Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • American Psychiatric Association. (2013). Diagnostic and Statistical manual of mental disorders (5th edition (DSM 5)). Arlington: American Psychiatric Publishing.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Baron-Cohen, S., Leslie, A. M., & Frith, U. (1985). Does the autistic-child have a theory of mind? Cognition, 21(1), 37–46.

    PubMed  Google Scholar 

  • 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.

    PubMed  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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Binder, M. (2015). Neural correlates of audiovisual temporal processing—Comparison of temporal order and simultaneity judgments. Neuroscience, 300, 432–447.

    PubMed  Google Scholar 

  • Campanella, S., & Belin, P. (2007). Integrating face and voice in person perception. Trends in Cognitive Sciences, 11(12), 535–543.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2003). Autistic traits in the general population: A twin study. Archives of General Psychiatry, 60(5), 524–530.

    PubMed  Google Scholar 

  • Crane, L., Goddard, L., & Pring, L. (2009). Sensory processing in adults with autism spectrum disorders. Autism, 13(3), 215–228.

    PubMed  Google Scholar 

  • 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.

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • de Gelder, B., & Vroomen, J. (2000). The perception of emotions by ear and by eye. Cognition & Emotion, 14(3), 289–311.

    Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Elsabbagh, M., & Johnson, M. H. (2016). Autism and the social brain: The first-year puzzle. Biological Psychiatry, 80(2), 94–99.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Günay, C., & Maida, A. S. (2006). Using temporal binding for hierarchical recruitment of conjunctive concepts over delayed lines. Neurocomputing, 69(4–6), 317–367.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York, NY: The Guilford Press.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Shams, L., Kamitani, Y., & Shimojo, S. (2000). Illusions - What you see is what you hear. Nature, 408(6814), 788–788.

    PubMed  Google Scholar 

  • Smith, E. G., & Bennetto, L. (2007). Audiovisual speech integration and lipreading in autism. Journal of Child Psychology and Psychiatry, 48(8), 813–821.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Turi, M., Karaminis, T., Pellicano, E., & Burr, D. (2016). No rapid audiovisual recalibration in adults on the autism spectrum. Scientific Reports, 6, 21756.

    PubMed  PubMed Central  Google Scholar 

  • van Boxtel, J. J. A., & Lu, H. J. (2013). A predictive coding perspective on autism spectrum disorders. Frontiers in Psychology, 4, 19.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Wechsler, D. (1997). Wechsler Adult Intelligence Scale-third edition (WAIS-III). San Antonio: The Psychological Corporation.

    Google Scholar 

  • 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.

    Google Scholar 

Download references

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 information

Authors and Affiliations

  1. Faculty of Human Health Sciences, Graduate School of Medicine, Kyoto University, 53 Shogoin Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, Japan

    Sayaka Kawakami, Shuo Zhao & Motomi Toichi

  2. Department of Neurodevelopmental Psychiatry, Habilitation and Rehabilitation, Faculty of Human Health Sciences, Graduate School of Medicine, Kyoto University, 53 Shogoin Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, Japan

    Shota Uono

  3. Department of Psychiatry, Kyoto University Hospital, 54 Shogoin Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, Japan

    Sadao Otsuka

  4. The Organization for Promoting Neurodevelopmental Disorder Research, 40 Shogoin Sanno-cho, Sakyo-ku, Kyoto, 606-8392, Japan

    Sadao Otsuka, Shuo Zhao & Motomi Toichi

Authors
  1. Sayaka Kawakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shota Uono
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sadao Otsuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuo Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Motomi Toichi
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Sayaka Kawakami.

Ethics declarations

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawakami, S., Uono, S., Otsuka, S. et al. Everything has Its Time: Narrow Temporal Windows are Associated with High Levels of Autistic Traits Via Weaknesses in Multisensory Integration. J Autism Dev Disord 50, 1561–1571 (2020). https://doi.org/10.1007/s10803-018-3762-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-018-3762-z

Keywords

Search

Navigation