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Brief Report: Biological Sound Processing in Children with Autistic Spectrum Disorder

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Abstract

There is debate whether social impairments in autism spectrum disorder (ASD) are truly domain-specific, or if they reflect generalized deficits in lower-level cognitive processes. To solve this issue, we used auditory-evoked EEG responses to assess novelty detection (MMN component) and involuntary attentional orientation (P3 component) induced by socially-relevant, human-produced, biological sounds and acoustically-matched control stimuli in children with ASD and controls. Results show that early sensory and novelty processing of biological stimuli are preserved in ASD, but that automatic attentional orientation for biological sounds is markedly altered. These results support the notion that at least some cognitive processes of ASD are specifically altered when it comes to processing social stimuli.

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References

  • American Psychological Association (2013). Diagnostic and statistical manual of mental disorders (DSM-5 ® ) (5 ed.). Washington, DC: American Psychiatric Association.

    Book  Google Scholar 

  • Baum, S. H., Stevenson, R. A., & Wallace, M. T. (2015). Behavioral, perceptual, and neural alterations in sensory and multisensory function in autism spectrum disorder. Progress in Neurobiology, 134, 140–160. doi:10.1016/j.pneurobio.2015.09.007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Caron, K. G., Schaaf, R. C., Benevides, T. W., & Gal, E. (2012). Cross-cultural comparison of sensory behaviors in children with autism. American Journal of Occupational Therapy, 66(5), e77–e80.

    Article  PubMed  Google Scholar 

  • Ceponiene, R., Lepistö, T., Shestakova, A., Vanhala, R., Alku, P., Näätänen, R., & Yaguchi, K. (2003). Speech-sound-selective auditory impairment in children with autism: They can perceive but do not attend. Proceedings of the National Academy of Sciences, 100(9), 5567–5572. doi:10.1073/pnas.0835631100.

    Article  Google Scholar 

  • Chow, S. M. K. (2005). The suitability of the Sensory Profile for diagnosing sensory modulation dysfunctions in Chinese children. International Journal of Rehabilitation Research, 28, 153–158.

    Article  PubMed  Google Scholar 

  • Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998). Children with autism fail to orient to naturally occurring social stimuli. Journal of Autism and Developmental Disorders, 28(6), 479–485.

    Article  PubMed  Google Scholar 

  • Di Giorgio, E., Frasnelli, E., Rosa Salva, O., Maria Luisa, S., Puopolo, M., Tosoni, D., et al. (2016). Difference in visual social predispositions between newborns at low- and high-risk for autism. Scientific Reports, 6, 26395–26398. doi:10.1038/srep26395.

    Article  PubMed  PubMed Central  Google Scholar 

  • DiCriscio, A. S., Miller, S. J., Hanna, E. K., Kovac, M., Turner-Brown, L., Sasson, N. J., et al. (2016). Brief report: Cognitive control of social and nonsocial visual attention in autism. Journal of Autism and Developmental Disorders, 46, 2797–2805. doi:10.1007/s10803-016-2804-7.

    Article  PubMed  Google Scholar 

  • Donkers, F. C. L., Schipul, S. E., Baranek, G. T., Cleary, K. M., Willoughby, M. T., Evans, A. M., et al. (2013). Attenuated auditory event-related potentials and associations with atypical sensory response patterns in children with autism. Journal of Autism and Developmental Disorders, 45(2), 506–523. doi:10.1007/s10803-013-1948-y.

    Article  Google Scholar 

  • Fan, Y.-T., & Cheng, Y. (2014). Atypical mismatch negativity in response to emotional voices in people with autism spectrum conditions. PLoS ONE, 9(7), e102471–e102410. doi:10.1371/journal.pone.0102471.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fischer, J., Koldewyn, K., Jiang, Y. V., & Kanwisher, N. (2014). Unimpaired attentional disengagement and social orienting in children with autism. Clinical Psychological Science, 2(2), 214–223. doi:10.1177/2167702613496242.

    Article  PubMed  PubMed Central  Google Scholar 

  • Friedman, D., Cycowicz, Y. M., & Gaeta, H. (2001). The novelty P3: An event-related brain potential (ERP) sign of the brain’s evaluation of novelty. Neuroscience and Biobehavioral Reviews, 25(4), 355–373. doi:10.1016/S0149-7634(01)00019-7.

    Article  PubMed  Google Scholar 

  • Garrido, M. I., Kilner, J. M., Stephan, K. E., & Friston, K. J. (2009). The mismatch negativity: A review of underlying mechanisms. Clinical Neurophysiology, 120(3), 453–463. doi:10.1016/j.clinph.2008.11.029.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guillon, Q., Rogé, B., Afzali, M. H., Baduel, S., Kruck, J., & Hadjikhani, N. (2016). Intact perception but abnormal orientation towards face-like objects in young children with ASD. Scientific Reports, 6, 22119. doi:10.1038/srep22119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guthrie, D., & Buchwald, J. S. (1991). Significance testing of difference potentials. Psychophysiology, 28(2), 240–244. doi:10.1111/j.1469-8986.1991.tb00417.x.

    Article  PubMed  Google Scholar 

  • Hauk, O., Shtyrov, Y., & Pulvermüller, F. (2006). The sound of actions as reflected by mismatch negativity: Rapid activation of cortical sensory–motor networks by sounds associated with finger and tongue movements. European Journal of Neuroscience, 23(3), 811–821. doi:10.1111/j.1460-9568.2006.04586.x.

    Article  PubMed  Google Scholar 

  • Hay, R. A., Roach, B. J., Srihari, V. H., Woods, S. W., Ford, J. M., & Mathalon, D. H. (2015). Equivalent mismatch negativity deficits across deviant types in early illness schizophrenia-spectrum patients. Biological Psychology, 105, 130–137. doi:10.1016/j.biopsycho.2015.01.004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Javitt, D. C., & Sweet, R. A. (2015). Auditory dysfunction in schizophrenia: Integrating clinical and basic features. Nature Reviews Neuroscience, 16(9), 535–550. doi:10.1038/nrn4002.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature, 504, 427–431. doi:10.1038/nature12715.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karhson, D. S., & Golob, E. J. (2016). Atypical sensory reactivity influences auditory attentional control in adults with autism spectrum disorders. Autism Research, 9, 1079–1092. doi:10.1002/aur.1593.

    Article  PubMed  Google Scholar 

  • Klin, A., Lin, D. J., Gorrindo, P., Ramsay, G., & Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459(7244), 257–261. doi:10.1038/nature07868.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kujala, T., Lepistö, T., & Näätänen, R. (2013). The neural basis of aberrant speech and audition in autism spectrum disorders. Neuroscience and Biobehavioral Reviews, 37(4), 697–704. doi:10.1016/j.neubiorev.2013.01.006.

    Article  PubMed  Google Scholar 

  • Leekam, S. (2015). Social cognitive impairment and autism: What are we trying to explain? Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1686), 20150082–20150088. doi:10.1098/rstb.2015.0082.

    Article  Google Scholar 

  • Lepistö, T., Kajander, M., Vanhala, R., Alku, P., Huotilainen, M., Näätänen, R., & Kujala, T. (2008). The perception of invariant speech features in children with autism. Biological Psychology, 77(1), 25–31. doi:10.1016/j.biopsycho.2007.08.010.

    Article  PubMed  Google Scholar 

  • Lepistö, T., Silokallio, S., Nieminen-von Wendt, T., Alku, P., Näätänen, R., & Kujala, T. (2006). Auditory perception and attention as reflected by the brain event-related potentials in children with Asperger syndrome. Clinical Neurophysiology, 117(10), 2161–2171. doi:10.1016/j.clinph.2006.06.709.

    Article  PubMed  Google Scholar 

  • Lohvansuu, K., Hämäläinen, J. A., Tanskanen, A., Bartling, J., Bruder, J., Honbolygó, F., et al. (2013). Separating mismatch negativity (MMN) response from auditory obligatory brain responses in school-aged children. Psychophysiology, 50(7), 640–652. doi:10.1111/psyp.12048.

    Article  PubMed  Google Scholar 

  • Näätänen, R., Pakarinen, S., Rinne, T., & Takegata, R. (2004). The mismatch negativity (MMN): Towards the optimal paradigm. Clinical Neurophysiology, 115(1), 140–144. doi:10.1016/j.clinph.2003.04.001.

    Article  PubMed  Google Scholar 

  • Orekhova, E. V., & Stroganova, T. A. (2014). Arousal and attention re-orienting in autism spectrum disorders: Evidence from auditory event-related potentials. Frontiers in Human Neuroscience 8, 34. doi:10.3389/fnhum.2014.00034/abstract.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pelphrey, K. A., Shultz, S., Hudac, C. M., & Vander Wyk, B. C. (2011). Research review: Constraining heterogeneity: The social brain and its development in autism spectrum disorder. Journal of Child Psychology and Psychiatry, 52(6), 631–644. doi:10.1111/j.1469-7610.2010.02349.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ponton, C. W., Eggermont, J. J., Don, M., Waring, M. D., Kwong, B., Cunningham, J., & Trautwein, P. (2000). Maturation of the mismatch negativity: Effects of profound deafness and cochlear implant use. Audiology & Neuro-otology, 5(3–4), 167–185.

    Article  Google Scholar 

  • Shah, P., Gaule, A., Bird, G., & Cook, R. (2013). Robust orienting to protofacial stimuli in autism. Current Biology, 23(24), R1087–R1088. doi:10.1016/j.cub.2013.10.034.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sinclair, D., Oranje, B., Razak, K. A., Siegel, S. J., & Schmid, S. (2016). Sensory processing in autism spectrum disorders and Fragile X syndrome—From the clinic to animal models. Neuroscience and Biobehavioral Reviews. doi:10.1016/j.neubiorev.2016.05.029.

    PubMed  Google Scholar 

  • Wass, S. V., Jones, E. J. H., Gliga, T., Smith, T. J., Charman, T., Johnson, M. H., et al. (2015). Shorter spontaneous fixation durations in infants with later emerging autism. Scientific Reports, 5, 8284–8288. doi:10.1038/srep08284.

    Article  PubMed  PubMed Central  Google Scholar 

  • Whitehouse, A. J. O., & Bishop, D. V. M. (2008). Do children with autism “switch off” to speech sounds? An investigation using event-related potentials. Developmental Science, 11(4), 516–524. doi:10.1111/j.1467-7687.2008.00697.x.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants the Fonds de la Recherche du Québec- Santé (FRQS). ML was supported by a Canada Graduate Scholarship Doctoral Award from CIHR. JL is supported by a Junior 1 Salary Award from the FRQS.

Author Contributions

ML conceived of the study, acquired the data, performed the statistical analysis, and drafted the manuscript. LPB contributed to data processing, statistical analysis and helped to draft of the manuscript. DC participated in the design of the study and recruited participants. DS, HT and JL conceived of the study, supervised data processing, statistical analysis, and drafted the manuscript.

Funding

This study was funded by the Fonds de la Recherche du Québec-Santé (#34604).

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Correspondence to Jean-François Lepage.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in the study or their legal tutor in the case of children.

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Lortie, M., Proulx-Bégin, L., Saint-Amour, D. et al. Brief Report: Biological Sound Processing in Children with Autistic Spectrum Disorder. J Autism Dev Disord 47, 1904–1909 (2017). https://doi.org/10.1007/s10803-017-3093-5

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