Top

Journal of Autism and Developmental Disorders

Gepubliceerd in:

04-09-2015 | Original Paper

Altered Dynamics of the fMRI Response to Faces in Individuals with Autism

Auteurs: Natalia M. Kleinhans, Todd Richards, Jessica Greenson, Geraldine Dawson, Elizabeth Aylward

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 1/2016

Abstract

Abnormal fMRI habituation in autism spectrum disorders (ASDs) has been proposed as a critical component in social impairment. This study investigated habituation to fearful faces and houses in ASD and whether fMRI measures of brain activity discriminate between ASD and typically developing (TD) controls. Two identical fMRI runs presenting masked fearful faces, houses, and scrambled images were collected. We found significantly slower fMRI responses to fearful faces but not houses in ASD. In addition, the pattern of slow to emerge amygdala activation to faces had robust discriminability [ASD vs. TD; area under the curve (AUC) = .852, p < .001]. In contrast, habituation to houses had no predictive value (AUC = .573, p = .365). Amygdala habituation to emotional faces may be useful for quantifying risk in ASD.

vorige artikel Parents’ Translations of Child Gesture Facilitate Word Learning in Children with Autism, Down Syndrome and Typical Development

volgende artikel Are Sensory Processing Features Associated with Depressive Symptoms in Boys with an ASD?

Alleen toegankelijk voor geautoriseerde gebruikers

Adolphs, R., & Tranel, D. (2003). Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions. Neuropsychologia, 41(10), 1281–1289.PubMedCrossRef

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(9), 2145–2150.PubMedCrossRef

Bertone, A., Mottron, L., Jelenic, P., & Faubert, J. (2005). Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity. Brain, 128(10), 2430–2441. doi:10.1093/brain/awh561.PubMedCrossRef

Braeutigam, S., Bailey, A. J., & Swithenby, S. J. (2001). Task-dependent early latency (30–60 ms) visual processing of human faces and other objects. NeuroReport, 12(7), 1531–1536.PubMedCrossRef

Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., et al. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17(5), 875–887.PubMedCrossRef

Bukowski, H., Dricot, L., Hanseeuw, B., & Rossion, B. (2013). Cerebral lateralization of face-sensitive areas in left-handers: Only the FFA does not get it right. Cortex, 49(9), 2583–2589. doi:10.1016/j.cortex.2013.05.002.PubMedCrossRef

Caspers, J., Zilles, K., Amunts, K., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2013). Functional characterization and differential coactivation patterns of two cytoarchitectonic visual areas on the human posterior fusiform gyrus. Human Brain Mapping. doi:10.1002/hbm.22364.

Conturo, T. E., Williams, D. L., Smith, C. D., Gultepe, E., Akbudak, E., & Minshew, N. J. (2008). Neuronal fiber pathway abnormalities in autism: An initial MRI diffusion tensor tracking study of hippocampo-fusiform and amygdalo-fusiform pathways. Journal of International Neuropsychological Society, 14(6), 933–946.CrossRef

Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., et al. (2004). Early social attention impairments in autism: Social orienting, joint attention, and attention to distress. Developmental Psychology, 40(2), 271–283.PubMedCrossRef

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(3), 403–424.PubMedCrossRef

Eimer, M., & Holmes, A. (2002). An ERP study on the time course of emotional face processing. NeuroReport, 13(4), 427–431.PubMedCrossRef

Endo, T., Shioiri, T., Kitamura, H., Kimura, T., Endo, S., Masuzawa, N., et al. (2007). Altered chemical metabolites in the amygdala-hippocampus region contribute to autistic symptoms of autism spectrum disorders. Biological Psychiatry, 62(9), 1030–1037.PubMedCrossRef

Fang, F., Murray, S. O., Kersten, D., & He, S. (2005). Orientation-tuned FMRI adaptation in human visual cortex. Journal of Neurophysiology, 94(6), 4188–4195.PubMedCrossRef

Fischer, H., Wright, C. I., Whalen, P. J., McInerney, S. C., Shin, L. M., & Rauch, S. L. (2003). Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study. Brain Research Bulletin, 59(5), 387–392.PubMedCrossRef

Gabis, L., Wei, H., Azizian, A., DeVincent, C., Tudorica, A., Kesner-Baruch, Y., et al. (2008). 1H-magnetic resonance spectroscopy markers of cognitive and language ability in clinical subtypes of autism spectrum disorders. Journal of Child Neurology, 23(7), 766–774.PubMedCrossRef

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(3), 213–225.PubMedCrossRef

Grill-Spector, K., Henson, R., & Martin, A. (2006). Repetition and the brain: Neural models of stimulus-specific effects. Trends in Cognitive Science, 10(1), 14–23.CrossRef

Hanley, J. A., & McNeil, B. J. (1982). The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology, 143, 29–36.PubMedCrossRef

Harvey, D. Y., & Burgund, E. D. (2012). Neural adaptation across viewpoint and exemplar in fusiform cortex. Brain and Cognition, 80(1), 33–44. doi:10.1016/j.bandc.2012.04.009.PubMedCrossRef

Honeycutt, N. A., Smith, P. D., Aylward, E., Li, Q., Chan, M., Barta, P. E., et al. (1998). Mesial temporal lobe measurements on magnetic resonance imaging scans. Psychiatry Research, 83(2), 85–94.PubMedCrossRef

Ishai, A., Pessoa, L., Bikle, P. C., & Ungerleider, L. G. (2004). Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences of the United States of America, 101(26), 9827–9832.PubMedPubMedCentralCrossRef

Johnson, M. H. (2005). Subcortical face processing. Nature Reviews Neuroscience, 6(10), 766–774.PubMedCrossRef

Kenworthy, L., Yerys, B. E., Weinblatt, R., Abrams, D. N., & Wallace, G. L. (2013). Motor demands impact speed of information processing in autism spectrum disorders. Neuropsychology, 27(5), 529–536.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

Kleinhans, N. M., Richards, T., Johnson, L. C., Weaver, K. E., Greenson, J., Dawson, G., et al. (2011). fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage, 54(1), 697–704.PubMedPubMedCentralCrossRef

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(Pt 4), 1000–1012.PubMedCrossRef

Kleinhans, N. M., 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(12), 3665–3670.PubMedPubMedCentralCrossRef

Livingstone, M., & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science, 240(4853), 740–749.PubMedCrossRef

Lord, C., Risi, S., Lambrecht, L., Cook, E., Leventhal, B., DiLavore, P., 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(3), 205–223.PubMedCrossRef

Lord, C., Rutter, M., & Le Couteur, 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(5), 659–685.PubMedCrossRef

Merigan, W. H., & Maunsell, J. H. (1993). How parallel are the primate visual pathways? Annual Review of Neuroscience, 16, 369–402.PubMedCrossRef

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(6), 686–693.PubMedCrossRef

Murray, S. O., Olman, C. A., & Kersten, D. (2006). Spatially specific FMRI repetition effects in human visual cortex. Journal of Neurophysiology, 95(4), 2439–2445.PubMedCrossRef

Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., et al. (2006). Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Archives of General Psychiatry, 63(12), 1417–1428.PubMedCrossRef

Otsuka, H., Harada, M., Mori, K., Hisaoka, S., & Nishitani, H. (1999). Brain metabolites in the hippocampus-amygdala region and cerebellum in autism: An 1H-MR spectroscopy study. Neuroradiology, 41(7), 517–519.PubMedCrossRef

Page, L. A., Daly, E., Schmitz, N., Simmons, A., Toal, F., Deeley, Q., et al. (2006). In vivo 1H-magnetic resonance spectroscopy study of amygdala-hippocampal and parietal regions in autism. American Journal of Psychiatry, 163, 2189–2192.PubMedCrossRef

Pellicano, E., Jeffery, L., Burr, D., & Rhodes, G. (2007). Abnormal adaptive face-coding mechanisms in children with autism spectrum disorder. Current Biology, 17(17), 1508–1512.PubMedCrossRef

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(Pt 10), 2059–2073.PubMedCrossRef

Pourtois, G., Thut, G., Grave de Peralta, R., Michel, C., & Vuilleumier, P. (2005). Two electrophysiological stages of spatial orienting towards fearful faces: Early temporo-parietal activation preceding gain control in extrastriate visual cortex. Neuroimage, 26(1), 149–163.PubMedCrossRef

Prescott, S. A. (1998). Interactions between depression and facilitation within neural networks: Updating the dual-process theory of plasticity. Learning Memory, 5, 446–466.PubMedPubMedCentral

Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. Journal of Neuroscience, 26(29), 7674–7679.PubMedCrossRef

Schumann, C. M., Hamstra, J., Goodlin-Jones, B. L., Lotspeich, L. J., Kwon, H., Buonocore, M. H., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. Journal of Neuroscience, 24(28), 6392–6401.PubMedCrossRef

Simion, F., Leo, I., Turati, C., Valenza, E., & Dalla Barba, B. (2007). How face specialization emerges in the first months of life. Progress in Brain Research, 164, 169–185.PubMedCrossRef

Sparks, B. F., Friedman, S. D., Shaw, D. W., Aylward, E. H., Echelard, D., Artru, A. A., et al. (2002). Brain structural abnormalities in young children with autism spectrum disorder. Neurology, 59(2), 184–192.PubMedCrossRef

Streit, M., Dammers, J., Simsek-Kraues, S., Brinkmeyer, J., Wolwer, W., & Ioannides, A. (2003). Time course of regional brain activations during facial emotion recognition in humans. Neuroscience Letters, 342(1–2), 101–104.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

Thompson, R. F., & Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Review, 73(1), 16–43.PubMedCrossRef

Verbaten, M. N., Roelofs, J. W., van Engeland, H., Kenemans, J. K., & Slangen, J. L. (1991). Abnormal visual event-related potentials of autistic children. Journal of Autism and Developmental Disorders, 21(4), 449–470.PubMedCrossRef

Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nature Neuroscience, 6(6), 624–631.PubMedCrossRef

Webb, S. J., Jones, E. J., Merkle, K., Namkung, J., Toth, K., Greenson, J., et al. (2010). Toddlers with elevated autism symptoms show slowed habituation to faces. Child Neuropsychol, 16(3), 255–278.PubMedPubMedCentralCrossRef

Wiggins, J. L., Swartz, J. R., Martin, D. M., Lord, C., & Monk, C. S. (2014). Serotonin transporter genotype impacts amygdala habituation in youth with autism spectrum disorders. Social Cognitive and Affective Neuroscience, 9(6), 832–838. doi:10.1093/scan/nst039.PubMedPubMedCentralCrossRef

Wilson, F. A., & Rolls, E. T. (1993). The effects of stimulus novelty and familiarity on neuronal activity in the amygdala of monkeys performing recognition memory tasks. Experimental Brain Research, 93(3), 367–382.PubMedCrossRef

Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage, 14(6), 1370–1386.PubMedCrossRef

Titel: Altered Dynamics of the fMRI Response to Faces in Individuals with Autism
Auteurs: Natalia M. Kleinhans
Todd Richards
Jessica Greenson
Geraldine Dawson
Elizabeth Aylward
Publicatiedatum: 04-09-2015
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 1/2016
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-015-2565-8

Andere artikelen Uitgave 1/2016

Re-conceptualizing ASD Within a Dimensional Framework: Positive, Negative, and Cognitive Feature Clusters

Commentary

Parents’ Translations of Child Gesture Facilitate Word Learning in Children with Autism, Down Syndrome and Typical Development

Original Paper

Measuring Sensory Reactivity in Autism Spectrum Disorder: Application and Simplification of a Clinician-Administered Sensory Observation Scale

Original Paper

Preserved Proactive Interference in Autism Spectrum Disorder

Original Paper

Assessing Advanced Theory of Mind in Children and Adolescents with High-Functioning Autism: The Spanish Version of the Stories of Everyday Life

Original Paper

Additional Evidence is Needed to Recommend Acquiring a Dog to Families of Children with Autism Spectrum Disorder: A Response to Wright and Colleagues

Letter to the Editor