Reduced Sensory Habituation in Autism and Its Correlation with Behavioral Measures

Abstract

Autism is strongly associated with sensory processing difficulties. We investigate sensory habituation, given its relevance for understanding important phenotypic traits like hyper- and hypo-sensitivities. We collected electroencephalography data from 22 neuro-typical(NT) and 13 autistic(ASD) children during the presentation of visual and auditory sequences of repeated stimuli. Our data show that the ASD children have significantly reduced habituation relative to the NT children for both auditory and visual stimuli. These results point to impaired habituation as a modality-general phenomenon in ASD. Additionally, the rates of habituation are correlated with several clinical scores associated with competence along diverse phenotypic dimensions. These data suggest that the sensory difficulties in autism are likely to be associated with reduced habituation and are related to clinical symptomology.

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References

  1. Achenbach, T. M., & Rescorla, L. A. (2004). The Achenbach System of Empirically Based Assessment (ASEBA) for ages 1.5 to 18 years. In The use of psychological testing for treatment planning and outcomes assessment: Volume 2: Instruments for children and adolescents (3rd ed.). London: Routledge.

  2. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders-5 American Journal of Psychiatry (5th ed.). Washington D.C.: American Psychiatric Association.

  3. Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30(1), 52–73.

    Article  Google Scholar 

  4. Ashwin, E., Ashwin, C., Rhydderch, D., Howells, J., & Baron-Cohen, S. (2009). Eagle-eyed visual acuity: An experimental investigation of enhanced perception in autism. Biological Psychiatry, 65, 17–21.

    PubMed  Article  PubMed Central  Google Scholar 

  5. Barry, R. J., & James, A. L. (1988). Coding of stimulus parameters in autistic, retarded, and normal children: Evidence for a two-factor theory of autism. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 6(2), 139–149.

    Article  Google Scholar 

  6. Bernal, M. E., & Miller, W. H. (1970). Electrodermal and cardiac responses of schizophrenic children to sensory stimuli. Psychophysiology, 7(2), 155–168.

    PubMed  Article  PubMed Central  Google Scholar 

  7. Bleichner, M. G., Lundbeck, M., Selisky, M., Minow, F., Jäger, M., Emkes, R., et al. (2015). Exploring miniaturized EEG electrodes for brain-computer interfaces. An EEG you do not see? Physiological Reports. https://doi.org/10.14814/phy2.12362

    Article  PubMed  PubMed Central  Google Scholar 

  8. Bölte, S., Schlitt, S., Gapp, V., Hainz, D., Schirman, S., Poustka, F., et al. (2012). A close eye on the eagle-eyed visual acuity hypothesis of autism. Journal of Autism and Developmental Disorders, 42, 726–733.

    PubMed  Article  PubMed Central  Google Scholar 

  9. Bonnel, A. C., 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, 1–10.

    Article  Google Scholar 

  10. Cascio, C., McGlone, F., Folger, S., Tannan, V., Baranek, G., & Pelphrey, K. A. (2008). Tactile perception in adults with autism: A multidimensional psychophysical study. Journal of Autism and Developmental Disorders, 38(1), 127–137.

    PubMed  Article  PubMed Central  Google Scholar 

  11. Christensen, D. L., Bilder, D. A., Zahorodny, W., Pettygrove, S., Durkin, M. S., Fitzgerald, R. T., et al. (2016). Prevalence and characteristics of autism spectrum disorder among 4-year-old children in the autism and developmental disabilities monitoring network. Journal of Developmental & Behavioral Pediatrics, 37(1), 80–82.

    Article  Google Scholar 

  12. Dabbous, A. O. (2012). Characteristics of auditory brainstem response latencies in children with autism spectrum disorders. Audiological Medicine, 10(3), 122–131.

    Article  Google Scholar 

  13. DePape, A.-M.R., Hall, G. B. C., Tillmann, B., & Trainor, L. J. (2012). Auditory processing in high-functioning adolescents with autism spectrum disorder. PLoS ONE, 7, e44084.

    PubMed  PubMed Central  Article  Google Scholar 

  14. Dunn, W. (2014). Short sensory profile manual (2nd ed.). San Antonio, TX: Pearson Psychological Corporation.

    Google Scholar 

  15. Ferri, R., Agarwal, E. M., Lanuzza, B., Musumeci, S. A., & Pennisi, G. (2003). The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low functioning subjects. Clinical Neuropsychology, 114, 1671–1680.

    Google Scholar 

  16. Gomot, M., Giard, M. H., Adrien, J. L., Barthélémy, C., & Bruneau, N. (2002). Hypersensitivity to acoustic change in children with autism: Electrophysiological evidence of left frontal cortex dysfunctioning. Psychophysiology, 39, 577–584.

    PubMed  Article  Google Scholar 

  17. Guiraud, J. A., Kushnerenko, E., Tomalski, P., Davies, K., Ribeiro, H., & Johnson, M. H. (2011). Differential habituation to repeated sounds in infants at high risk for autism. NeuroReport, 22(16), 845–849.

    PubMed  PubMed Central  Google Scholar 

  18. Haenschel, C., Vernon, D. J., Dwivedi, P., Gruzelier, J. H., & Baldeweg, T. (2005). Event-related brain potential correlates of human auditory sensory memory-trace formation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 25(45), 10494–10501.

    Article  Google Scholar 

  19. Heaton, P., Hermelin, B., & Pring, L. (1998). Autism and pitch processing: A precursor for savant musical ability? Music Perception, 15, 291–305.

    Article  Google Scholar 

  20. Hudac, C., DesChamps, T., Arnett, A., Cairney, B., Ma, R., Webb, S., et al. (2018). Early enhanced processing and delayed habituation to deviance sounds in autism spectrum disorder. Brain and Cognition, 123(2018), 110–119.

    PubMed  PubMed Central  Article  Google Scholar 

  21. Jones, E., Dawson, G., Kelly, J., Estes, A., & Webb, S. (2017). Parent-delivered early intervention in infants at risk for ASD: Effects on electrophysiological and habituaiton measures of social attention. Autism Research, 10(5), 961–972. https://doi.org/10.1002/aur.1754

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kanner, L. (1943). Autistic disturbances of affective contact. Nervous Child., 2(3), 217–250.

    Google Scholar 

  23. Kavšek, M., & Bornstein, M. H. (2010). Visual habituation and dishabituation in preterm infants: A review and meta-analysis. Research in developmental disabilities, 31(5), 951–975.

    PubMed  PubMed Central  Article  Google Scholar 

  24. Khalfa, S., Bruneau, N., Rogé, B., Georgieff, N., Veuillet, E., Adrien, J. L., et al. (2004). Increased perception of loudness in autism. Hearing Research, 198, 87–92.

    PubMed  Article  PubMed Central  Google Scholar 

  25. 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. The American Journal of Psychiatry, 166, 467–475.

    PubMed  Article  PubMed Central  Google Scholar 

  26. Kolesnik, A., Ali, J., Gliga, T., Guiraud, J., Charman, T., Johnson, M., et al. (2019). Increased cortical reactivity to repeated tones at 8 months in infants with later ASD. Translational Psychiatry, 9, 46. https://doi.org/10.1038/s41398-019-0393-x

    Article  PubMed  PubMed Central  Google Scholar 

  27. Lagemann, L., Okamoto, H., Teismann, H., et al. (2010). Bottom-up driven involuntary attention modulates auditory signal in noise processing. BMC Neuroscience, 11, 156.

    PubMed  PubMed Central  Article  Google Scholar 

  28. Lane, A. E., Molloy, C. A., & Bishop, S. L. (2014). Classification of children with autism spectrum disorder by sensory subtype: A case for sensory-based phenotypes. Autism Research, 7(3), 322–333.

    PubMed  Article  PubMed Central  Google Scholar 

  29. Lawson, R. P., Aylward, J., White, S., & Rees, G. (2015). A striking reduction of simple loudness adaptation in autism. Scientific Reports, 5(1), 16157.

    PubMed  PubMed Central  Article  Google Scholar 

  30. Leekam, S. R., Nieto, C., Libby, S. J., Wing, L., & Gould, J. (2007). Describing the sensory abnormalities of children and adults with autism. Journal of Autism and Developmental Disorders, 37(5), 894–910.

    PubMed  Article  PubMed Central  Google Scholar 

  31. Lord, C., Rutter, M., DiLarore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism diagnostic observation schedule—second edition (ADOS-2). Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  32. Marco, E. J., Hinkley, L. B. N., Hill, S. S., & Nagarajan, S. S. (2011). Sensory processing in autism: A review of neurophysiologic findings. Pediatric Research, 69(8), 48–54.

    Article  Google Scholar 

  33. Martineau, J., Roux, S., Garreau, B., Adrien, J. L., & Lelord, G. (1992). Unimodal and crossmodal reactivity in autism: Presence of auditory evoked responses and effect of the repetition of auditory stimuli. Biological Psychiatry, 31(12), 1190–1203.

    PubMed  Article  Google Scholar 

  34. Mazefsky, C. A., Kao, J., & Oswald, D. P. (2011). Preliminary evidence suggesting caution in the use of psychiatric self-report measures with adolescents with high-functioning autism spectrum disorders. Research in Autism Spectrum Disorders, 5(1), 164–174.

    PubMed  PubMed Central  Article  Google Scholar 

  35. McAdam, D. W. (1966). Slow potential changes recorded from human brain during learning of a temporal interval. Psychonomic Science, 6, 435–436.

    Article  Google Scholar 

  36. Miller, L. J., Reisman, J. E., McIntosh, D. N., & Simon, J. (2001). An ecological model of sensory modulation: Performance of children with fragile X syndrome, autistic disorder, attention-deficit/hyperactivity disorder, and sensory modulation dysfunction. In: Understanding the nature of sensory integration with diverse populations (pp. 57–88).

  37. Montagu, J. D., & Coles, E. M. (1966). Mechanism and measurement of the galvanic skin response. Psychological Bulletin, 65(5), 261–279. https://doi.org/10.1037/h0023204

    Article  PubMed  Google Scholar 

  38. O’Riordan, M. A., & Passetti, F. (2006). Discimination in autism within different sensory modalities. Journal of Autism and Developmental Disorders, 36, 665–675.

    PubMed  Article  Google Scholar 

  39. Perry, W., Minassian, A., Lopez, B., Maron, L., & Lincoln, A. (2007). Sensorimotor gating deficits in adults with autism. Biological Psychiatry, 61(4), 482–486.

    PubMed  Article  Google Scholar 

  40. Plichta, M. M., Grimm, O., Morgen, K., Mier, D., Sauer, C., Haddad, L., et al. (2014). Amygdala habituation: A reliable fMRI phenotype. NeuroImage, 103, 383–390.

    PubMed  Article  Google Scholar 

  41. Rankin, C. H., et al. (2009). Habituation revisited: An updated and revised description of the behavioral characteristics of habituation. Neurobiology of Learning and Memory, 92(2), 135–138.

    PubMed  Article  Google Scholar 

  42. Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  43. Sinha, P., Kjelgaard, M. M., Gandhi, T. K., Tsourides, K., Cardinaux, A. L., Pantazis, D., et al. (2014). Autism as a disorder of prediction. Proceedings of the National Academy of Sciences, 111(42), 15220–15225.

    Article  Google Scholar 

  44. Sörqvist, P., Nöstl, A., & Halin, N. (2012). Working memory capacity modulates habituation rate: Evidence from a cross-modal auditory distraction paradigm. Psychonomic Bulletin & Review, 19(2), 245–250.

    Article  Google Scholar 

  45. Tam, F. I., King, J. A., Geisler, D., Korb, F. M., Sareng, J., Ritschel, F., et al. (2017). Altered behavioral and amygdala habituation in high-functioning adults with autism spectrum disorder: An fMRI study. Scientific Reports, 7(1), 13611.

    PubMed  PubMed Central  Article  Google Scholar 

  46. 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.

    PubMed  Article  PubMed Central  Google Scholar 

  47. Tomchek, S. D., & Dunn, W. (2007). Sensory processing in children with and without autism: A comparative study using the short sensory profile. The American Journal of Occupational Therapy, 61(2), 190–200.

    PubMed  Article  PubMed Central  Google Scholar 

  48. Webb, S. J., Jones, E. J. H., Merkle, K., Murias, M., Greenson, J., Richards, T., et al. (2010). Response to familiar faces, newly familiar faces, and novel faces as assessed by ERPs is intact in adults with autism spectrum disorders. International Journal of Psychophysiology, 77(2), 106–117.

    PubMed  PubMed Central  Article  Google Scholar 

  49. Wechsler, D. (2014). WISC-V administration and scoring manual. San Antonio, TX: Psychological Corporation.

    Google Scholar 

  50. Williams, D. L., Goldstein, G., & Minshew, N. J. (2006). The profile of memory function in children with autism. Neuropsychology, 20(1), 21–29.

    PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgments

We are grateful to the families who participated in our research for their time and dedication to the pursuit of better understanding autism spectrum disorder. We also wish to express our gratitude to the McGovern Institute for Brain Research Martinos Imaging Center facility and staff, and the contributions of Lukas Vogelsang, Rowan Cheung, Leila Denna, Emily Losordo, Alison Franco, James Borders, Molly Jabeck, Xue Bao, Alesa Commedore, Jennifer McCleary, Thuy Duong Vuong, Anita Liu, Lily Zhang, Arushi Agarwal, and Nishad Sharker.

Funding

This research was supported by the Simons Foundation Autism Research Initiative and a pilot grant from the MIT Simons Center for the Social Brain.

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WJ designed and performed the experiments, collected and analyzed the data, and wrote the manuscript. AC conducted outreach, screening, enrollment of participants; contributed to the design of experiments, collected data, performed scoring and administration of behavioral measures, and reviewed the manuscript. AJH contributed to participant enrollment and phenotyping. MK and PS contributed to study design, data analysis, and writing the manuscript.

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Correspondence to Wasifa Jamal.

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This study was approved by Massachusetts Institute of Technology (MIT) Committee on Use of Humans as Experimental Subjects (COUHES) in accordance with all institutional review board requirements.

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Jamal, W., Cardinaux, A., Haskins, A.J. et al. Reduced Sensory Habituation in Autism and Its Correlation with Behavioral Measures. J Autism Dev Disord (2020). https://doi.org/10.1007/s10803-020-04780-1

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Keywords

  • Sensory habituation
  • Autism
  • Hyper and hypo-sensitivity
  • Audition
  • Vision
  • Electroencephalography