Top

Journal of Autism and Developmental Disorders

Gepubliceerd in:

01-06-2015 | Original Paper

Typical and Atypical Neurodevelopment for Face Specialization: An fMRI Study

Auteurs: Jane E. Joseph, Xun Zhu, Andrew Gundran, Faraday Davies, Jonathan D. Clark, Lisa Ruble, Paul Glaser, Ramesh S. Bhatt

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 6/2015

Abstract

Individuals with autism spectrum disorder (ASD) and their relatives process faces differently from typically developed (TD) individuals. In an fMRI face-viewing task, TD and undiagnosed sibling (SIB) children (5–18 years) showed face specialization in the right amygdala and ventromedial prefrontal cortex, with left fusiform and right amygdala face specialization increasing with age in TD subjects. SIBs showed extensive antero-medial temporal lobe activation for faces that was not present in any other group, suggesting a potential compensatory mechanism. In ASD, face specialization was minimal but increased with age in the right fusiform and decreased with age in the left amygdala, suggesting atypical development of a frontal–amygdala–fusiform system which is strongly linked to detecting salience and processing facial information.

vorige artikel Parents’ Adoption of Social Communication Intervention Strategies: Families Including Children with Autism Spectrum Disorder Who are Minimally Verbal

volgende artikel Autism Spectrum Disorder Risk Factors and Autistic Traits in Gender Dysphoric Children

Alleen toegankelijk voor geautoriseerde gebruikers

Aylward, E. H., Park, J. E., Field, K. M., Parsons, A. C., Richards, T. L., & Cramer, S. C. (2005). Brain activation during face perception: Evidence of a developmental change. Journal of Cognitive Neuroscience, 17, 308–319.CrossRefPubMed

Bailey, A. J., Braeutigam, S., Jousmaki, V., & Swithenby, S. J. (2005). Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: A magnetoencephalographic study. European Journal of Neuroscience, 21, 2575–2585.CrossRefPubMed

Baron-Cohen, S., Ring, H., Chitnis, X., Wheelwright, S., Gregory, L., Williams, S., et al. (2006). fMRI of parents of children with Asperger syndrome: A pilot study. Brain and Cognition, 61(1), 122–130.CrossRefPubMed

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(6), 1891–1898.CrossRefPubMed

Belmonte, M. K., Gomot, M., & Baron-Cohen, S. (2010). Visual attention in autism families: ‘Unaffected’ sibs share atypical frontal activation. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51(3), 259–276.CrossRef

Bolte, S., & Poustka, F. (2003). The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychological Medicine, 33(5), 907–915.CrossRefPubMed

Bookheimer, S., Wang, A. T., Scott, A., Sigman, M., & Dapretto, M. (2008). Frontal contributions to face processing differences in autism: Evidence from fMRI of inverted face processing. Journal of the International Neuropsychological Society, 14(6), 922–932.CrossRefPubMedCentralPubMed

Cantlon, J. F., Pinel, P., Dehaene, S., & Pelphrey, K. A. (2011). Cortical representations of symbols, objects, and faces are pruned back during early childhood. Cerebral Cortex, 21(1), 191–199.CrossRefPubMedCentralPubMed

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.CrossRefPubMed

Corbett, B. A., Carmean, V., Ravizza, S., Wendelken, C., Henry, M. L., Carter, C., et al. (2009). A functional and structural study of emotion and face processing in children with autism. Psychiatry Research: Neuroimaging, 173, 196–205.CrossRefPubMedCentralPubMed

Dalton, K. M., Nacewicz, B. M., Alexander, A. L., & Davidson, R. J. (2007). Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biological Psychiatry, 61, 512–560.CrossRefPubMed

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(4), 519–526.PubMedCentralPubMed

Dawson, G., Carver, L., Meltzoff, A. N., Panagiotides, H., McPartland, J., & Webb, S. J. (2002). Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. Child Development, 73(3), 700–717.CrossRefPubMedCentralPubMed

DiMartino, A., Ross, K., Uddin, L. Q., Sklar, A., 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, 63–74.CrossRef

Domes, G., Heinrichs, M., Kumbier, E., Grossmann, A., Hauenstein, K., & Herpertz, S. C. (2013). Effects of intranasal oxytocin on the neural basis of face processing in autism spectrum disorder. Biological Psychiatry, 74(3), 164–171.CrossRefPubMed

Dunn, L. M., & Dunn, L. M. (1997). Peabody Picture Vocabulary Test (3rd ed.). Circle Pines, MN: American Guidance Service.

Ebner, N. C., Johnson, M. R., Rieckmann, A., Durbin, K. A., Johnson, M. K., & Fischer, H. (2013). Processing own-age vs. other-age faces: Neuro-behavioral correlates and effects of emotion. Neuroimage, 78, 363–371.CrossRefPubMedCentralPubMed

Gathers, A. D., Bhatt, R. S., Corbly, C. R., Farley, A. B., & Joseph, J. E. (2004). Developmental shifts in cortical loci for face and object recognition. NeuroReport, 15(10), 1549–1553.CrossRefPubMed

Golarai, G., Ghahremani, D. G., Whitfield-Gabrieli, S., Reiss, A., Eberhardt, J. L., Gabrieli, J. D., et al. (2007). Differential development of high-level visual cortex correlates with category-specific recognition memory. Nature Neuroscience, 10(4), 512–522.PubMedCentralPubMed

Golarai, G., Liberman, A., Yoon, J., & Grill-Spector, K. (2010). Differential development of the ventral visual cortex extends through adolescence. Frontiers in Human Neuroscience., 3, 80.PubMedCentralPubMed

Grelotti, D. J., Klin, A. J., Gauthier, I., Skudlarski, P., Cohen, D. J., Gore, J. C., et al. (2005). fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia, 43(3), 373–385.CrossRefPubMed

Grice, S. J., Spratling, M. W., Karmiloff-Smith, A., Halit, H., Csibra, G., de Haan, M., et al. (2001). Disordered visual processing and oscillatory brain activity in autism and Williams Syndrome. NeuroReport, 12(12), 2697–2700.CrossRefPubMed

Guyer, A. E., Monk, C. S., McClure-Tone, E. B., Nelson, E. E., Roberson-Nay, R., Adler, A. D., et al. (2008). A developmental examination of amygdala response to facial expressions. Journal of Cognitive Neuroscience, 20(9), 1565–1582.CrossRefPubMedCentralPubMed

Hadjikhani, N., Joseph, R. M., Snyder, J., & Tager-Flusberg, H. (2007). Abnormal activation of the social brain during face perception in autism. Human Brain Mapping, 28(5), 431–440.CrossRef

Hadjikhani, N., Joseph, R. M., Synder, J., Chabris, C. F., Clark, J., Steele, S., et al. (2004). Early visual cortex organization in autism: An fMRI study. NeuroReport, 15(2), 267–270.CrossRefPubMed

Haist, F., Lee, K., & Stiles, J. (2010). Individuating faces and common objects produces equal responses in putative face-processing areas in the ventral occipitotemporal cortex. Frontiers in Human Neurosciences, 4, 181.

Hall, G. B., Doyle, K. A., Goldberg, J., West, D., & Szatmari, P. (2010). Amygdala engagement in response to subthreshold presentations of anxious face stimuli in adults with autism spectrum disorders: preliminary insights. PLoS ONE, 5(5), e10804.CrossRefPubMedCentralPubMed

Hoehl, S., Brauer, J., Brasse, G., Striano, T., & Friederici, A. D. (2010). Children’s processing of emotions expressed by peers and adults: An fMRI study. Social Neuroscience, 5(5–6), 543–559.CrossRefPubMed

Hubl, D., Bolte, S., Feines-Matthews, S., Lanfermann, H., Federspiel, A., Strik, W., et al. (2003). Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology, 61(9), 1232–1237.CrossRefPubMed

Humphreys, K., Hasson, U., Avidan, G., Minshew, N., & Behrmann, M. (2008). Cortical patterns of category-selective activation for faces, places and objects in adults with autism. Autism Research, 1(1), 52–63.CrossRefPubMedCentralPubMed

Jemel, B., Mottron, L., & Dawson, M. (2006). Impaired face processing in autism: Fact or artifact? Journal of Autism and Developmental Disorders, 36(1), 91–106.CrossRefPubMed

Johnson, M. H., Griffin, R., Csibra, G., Halit, H., Farroni, T., De Haan, M., et al. (2005). The emergence of the social brain network: Evidence from typical and atypical development. Development and Psychopathology, 17(3), 599–619.CrossRefPubMedCentralPubMed

Joseph, J. E., & Farley, A. B. (2004). Cortical regions associated with different aspects of object recognition performance. Cognitive, Affective, & Behavioral Neuroscience, 4, 364–378.

Joseph, J. E., & Gathers, A. D. (2003). Effects of structural similarity on neural substrates for object recognition. Cognitive, Affective, & Behavioral Neuroscience, 3, 1–16.

Joseph, J. E., Gathers, A. D., & Bhatt, R. (2011). Progressive and regressive developmental changes in neural substrates for face processing: Testing specific predictions of the interactive specialization account. Developmental Science, 14(2), 227–241.CrossRefPubMedCentralPubMed

Kaiser, M. D., Hudac, C. M., Shultz, S., Lee, S. M., Cheung, C., Berken, A. M., et al. (2010). Neural signatures of autism. Proceedings of the National Academy of Sciences of the USA, 107(49), 21223–21228.CrossRefPubMedCentralPubMed

Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. Journal of Neuroscience, 17(11), 4302–4311.PubMed

Killgore, W. D., & Yurgelun-Todd, D. A. (2007). Unconscious processing of facial affect in children and adolescents. Social Neuroscience, 2(1), 28–47.CrossRefPubMed

Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry, 166(4), 467–475.CrossRefPubMed

Kleinhans, N., Richards, T. L., Johnson, L. C., Weaver, K., Greenson, J., Dawson, G., et al. (2011). fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. NeuroImage, 54, 697–704.CrossRefPubMedCentralPubMed

Kleinhans, N. M., Richards, T., Sterling, L., Stegbauer, K. C., Mahurin, R., Johnson, L. C., et al. (2008). Abnormal functional connectivity in autism spectrum disorders during face processing. Brain, 131, 1000–1012.CrossRefPubMed

Kleinhans, N., Richards, T., Weaver, K., Johnson, L. C., Greenson, J., Dawson, G., et al. (2010). Association between amygdala response to emotional faces and social anxiety in autism spectrum disorders. Neuropsychologia, 48, 3665–3670.CrossRefPubMedCentralPubMed

Koshino, H., Kana, R. K., Keller, T. A., Cherkassky, V. L., Minshew, N. J., & Just, M. A. (2008). fMRI investigation of working memory for faces in autism: Visual coding and underconnectivity with frontal areas. Cerebral Cortex, 18(2), 289–300.CrossRefPubMed

Kriegeskorte, N., Simmons, W. K., Bellgowan, P. S., & Baker, C. I. (2009). Circular analysis in systems neuroscience: The dangers of double dipping. Nature Neuroscience, 12(5), 535–540.CrossRefPubMedCentralPubMed

Liu, X., Steinmetz, N. A., Farley, A. B., Smith, C. D., & Joseph, J. E. (2008). Mid-fusiform activation during object discrimination reflects the process of differentiating structural descriptions. Journal of Cognitive Neuroscience, 20, 1711–1726.

Lobaugh, N. J., Gibson, E., & Taylor, M. J. (2006). Children recruit distinct neural systems for implicit emotional face processing. NeuroReport, 17(2), 215–219.CrossRefPubMed

Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2007). Autism diagnostic observation schedule. Los Angeles, CA: Western Psychological Services.

Marusak, H. A., Carre, J. M., & Thomason, M. E. (2013). The stimuli drive the response: An fMRI study of youth processing adult or child emotional face stimuli. NeuroImage, 83, 679–689.CrossRefPubMed

McClure, E. B. (2000). A meta-analytic review of sex differences in facial expression processing and their development in infants, children, and adolescents. Psychological Bulletin, 126(3), 424–453.CrossRefPubMed

McPartland, J., Dawson, G., Webb, S. J., Panagiotides, H., & Carver, L. (2004). Event-related brain potentials reveal anomalies in temporal processing of faces in autism spectrun disorder. Journal of Child Psychology and Psychiatry, 45(7), 1235–1245.CrossRefPubMed

Minshew, N. J., & Keller, T. A. (2010). The nature of brain dysfunction in autism: Functional brain imaging studies. Current Opinion in Neurology, 23(2), 124–130.CrossRefPubMedCentralPubMed

Monk, C. S., Weng, S.-J., Wiggins, J. L., Kurapati, N., Louro, H. M. C., Carrasco, M., et al. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry and Neuroscience, 35(2), 105–114.CrossRefPubMedCentralPubMed

O’Connor, K., Hamm, J. P., & Kirk, I. J. (2005). The neurophysiological correlates of face processing in adults and children with Asperger’s syndrome. Brain and Cognition, 59, 82–95.CrossRefPubMed

Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.CrossRefPubMed

Pagliaccio, D., Luby, J. L., Gaffrey, M. S., Belden, A. C., Botteron, K. N., Harms, M. P., et al. (2013). Functional brain activation to emotional and nonemotional faces in healthy children: Evidence for developmentally undifferentiated amygdala function during the school-age period. Cognitive, Affective, & Behavioral Neuroscience, 13(4), 771–789.CrossRef

Passarotti, A. M., Paul, B. M., Bussiere, J. R., Buxton, R. B., Wong, E. C., & Stiles, J. (2003). The development of face and location processing: An fMRI study. Developmental Science., 6(1), 100–117.CrossRef

Pelphrey, K., Lopez, J., & Morris, J. P. (2009). Developmental continuity and change in responses to social and nonsocial categories in human extrastriate visual cortex. Frontiers in Human Neuroscience, 3(25), 1–9.

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(4), 249–261.CrossRefPubMed

Perlman, S. B., Hudac, C. M., Pegors, T., Minshew, N. J., & Pelphrey, K. A. (2011). Experimental manipulation of face-evoked activity in the fusiform gyrus of individuals with autism. Social Neuroscience, 6(1), 22–30.CrossRefPubMedCentralPubMed

Pierce, K., Haist, F., Sedaghat, F., & Courchesne, E. (2004). The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond. Brain: A Journal of Neurology, 127(Pt 12), 2703–2716.CrossRef

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.CrossRefPubMed

Pierce, K., & Redcay, E. (2008). Fusiform function in children with an autism spectrum disorder is a matter of “who”. Biological Psychiatry, 64(7), 552–560.CrossRefPubMedCentralPubMed

Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59(3), 2142–2154.CrossRefPubMedCentralPubMed

Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2013). Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage, 84C, 320–341.

Rutter, M., Le Couteur, A., & Lord, C. (2005). Autism Diagnostic Interview revised (ADIR). Los Angeles, CA: Western Psychological Association.

Santos, A., Mier, D., Kirsch, P., & Meyer-Lindenberg, A. (2011). Evidence for a general face salience signal in human amygdala. NeuroImage, 54(4), 3111–3116.CrossRefPubMed

Scherf, K. S., Behrmann, M., & Dahl, R. E. (2012). Facing changes and changing faces in adolescence: A new model for investigating adolescent-specific interactions between pubertal, brain and behavioral development. Developmental Cognitive Neuroscience, 2(2), 199–219.CrossRefPubMed

Scherf, K. S., Behrmann, M., Humphreys, K., & Luna, B. (2007). Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Developmental Science, 10(4), F15–F30.CrossRefPubMed

Scherf, K. S., Luna, B., Avidan, G., & Behrmann, M. (2011). “What” precedes “which”: Developmental neural tuning in face- and place-related cortex. Cerebral Cortex, 21(9), 1963–1980.CrossRefPubMedCentralPubMed

Scherf, K. S., Luna, B., Minshew, N., & Behrmann, M. (2010). Location, location, location: Alterations in the functional topography of face-but not object-or place-related cortex in adolescents with autism. Frontiers in Human Neuroscience, 4, 26.PubMedCentralPubMed

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.CrossRefPubMed

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

Simmons, W. K., Bellgowan, P. S., & Martin, A. (2007). Measuring selectivity in fMRI data. Nature Neuroscience, 10(1), 4–5.CrossRefPubMed

Spencer, M. D., Holt, R. J., Chura, L. R., Calder, A. J., Suckling, J., Bullmore, E. T., et al. (2012). Atypical activation during the embedded figures task as a functional magnetic resonance imaging endophenotype of autism. Brain: A Journal of Neurology, 135(Pt 11), 3469–3480.CrossRef

Spencer, M. D., Holt, R. J., Chura, L. R., Suckling, J., Calder, A. J., Bullmore, E. T., et al. (2011). A novel functional brain imaging endophenotype of autism: The neural response to facial expression of emotion. Translational psychiatry, 1, e19.CrossRefPubMedCentralPubMed

Swartz, J. R., Wiggins, J. L., Carrasco, M., Lord, C., & Monk, C. S. (2013). Amygdala habituation and prefrontal functional connectivity in youth with autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 52(1), 84–93.CrossRefPubMedCentralPubMed

Todd, R. M., Evans, J. W., Morris, D., Lewis, M. D., & Taylor, M. J. (2011). The changing face of emotion: Age-related patterns of amygdala activation to salient faces. Social Cognitive and Affective Neuroscience, 6(1), 12–23.CrossRefPubMedCentralPubMed

Tottenham, N., Hertzig, M. E., Gillespie-Lynch, K., Gilhooly, T., Millner, A. J., & Casey, B. J. (2014). Elevated amygdala response to faces and gaze aversion in autism spectrum disorder. Social Cognitive and Affective Neuroscience, 9(1), 106–117.CrossRefPubMedCentralPubMed

Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273–289.CrossRefPubMed

Uddin, L. Q., Davies, M. S., Scott, A. A., Zaidel, E., Bookheimer, S. Y., Iacoboni, M., et al. (2008). Neural basis of self and other representation in autism: An FMRI study of self-face recognition. PLoS ONE, 3(10), e3526.CrossRefPubMedCentralPubMed

Vasa, R. A., Pine, D. S., Thorn, J. M., Nelson, T. E., Spinelli, S., Nelson, E., et al. (2011). Enhanced right amygdala activity in adolescents during encoding of positively valenced pictures. Developmental Cognitive Neuroscience, 1(1), 88–99.CrossRefPubMedCentralPubMed

von dem Hagen, E. A., Stoyanova, R. S., Rowe, J. B., Baron-Cohen, S., & Calder, A. J. (2014). Direct gaze elicits atypical activation of the theory-of-mind network in autism spectrum conditions. Cerebral Cortex, 24(6), 1485–1492.

Wechsler, D. (2003). Wechsler Intelligence Scale for children (4th ed.). San Antonio, TX: Harcourt Assessment Inc.

Weigelt, S., Koldewyn, K., & Kanwisher, N. (2012). Face identity recognition in autism spectrum disorders: A review of behavioral studies. Neuroscience and Biobehavioral Reviews, 36(3), 1060–1084.CrossRefPubMed

Weng, S. J., Carrasco, M., Swartz, J. R., Wiggins, J. L., Kurapati, N., Liberzon, I., et al. (2011). Neural activation to emotional faces in adolescents with autism spectrum disorders. Journal of Child Psychology and Psychiatry and Allied Disciplines, 52(3), 296–305.CrossRef

Zurcher, N. R., Donnelly, N., Rogier, O., Russo, B., Hippolyte, L., Hadwin, J., et al. (2013). It’s all in the eyes: Subcortical and cortical activation during grotesqueness perception in autism. PLoS ONE, 8(1), e54313.CrossRefPubMedCentralPubMed

Titel: Typical and Atypical Neurodevelopment for Face Specialization: An fMRI Study
Auteurs: Jane E. Joseph
Xun Zhu
Andrew Gundran
Faraday Davies
Jonathan D. Clark
Lisa Ruble
Paul Glaser
Ramesh S. Bhatt
Publicatiedatum: 01-06-2015
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 6/2015
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-014-2330-4

Andere artikelen Uitgave 6/2015

Effectiveness of Community-Based Early Intervention Based on Pivotal Response Treatment

Original Paper

Adolescent Judgments and Reasoning About the Failure to Include Peers with Social Disabilities

Original Paper

Increased Exposure to Rigid Routines can Lead to Increased Challenging Behavior Following Changes to Those Routines

Original Paper

Maternal Smoking and Autism Spectrum Disorder: A Meta-analysis

Original Paper

Detail and Gestalt Focus in Individuals with Optimal Outcomes from Autism Spectrum Disorders

Original Paper

Support Needs of Fathers and Mothers of Children and Adolescents with Autism Spectrum Disorder

Original Paper