Abstract
Individuals with autism spectrum disorders (ASD) exhibit alterations in sensory processing, including changes in the integration of information across the different sensory modalities. In the current study, we used the sound-induced flash illusion to assess multisensory integration in children with ASD and typically-developing (TD) controls. Thirty-one children with ASD and 31 age and IQ matched TD children (average age = 12 years) were presented with simple visual (i.e., flash) and auditory (i.e., beep) stimuli of varying number. In illusory conditions, a single flash was presented with 2–4 beeps. In TD children, these conditions generally result in the perception of multiple flashes, implying a perceptual fusion across vision and audition. In the present study, children with ASD were significantly less likely to perceive the illusion relative to TD controls, suggesting that multisensory integration and cross-modal binding may be weaker in some children with ASD. These results are discussed in the context of previous findings for multisensory integration in ASD and future directions for research.
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Altieri, N., Stevenson, R. A., Wallace, M. T., & Wenger, M. J. (2013). Learning to associate auditory and visual stimuli: Behavioral and neural mechanisms. Brain Topography. doi:10.1007/s10548-013-0333-7.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders-IV-TR. Washington, DC: APA.
American Psychiatric Association, & American Psychiatric Association DSM-5 Task Force. (2013). Diagnostic and statistical manual of mental disorders: DSM-5 (5th ed.). Arlington, VA: American Psychiatric Association.
Bebko, J. M., Weiss, J. A., Demark, J. L., & Gomez, P. (2006). Discrimination of temporal synchrony in intermodal events by children with autism and children with developmental disabilities without autism. Journal of Child Psychology and Psychiatry, 47(1), 88–98. doi:10.1111/j.1469-7610.2005.01443.x.
Bertone, A., Mottron, L., Jelenic, P., & Faubert, J. (2005). Enhanced and diminished visuo-spatial information processing in autism depends on stimulus complexity. Brain, 128(Pt 10), 2430–2441. doi:10.1093/brain/awh561.
Bonnel, A., Mottron, L., Peretz, I., Trudel, M., Gallun, E., & Bonnel, A. M. (2003). Enhanced pitch sensitivity in individuals with autism: A signal detection analysis. Journal of Cognitive Neuroscience, 15(2), 226–235. doi:10.1162/089892903321208169.
Brock, J., Brown, C. C., Boucher, J., & Rippon, G. (2002). The temporal binding deficit hypothesis of autism. Development and Psychopathology, 14(2), 209–224.
Calvert, G. A., & Thesen, T. (2004). Multisensory integration: Methodological approaches and emerging principles in the human brain. Journal of Physiology—Paris, 98(1–3), 191–205.
Conrey, B., & Pisoni, D. B. (2006). Auditory-visual speech perception and synchrony detection for speech and nonspeech signals. Journal of the Acoustical Society of America, 119(6), 4065–4073.
de Boer-Schellekens, L., Eussen, M., & Vroomen, J. (2013). Diminished sensitivity of audiovisual temporal order in autism spectrum disorder. Frontiers in Integrative Neuroscience, 7, 8. doi:10.3389/fnint.2013.00008.
de Gelder, B., Vroomen, J., & Van der Heide, L. (1991). Face recognition and lip-reading in autism. European Journal of Cognitive Psychology, 3(1), 69–86.
Dixon, N. F., & Spitz, L. (1980). The detection of auditory visual desynchrony. Perception, 9(6), 719–721.
Foss-Feig, J. H., Kwakye, L. D., Cascio, C. J., Burnette, C. P., Kadivar, H., Stone, W. L., et al. (2010). An extended multisensory temporal binding window in autism spectrum disorders. Experimental Brain Research, 203(2), 381–389. doi:10.1007/s00221-010-2240-4.
Foxe, J. J., Molholm, S., Del Bene, V. A., Frey, H. P., Russo, N. N., Blanco, D., et al. (2013). Severe multisensory speech integration deficits in high-functioning school-aged children with autism spectrum disorder (ASD) and their resolution during early adolescence. Cerebral Cortex. doi:10.1093/cercor/bht213.
Gregory, R. L. (1980). Perceptions as hypotheses. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 290, 181–197.
Happé, F., & Frith, U. (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5–25. doi:10.1007/s10803-005-0039-0.
Hillock, A. R., Powers, A. R., & Wallace, M. T. (2011). Binding of sights and sounds: Age-related changes in multisensory temporal processing. Neuropsychologia, 49(3), 461–467. doi:10.1016/j.neuropsychologia.2010.11.041.
Hillock-Dunn, A., & Wallace, M. T. (2012). Developmental changes in the multisensory temporal binding window persist into adolescence. Developmental Science, 15(5), 688–696. doi:10.1111/j.1467-7687.2012.01171.x.
Iarocci, G., & McDonald, J. (2006). Sensory integration and the perceptual experience of persons with autism. Journal of Autism and Developmental Disorders, 36(1), 77–90. doi:10.1007/s10803-005-0044-3.
Iarocci, G., Rombough, A., Yager, J., Weeks, D. J., & Chua, R. (2010). Visual influences on speech perception in children with autism. Autism, 14(4), 305–320. doi:10.1177/1362361309353615.
Irwin, J. R., Tornatore, L. A., Brancazio, L., & Whalen, D. H. (2011). Can children with autism spectrum disorders “hear” a speaking face? Child Development, 82(5), 1397–1403. doi:10.1111/j.1467-8624.2011.01619.x.
Joseph, R. M., Keehn, B., Connolly, C., Wolfe, J. M., & Horowitz, T. S. (2009). Why is visual search superior in autism spectrum disorder? Developmental Science, 12(6), 1083–1096.
Keane, B. P., Rosenthal, O., Chun, N. H., & Shams, L. (2010). Audiovisual integration in high functioning adults with autism. Research in Autism Spectrum Disorders, 4(2), 276–289.
Kuhl, P., Coffey-Corina, S., Padden, D., & Dawson, G. (2005). Links between social and linguistic processing of speech in preschool children with autism: Behavioral and electrophysiological measures. Developmental Science, 8(1), F1–F12.
Kwakye, L. D., Foss-Feig, J. H., Cascio, C. J., Stone, W. L., & Wallace, M. T. (2011). Altered auditory and multisensory temporal processing in autism spectrum disorders. Frontiers in Integrative Neuroscience, 4, 129. doi:10.3389/fnint.2010.00129.
Lewkowicz, D. J. (2000). The development of intersensory temporal perception: An epigenetic systems/limitations view. Psychological Bulletin, 126(2), 281–308.
Lewkowicz, D. J. (2010). Infant perception of audio–visual speech synchrony. Developmental Psychology, 46(1), 66–77. doi:10.1037/a0015579.
Lewkowicz, D. J. (2012). Development of multisensory temporal perception. In M. M. Murray & M. T. Wallace (Eds.), The neural bases of multisensory processes. Boca Raton, FL: CRC Press.
Lewkowicz, D. J., & Flom, R. (2014). The audiovisual temporal binding window narrows in early childhood. Child Development, 85(2), 685–694. doi:10.1111/cdev.12142.
Lord, C., Risi, S., Lambrecht, L., Cook, E. H, Jr, Leventhal, B. L., DiLavore, P. C., 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.
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.
McGurk, H., & MacDonald, J. (1976). Hearing lips and seeing voices. Nature, 264(5588), 746–748.
Minshew, N. J., & Hobson, J. A. (2008). Sensory sensitivities and performance on sensory perceptual tasks in high-functioning individuals with autism. Journal of Autism and Developmental Disorders, 38(8), 1485–1498. doi:10.1007/s10803-007-0528-4.
Mongillo, E., Irwin, J., Whalen, D., Klaiman, C., Carter, A., & Schultz, R. (2008). Audiovisual processing in children with and without autism spectrum disorders. Journal of Autism and Developmental Disorders, 38(7), 1349–1358. doi:10.1007/s10803-007-0521-y.
Neil, P. A., Chee-Ruiter, C., Scheier, C., Lewkowicz, D. J., & Shimojo, S. (2006). Development of multisensory spatial integration and perception in humans. Developmental Science, 9(5), 454–464. doi:10.1111/j.1467-7687.2006.00512.x.
O’Riordan, M. A. (2004). Superior visual search in adults with autism. Autism, 8(3), 229–248. doi:10.1177/1362361304045219.
O’Riordan, M., & Passetti, F. (2006). Discrimination in autism within different sensory modalities. Journal of Autism and Developmental Disorders, 36(5), 665–675. doi:10.1007/s10803-006-0106-1.
O’Riordan, M., & Plaisted, K. (2001). Enhanced discrimination in autism. Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology, 54(4), 961–979.
O’Riordan, M. A., Plaisted, K. C., Driver, J., & Baron-Cohen, S. (2001). Superior visual search in autism. Journal of Experimental Psychology: Human Perception and Performance, 27(3), 719–730.
Pellicano, E., & Burr, D. (2012). When the world becomes ‘too real’: A Bayesian explanation of autistic perception. Trends in Cognitive Sciences, 16(10), 504–510.
Plaisted, K., O’Riordan, M., & Baron-Cohen, S. (1998a). Enhanced discrimination of novel, highly similar stimuli by adults with autism during a perceptual learning task. Journal of Child Psychology and Psychiatry, 39(5), 765–775.
Plaisted, K., O’Riordan, M., & Baron-Cohen, S. (1998b). Enhanced visual search for a conjunctive target in autism: A research note. Journal of Child Psychology and Psychiatry, 39(5), 777–783.
Ross, L. A., Molholm, S., Blanco, D., Gomez-Ramirez, M., Saint-Amour, D., & Foxe, J. J. (2011). The development of multisensory speech perception continues into the late childhood years. European Journal of Neuroscience, 33(12), 2329–2337. doi:10.1111/j.1460-9568.2011.07685.x.
Shams, L., Kamitani, Y., & Shimojo, S. (2000). Illusions. What you see is what you hear. Nature, 408(6814), 788.
Stevenson, R. A., Altieri, N. A., Kim, S., Pisoni, D. B., & James, T. W. (2010). Neural processing of asynchronous audiovisual speech perception. Neuroimage, 49(4), 3308–3318. doi:10.1016/j.neuroimage.2009.12.001.
Stevenson, R. A., Fister, J. K., Barnett, Z. P., Nidiffer, A. R., & Wallace, M. T. (2012a). Interactions between the spatial and temporal stimulus factors that influence multisensory integration in human performance. Experimental Brain Research. doi:10.1007/s00221-012-3072-1.
Stevenson, R. A., Magali, S., Susanne, F., Morgan, D. B., & Mark, T. W. (2014a). The impact of multisensory integration deficits on speech perception in children with autism spectrum disorders. Frontiers in Psychology, 5, 379.
Stevenson, R. A., Siemann, J. K., Schneider, B. C., Eberly, H. E., Woynaroski, T. G., Camarata, S. M., et al. (2014b). Multisensory temporal integration in autism spectrum disorders. The Journal of Neuroscience, 34(3), 691–697. doi:10.1523/jneurosci.3615-13.2014.
Stevenson, R. A., Siemann, J. K., Woynaroski, T. G., Schneider, B. C., Eberly, H. E., Camarata, S. M., et al. (2014c). Brief report: Arrested development of audiovisual speech perception in autism spectrum disorders. Journal of Autism and Developmental Disorders, 44(6), 1470–1477.
Stevenson, R. A., VanDerKlok, R. M., Pisoni, D. B., & James, T. W. (2011). Discrete neural substrates underlie complementary audiovisual speech integration processes. Neuroimage, 55(3), 1339–1345. doi:10.1016/j.neuroimage.2010.12.063.
Stevenson, R. A., & Wallace, M. T. (2013). Multisensory temporal integration: Task and stimulus dependencies. Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale, 227(2), 249–261. doi:10.1007/s00221-013-3507-3.
Stevenson, R. A., Zemtsov, R. K., & Wallace, M. T. (2012b). Individual differences in the multisensory temporal binding window predict susceptibility to audiovisual illusions. Journal of Experimental Psychology: Human Perception and Performance. doi:10.1037/a0027339.
Taylor, N., Isaac, C., & Milne, E. (2010). A comparison of the development of audiovisual integration in children with autism spectrum disorders and typically developing children. Journal of Autism and Developmental Disorders, 40(11), 1403–1411. doi:10.1007/s10803-010-1000-4.
van der Smagt, M. J., van Engeland, H., & Kemner, C. (2007). Brief report: Can you see what is not there? low-level auditory-visual integration in autism spectrum disorder. Journal of Autism and Developmental Disorders, 37(10), 2014–2019. doi:10.1007/s10803-006-0346-0.
van Wassenhove, V., Grant, K. W., & Poeppel, D. (2007). Temporal window of integration in auditory-visual speech perception. Neuropsychologia, 45(3), 598–607. doi:10.1016/j.neuropsychologia.2006.01.001.
Vatakis, A., & Spence, C. (2006). Audiovisual synchrony perception for music, speech, and object actions. Brain Research, 1111(1), 134–142. doi:10.1016/j.brainres.2006.05.078.
von Helmholtz, H. (2005). Treatise on physiological optics (Vol. 3). Courier: Dover Publications.
Vroomen, J., & Keetels, M. (2010). Perception of intersensory synchrony: A tutorial review. Attention, Perception, & Psychophysics, 72(4), 871–884. doi:10.3758/APP.72.4.871.
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence. San Antonio: Harcourt Brace.
Williams, J., Massaro, D. W., Peel, N. J., Bosseler, A., & Suddendorf, T. (2004). Visual-auditory integration during speech imitation in autism. Research in Developmental Disabilities, 25(6), 559–575. doi:10.1016/j.ridd.2004.01.008.
Woynaroski, T. G., Kwakye, L. D., Foss-Feig, J. H., Stevenson, R. A., Stone, W. L., & Wallace, M. T. (2013). Multisensory speech perception in children with autism spectrum disorders. Journal of Autism and Developmental Disorders. doi:10.1007/s10803-013-1836-5.
Acknowledgments
Funding for this work was provided by a Banting Postdoctoral Fellowship, National Institutes of Health Grant F32 DC011993, Multisensory Integration and Temporal Processing in ASD, a Grant from the Vanderbilt Institute for Clinical and Translational Research, VICTR VR5807.1, Development and Modulation of Multisensory Integration, National Institutes of Health Grant R34 DC010927, Evaluation of Sensory Integration Treatment in ASD, a Vanderbilt Kennedy Center MARI/Hobbs Award, the Vanderbilt Brain Institute, and the Vanderbilt University Kennedy Center. We also acknowledge the help of Walter Lee and Zachary Barnett for technical assistance, and Magali Segers for clinical input.
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Stevenson, R.A., Siemann, J.K., Woynaroski, T.G. et al. Evidence for Diminished Multisensory Integration in Autism Spectrum Disorders. J Autism Dev Disord 44, 3161–3167 (2014). https://doi.org/10.1007/s10803-014-2179-6
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DOI: https://doi.org/10.1007/s10803-014-2179-6