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Everything has Its Time: Narrow Temporal Windows are Associated with High Levels of Autistic Traits Via Weaknesses in Multisensory Integration

  • Sayaka KawakamiEmail author
  • Shota Uono
  • Sadao Otsuka
  • Shuo Zhao
  • Motomi Toichi
Original Paper

Abstract

The present study examined whether fundamental sensory functions such as temporal processing and multisensory integration are related to autistic traits in the general population. Both a narrower temporal window (TW) for simultaneous perception, as measured by a temporal order judgement task, and a reduced ability to engage in multisensory integration during the sound-induced flash illusion task were related to higher levels of autistic traits. Additionally, a narrow TW is associated with high levels of autistic traits due to a deficiency in multisensory integration. Taken together, these findings suggest that alterations in fundamental functions produce a cascading effect on higher-order social and cognitive functions, such as those experienced by people with autism spectrum disorder.

Keywords

Autism spectrum disorder (ASD) Temporal processing Multisensory integration Social cognition 

Notes

Acknowledgments

We thank Emi Yokoyama for her technical support. This study was supported by the Organization for Promoting Neurodevelopmental Disorder Research (OPNDR), and Grant-in-Aid for Young Scientists (B) (16K17360), Japan Society for the Promotion of Sciences.

Author Contributions

SK, SU, SO, SZ, and MT conceived and designed the experiments. SK performed the experiments. SK, SU, and SO analysed the data. SK wrote the first draft of the manuscript, and SU substantially revised the manuscript. All authors contributed to the writing of the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in the present study were in accordance with the ethical standards of the Ethics Committee of the Graduate School and Faculty of Medicine at Kyoto University and with the 1964 Declaration of Helsinki and its later amendments.

Informed Consent

All individual participants included in the present study provided written informed consent.

References

  1. American Psychiatric Association. (2013). Diagnostic and Statistical manual of mental disorders (5th edition (DSM 5)). Arlington: American Psychiatric Publishing.CrossRefGoogle Scholar
  2. Balz, J., Keil, J., Romero, Y. R., Mekle, R., Schubert, F., Aydin, S., et al. (2016). GABA concentration in superior temporal sulcus predicts gamma power and perception in the sound-induced flash illusion. Neuroimage, 125, 724–730.CrossRefGoogle Scholar
  3. Baron, R. M., & Kenny, D. A. (1986). The moderator mediator variable distinction in social psychological-research-conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology, 51(6), 1173–1182.CrossRefGoogle Scholar
  4. Baron-Cohen, S., Leslie, A. M., & Frith, U. (1985). Does the autistic-child have a theory of mind? Cognition, 21(1), 37–46.CrossRefGoogle Scholar
  5. Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001). The Autism-Spectrum Quotient (AQ): Evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31(1), 5–17.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. Ben-Artzi, E., Fostick, L., & Babkoff, H. (2005). Deficits in temporal-order judgments in dyslexia: evidence from diotic stimuli differing spectrally and from dichotic stimuli differing only by perceived location. Neuropsychologia, 43(5), 714–723.CrossRefGoogle Scholar
  8. Binder, M. (2015). Neural correlates of audiovisual temporal processing—Comparison of temporal order and simultaneity judgments. Neuroscience, 300, 432–447.CrossRefGoogle Scholar
  9. Campanella, S., & Belin, P. (2007). Integrating face and voice in person perception. Trends in Cognitive Sciences, 11(12), 535–543.CrossRefGoogle Scholar
  10. Chan, J. S., Langer, A., & Kaiser, J. (2016). Temporal integration of multisensory stimuli in autism spectrum disorder: A predictive coding perspective. Journal of Neural Transmission, 123(8), 917–923.CrossRefGoogle Scholar
  11. Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012). The social motivation theory of autism. Trends in Cognitive Sciences, 16(4), 231–239.CrossRefGoogle Scholar
  12. Constantino, J. N., & Todd, R. D. (2003). Autistic traits in the general population: A twin study. Archives of General Psychiatry, 60(5), 524–530.CrossRefGoogle Scholar
  13. Crane, L., Goddard, L., & Pring, L. (2009). Sensory processing in adults with autism spectrum disorders. Autism, 13(3), 215–228.CrossRefGoogle Scholar
  14. Dairoku, K., Yamanaka, K., Fujita, K., & Maekawa, H. (2009). Short forms of Japanese WAIS-III for estimating FSIQ. Paper presented at the meeting of the Japanese Psychological Association, Kyoto, Japan. Abstract retrieved from https://www.psych.or.jp/meeting/proceedings/73/contents/poster/detail/3pm056.html.
  15. 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.CrossRefGoogle Scholar
  16. de Gelder, B., & Vroomen, J. (2000). The perception of emotions by ear and by eye. Cognition & Emotion, 14(3), 289–311.CrossRefGoogle Scholar
  17. de Haas, B., Kanai, R., Jalkanen, L., & Rees, G. (2012). Grey matter volume in early human visual cortex predicts proneness to the sound-induced flash illusion. Proceedings of the Royal Society B: Biological Sciences, 279(1749), 4955–4961.Google Scholar
  18. Deruelle, C., Rondan, C., Gepner, B., & Tardif, C. (2004). Spatial frequency and face processing in children with autism and Asperger syndrome. Journal of Autism and Developmental Disorders, 34(2), 199–210.CrossRefGoogle Scholar
  19. Donohue, S. E., Woldorff, M. G., & Mitroff, S. R. (2010). Video game players show more precise multisensory temporal processing abilities. Attention Perception & Psychophysics, 72(4), 1120–1129.CrossRefGoogle Scholar
  20. Elsabbagh, M., & Johnson, M. H. (2016). Autism and the social brain: The first-year puzzle. Biological Psychiatry, 80(2), 94–99.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Fujita, K., Maekawa, H., Dairoku, H., & Yamanaka, K. (2006). Japanese version of the Wechsler Adult Intelligence Scale (3rd edition (WAIS-III)). Tokyo: Nihon Bunka Kagakusha. (in Japanese).Google Scholar
  23. Golan, O., Baron-Cohen, S., Hill, J. J., & Golan, Y. (2006). The “reading the mind in films” task: Complex emotion recognition in adults with and without autism spectrum conditions. Social Neuroscience, 1(2), 111–123.CrossRefGoogle Scholar
  24. Günay, C., & Maida, A. S. (2006). Using temporal binding for hierarchical recruitment of conjunctive concepts over delayed lines. Neurocomputing, 69(4–6), 317–367.CrossRefGoogle Scholar
  25. Haß, K., Sinke, C., Reese, T., Roy, M., Wiswede, D., Dillo, W., et al. (2016). Enlarged temporal integration window in schizophrenia indicated by the double-flash illusion. Cognitive Neuropsychiatry, 22(2), 145–158.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. Harms, M. B., Martin, A., & Wallace, G. L. (2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychology Review, 20(3), 290–322.CrossRefGoogle Scholar
  28. Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York, NY: The Guilford Press.Google Scholar
  29. Jaśkowski, P., Jaroszyk, F., & Hojanjezierska, D. (1990). Temporal-order judgments and reaction-time for stimuli of different modalities. Psychological Research-Psychologische Forschung, 52(1), 35–38.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Magiati, I., Tay, X. W., & Howlin, P. (2014). Cognitive, language, social and behavioural outcomes in adults with autism spectrum disorders: A systematic review of longitudinal follow-up studies in adulthood. Clinical Psychology Review, 34(1), 73–86.CrossRefGoogle Scholar
  32. Mishra, J., Martinez, A., Sejnowski, T. J., & Hillyard, S. A. (2007). Early cross-modal interactions in auditory and visual cortex underlie a sound-induced visual illusion. Journal of Neuroscience, 27(15), 4120–4131.CrossRefGoogle Scholar
  33. Nakano, T., Ota, H., Kato, N., & Kitazawa, S. (2010). Deficit in visual temporal integration in autism spectrum disorders. Proceedings of the Royal Society B: Biological Sciences, 277(1684), 1027–1030.CrossRefGoogle Scholar
  34. Noel, J. P., De Niear, M., Van der Burg, E., & Wallace, M. T. (2016). Audiovisual simultaneity judgment and rapid recalibration throughout the lifespan. PLoS ONE, 11(8), e0161698.CrossRefGoogle Scholar
  35. O’Connor, K. (2007). Brief report: Impaired identification of discrepancies between expressive faces and voices in adults with Asperger’s syndrome. Journal of Autism and Developmental Disorders, 37(10), 2008–2013.CrossRefGoogle Scholar
  36. Otsuka, S., Uono, S., Yoshimura, S., Zhao, S., & Toichi, M. (2017). Emotion perception mediates the predictive relationship between verbal ability and functional outcome in high-functioning adults with autism spectrum disorder. Journal of Autism and Developmental Disorders, 47(4), 1166–1182.CrossRefGoogle Scholar
  37. Preacher, K. J., & Hayes, A. F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods Instruments & Computers, 36(4), 717–731.CrossRefGoogle Scholar
  38. Preacher, K. J., & Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40(3), 879–891.CrossRefGoogle Scholar
  39. Ross, L. A., Saint-Amour, D., Leavitt, V. M., Javitt, D. C., & Foxe, J. J. (2007). Do you see what I am saying? Exploring visual enhancement of speech comprehension in noisy environments. Cerebral Cortex, 17(5), 1147–1153.CrossRefGoogle Scholar
  40. Sasson, N. J., Pinkham, A. E., Carpenter, K. L. H., & Belger, A. (2011). The benefit of directly comparing autism and schizophrenia for revealing mechanisms of social cognitive impairment. Journal of Neurodevelopmental Disorders, 3(2), 87–100.CrossRefGoogle Scholar
  41. Schür, R. R., Draisma, L. W. R., Wijnen, J. P., Boks, M. P., Koevoets, M., Joels, M., et al. (2016). Brain GABA Levels across psychiatric disorders: A systematic literature review and meta-analysis of H-1-MRS studies. Human Brain Mapping, 37(9), 3337–3352.CrossRefGoogle Scholar
  42. Setti, A., Stapleton, J., Leahy, D., Walsh, C., Kenny, R. A., & Newell, F. N. (2014). Improving the efficiency of multisensory integration in older adults: Audio-visual temporal discrimination training reduces susceptibility to the sound-induced flash illusion. Neuropsychologia, 61, 259–268.CrossRefGoogle Scholar
  43. Shah, A., & Frith, U. (1993). Why do autistic individuals show superior performance on the block design task? Journal of Child Psychology and Psychiatry, 34(8), 1351–1364.CrossRefGoogle Scholar
  44. Shams, L., Kamitani, Y., & Shimojo, S. (2000). Illusions - What you see is what you hear. Nature, 408(6814), 788–788.CrossRefGoogle Scholar
  45. Smith, E. G., & Bennetto, L. (2007). Audiovisual speech integration and lipreading in autism. Journal of Child Psychology and Psychiatry, 48(8), 813–821.CrossRefGoogle Scholar
  46. Stevenson, R. A., Park, S., Cochran, C., McIntosh, L. G., Noel, J. P., Barense, M. D., et al. (2017). The associations between multisensory temporal processing and symptoms of schizophrenia. Schizophrenia Research, 179, 97–103.CrossRefGoogle Scholar
  47. Stevenson, R. A., Siemann, J. K., Woynaroski, T. G., Schneider, B. C., Eberly, H. E., Camarata, S. M., et al. (2014). Evidence for diminished multisensory integration in autism spectrum disorders. Journal of Autism and Developmental Disorders, 44(12), 3161–3167.CrossRefGoogle Scholar
  48. Stevenson, R. A., Wilson, M. M., Powers, A. R., & Wallace, M. T. (2013). The effects of visual training on multisensory temporal processing. Experimental Brain Research, 225(4), 479–489.CrossRefGoogle Scholar
  49. Stevenson, R. A., Zemtsov, R. K., & Wallace, M. T. (2012). Individual differences in the multisensory temporal binding window predict susceptibility to audiovisual illusions. Journal of Experimental Psychology: Human Perception and Performance, 38(6), 1517–1529.PubMedGoogle Scholar
  50. Turi, M., Karaminis, T., Pellicano, E., & Burr, D. (2016). No rapid audiovisual recalibration in adults on the autism spectrum. Scientific Reports, 6, 21756.CrossRefGoogle Scholar
  51. van Boxtel, J. J. A., & Lu, H. J. (2013). A predictive coding perspective on autism spectrum disorders. Frontiers in Psychology, 4, 19.PubMedPubMedCentralGoogle Scholar
  52. Van de Cruys, S., Evers, K., Van der Hallen, R., Van Eylen, L., Boets, B., de-Wit, L., et al. (2014). Precise minds in uncertain worlds: Predictive coding in autism. Psychological Review, 121(4), 649–675.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. van Vugt, F. T., & Tillmann, B. (2014). Thresholds of auditory-motor coupling measured with a simple task in musicians and non-musicians: Was the sound simultaneous to the key press? PLoS One, 9(2), e87176.CrossRefGoogle Scholar
  55. Vanes, L. D., White, T. P., Wigton, R. L., Joyce, D., Collier, T., & Shergill, S. S. (2016). Reduced susceptibility to the sound-induced flash fusion illusion in schizophrenia. Psychiatry Research, 245, 58–65.CrossRefGoogle Scholar
  56. Wakabayashi, A., Tojo, Y., Baron-Cohen, S., & Wheelwright, S. (2004). The autism-spectrum quotient (AQ) Japanese version: Evidence from high-functioning clinical group and normal adults. Shinrigaku Kenkyu, 75(1), 78–84. (in Japanese).CrossRefGoogle Scholar
  57. Wechsler, D. (1997). Wechsler Adult Intelligence Scale-third edition (WAIS-III). San Antonio: The Psychological Corporation.Google Scholar
  58. Zmigrod, L., & Zmigrod, S. (2016). On the temporal precision of thought: Individual differences in the multisensory temporal binding window predict performance on verbal and nonverbal problem-solving tasks. Multisensory Research, 29(8), 679–701.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Human Health Sciences, Graduate School of MedicineKyoto UniversityKyotoJapan
  2. 2.Department of Neurodevelopmental Psychiatry, Habilitation and Rehabilitation, Faculty of Human Health Sciences, Graduate School of MedicineKyoto UniversityKyotoJapan
  3. 3.Department of PsychiatryKyoto University HospitalKyotoJapan
  4. 4.The Organization for Promoting Neurodevelopmental Disorder ResearchKyotoJapan

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