 6/2019

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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.
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Literatuur
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31, 137–145.CrossRefPubMed Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31, 137–145.CrossRefPubMed
go back to reference Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30, 52–73.CrossRef Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30, 52–73.CrossRef
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference Bauman, M., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35, 866–874.CrossRefPubMed Bauman, M., & Kemper, T. L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35, 866–874.CrossRefPubMed
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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. 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.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference Hamann, S. B., Stefanacci, L., Squire, L. R., Adolphs, R., Tranel, D., et al. (1996). Recognizing facial emotion. Nature, 379, 497.CrossRefPubMed Hamann, S. B., Stefanacci, L., Squire, L. R., Adolphs, R., Tranel, D., et al. (1996). Recognizing facial emotion. Nature, 379, 497.CrossRefPubMed
go back to reference Happe, F., Ronald, A., & Plomin, R. (2006). Time to give up on a single explanation for autism. Nature Neuroscience, 9, 1218–1220.CrossRefPubMed Happe, F., Ronald, A., & Plomin, R. (2006). Time to give up on a single explanation for autism. Nature Neuroscience, 9, 1218–1220.CrossRefPubMed
go back to reference Hofer, P. A. (1973). Urbach-Wiethe disease (lipoglycoproteinosis; lipoid proteinosis; hyalinosis cutis et mucosae). A review. Acta Derm Venereol Suppl (Stockh), 53, 1–52. Hofer, P. A. (1973). Urbach-Wiethe disease (lipoglycoproteinosis; lipoid proteinosis; hyalinosis cutis et mucosae). A review. Acta Derm Venereol Suppl (Stockh), 53, 1–52.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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. 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.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. The Journal of Neuroscience, 26, 7674–7679.CrossRefPubMed Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. The Journal of Neuroscience, 26, 7674–7679.CrossRefPubMed
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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. 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.
go back to reference Wang, S., & Adolphs, R. (2017). Social saliency. In Q. Zhao (Ed.), Computational and cognitive neuroscience of vision (pp. 171–193). Singapore: Springer.CrossRef Wang, S., & Adolphs, R. (2017). Social saliency. In Q. Zhao (Ed.), Computational and cognitive neuroscience of vision (pp. 171–193). Singapore: Springer.CrossRef
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
go back to reference Xu, J., Jiang, M., Wang, S., Kankanhalli, M. S., & Zhao, Q. (2014). Predicting human gaze beyond pixels. Journal of Vision, 14, 28.CrossRefPubMed Xu, J., Jiang, M., Wang, S., Kankanhalli, M. S., & Zhao, Q. (2014). Predicting human gaze beyond pixels. Journal of Vision, 14, 28.CrossRefPubMed
Metagegevens
Titel
Brief Report: Atypical Visual Exploration in Autism Spectrum Disorder Cannot be Attributed to the Amygdala
Auteur
Shuo Wang
Publicatiedatum
10-04-2019
Uitgeverij
Springer US
Gepubliceerd in
Journal of Autism and Developmental Disorders / Uitgave 6/2019
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI
https://doi.org/10.1007/s10803-019-04009-w

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