Skip to main content
SpringerLink
Log in

Reduced Sensory Habituation in Autism and Its Correlation with Behavioral Measures

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

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.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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.

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

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

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

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

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

    Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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).

  • 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 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Author notes

  1. Amanda J. Haskins

    Present address: Psychological and Brain Sciences, Dartmouth College, Hanover, NH, USA

  2. Margaret Kjelgaard

    Present address: Bridgewater State University, Bridgewater, MA, USA

Authors and Affiliations

  1. Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

    Wasifa Jamal, Annie Cardinaux, Amanda J. Haskins, Margaret Kjelgaard & Pawan Sinha

  2. Department of Communication Sciences and Disorders, Massachusetts General Hospital Institute of Health Professions, Boston, MA, USA

    Margaret Kjelgaard

Authors
  1. Wasifa Jamal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Annie Cardinaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amanda J. Haskins
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Margaret Kjelgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pawan Sinha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to Wasifa Jamal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Consent to Participate

Written consent was obtained from the legal guardians, and assent from each participant.

Ethical Approval

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.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jamal, W., Cardinaux, A., Haskins, A.J. et al. Reduced Sensory Habituation in Autism and Its Correlation with Behavioral Measures. J Autism Dev Disord 51, 3153–3164 (2021). https://doi.org/10.1007/s10803-020-04780-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-020-04780-1

Keywords

Search

Navigation