Journal of Autism and Developmental Disorders

, Volume 45, Issue 2, pp 506–523 | Cite as

Attenuated Auditory Event-Related Potentials and Associations with Atypical Sensory Response Patterns in Children with Autism

  • Franc C. L. Donkers
  • Sarah E. Schipul
  • Grace T. Baranek
  • Katherine M. Cleary
  • Michael T. Willoughby
  • Anna M. Evans
  • John C. Bulluck
  • Jeanne E. Lovmo
  • Aysenil Belger
Original Paper

Abstract

Neurobiological underpinnings of unusual sensory features in individuals with autism are unknown. Event-related potentials elicited by task-irrelevant sounds were used to elucidate neural correlates of auditory processing and associations with three common sensory response patterns (hyperresponsiveness; hyporesponsiveness; sensory seeking). Twenty-eight children with autism and 39 typically developing children (4–12 year-olds) completed an auditory oddball paradigm. Results revealed marginally attenuated P1 and N2 to standard tones and attenuated P3a to novel sounds in autism versus controls. Exploratory analyses suggested that within the autism group, attenuated N2 and P3a amplitudes were associated with greater sensory seeking behaviors for specific ranges of P1 responses. Findings suggest that attenuated early sensory as well as later attention-orienting neural responses to stimuli may underlie selective sensory features via complex mechanisms.

Keywords

Autism spectrum disorder Sensory processing Event-related potentials P1 N2 P3a 

References

  1. Adoh, T. O., Woodhouse, J. M., & Oduwaiye, K. A. (1992). The Cardiff test: A new visual acuity test for toddlers and children with intellectual impairment. A preliminary report. Optometry and Vision Science, 69(6), 427–432.PubMedCrossRefGoogle Scholar
  2. Aiken, L., & West, S. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: Sage Publications.Google Scholar
  3. Albrecht, R., Suchodoletz, W., & Uwer, R. (2000). The development of auditory evoked dipole source activity from childhood to adulthood. Clinical Neurophysiology, 111(12), 2268–2276.PubMedCrossRefGoogle Scholar
  4. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Association.Google Scholar
  5. Baranek, G. T. (1999). Autism during infancy: A retrospective video analysis of sensory-motor and social behaviors at 9–12 months of age. Journal of Autism and Developmental Disorders, 29(3), 213–224.PubMedCrossRefGoogle Scholar
  6. Baranek, G. T., & Berkson, G. (1994). Tactile defensiveness in children with developmental disabilities: Responsiveness and habituation. Journal of Autism and Developmental Disorders, 24(4), 457–471.PubMedCrossRefGoogle Scholar
  7. Baranek, G. T., Boyd, B. A., Poe, M. D., David, F. J., & Watson, L. R. (2007). Hyperresponsive sensory patterns in young children with autism, developmental delay, and typical development. American Journal of Mental Retardation, 112(4), 233–245.PubMedCrossRefGoogle Scholar
  8. Baranek, G. T., David, F. J., Poe, M. D., Stone, W. L., & Watson, L. R. (2006). Sensory Experiences Questionnaire: Discriminating sensory features in young children with autism, developmental delays, and typical development. Journal of Child Psychology and Psychiatry, 47(6), 591–601.PubMedCrossRefGoogle Scholar
  9. Baranek, G. T., Watson, L. R., Boyd, B. A., Poe, M. D., David, F. J., & McGuire, L. (2013). Hyporesponsiveness to social and nonsocial sensory stimuli in children with autism, children with developmental delays, and typically developing children. Development and Psychopathology, 25, 307–320.PubMedCentralPubMedCrossRefGoogle Scholar
  10. Ben-Sasson, A., Cermak, S. A., Orsmond, G. I., Tager-Flusberg, H., Carter, A. S., Kadlec, M. B., et al. (2007). Extreme sensory modulation behaviors in toddlers with autism spectrum disorders. The American Journal of Occupational Therapy, 61(5), 584–592.PubMedCrossRefGoogle Scholar
  11. Ben-Sasson, A., Cermak, S. A., Orsmond, G. I., Tager-Flusberg, H., Kadlec, M. B., & Carter, A. S. (2008). Sensory clusters of toddlers with autism spectrum disorders: Differences in affective symptoms. Journal of Child Psychology and Psychiatry, 49(8), 817–825.PubMedCrossRefGoogle Scholar
  12. Ben-Sasson, A., Hen, L., Fluss, R., Cermak, S. A., Engel-Yeger, B., & Gal, E. (2009). A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(1), 1–11.PubMedCrossRefGoogle Scholar
  13. Bomba, M. D., & Pang, E. W. (2004). Cortical auditory evoked potentials in autism: A review. International Journal of Psychophysiology, 53(3), 161–169.PubMedCrossRefGoogle Scholar
  14. Brock, M. E., Freuler, A., Baranek, G. T., Watson, L. R., Poe, M. D., & Sabatino, A. (2012). Temperament and sensory features of children with autism. Journal of Autism and Developmental Disorders, 42(11), 2271–2284.PubMedCentralPubMedCrossRefGoogle Scholar
  15. Bruneau, N., Roux, S., Adrien, J. L., & Barthélémy, C. (1999). Auditory associative cortex dysfunction in children with autism: Evidence from late auditory evoked potentials (N1 wave-T complex). Clinical Neurophysiology, 110(11), 1927–1934.PubMedCrossRefGoogle Scholar
  16. Caviness, V. S., Jr., Kennedy, D. N., Richelme, C., Rademacher, J., & Filipek, P. A. (1996). The human brain age 7–11 years: A volumetric analysis based on magnetic resonance images. Cerebral Cortex, 6(5), 726–736.PubMedCrossRefGoogle Scholar
  17. Ceponiene, R., Cheour, M., & Näätänen, R. (1998). Interstimulus interval and auditory event-related potentials in children: evidence for multiple generators. Electroencephalography and Clinical Neurophysiology, 108(4), 345–354.PubMedCrossRefGoogle Scholar
  18. Ceponiene, R., Lepistö, T., Shestakova, A., Vanhala, R., Alku, P., Näätänen, R., et al. (2003). Speech-sound-selective auditory impairment in children with autism: They can perceive but do not attend. Proceedings of the National Academy of Sciences of the United States of America, 100(9), 5567–5572.PubMedCentralPubMedCrossRefGoogle Scholar
  19. Ceponiene, R., Rinne, T., & Näätänen, R. (2002). Maturation of cortical sound processing as indexed by event-related potentials. Clinical Neurophysiology, 113(6), 870–882.PubMedCrossRefGoogle Scholar
  20. Cheour, M. (2007). Development of mismatch negativity (MMN) during infancy. In M. De Haan (Ed.), Infant EEG and event-related potentials (pp. 19–30). London: Psychology Press.Google Scholar
  21. Comerchero, M. D., & Polich, J. (1998). P3a, perceptual distinctiveness, and stimulus modality. Cognitive Brain Research, 7(1), 41–48.PubMedCrossRefGoogle Scholar
  22. Cornish, K. M., & McManus, I. C. (1996). Hand preference and hand skill in children with autism. Journal of Autism and Developmental Disorders, 26(6), 597–609.PubMedCrossRefGoogle Scholar
  23. Crane, L., Goddard, L., & Pring, L. (2009). Sensory processing in adults with autism spectrum disorders. Autism, 13(3), 215–228.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. Dawson, G., & Watling, R. (2000). Interventions to facilitate auditory, visual, and motor integration in autism: A review of the evidence. Journal of Autism and Developmental Disorders, 30(5), 415–421.PubMedCrossRefGoogle Scholar
  26. Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21.PubMedCrossRefGoogle Scholar
  27. Dunn, W. (1997). The impact of sensory processing abilities on the daily lives of young children and their families: A conceptual model. Infants and Young Children, 9(4), 23–35.CrossRefGoogle Scholar
  28. Dunn, W. (1999). Sensory profile. San Antonio, TX: Psychological Corporation.Google Scholar
  29. Dunn, W., & Westman, K. (1997). The sensory profile: The performance of a national sample of children without disabilities. The American Journal of Occupational Therapy, 51(1), 25–34.PubMedCrossRefGoogle Scholar
  30. Fox, J. (1991). Regression diagnostics. Newbury Park, CA: Sage Publications.Google Scholar
  31. Gage, N. M., Siegel, B., Callen, M., & Roberts, T. P. (2003). Cortical sound processing in children with autism disorder: An MEG investigation. Neuroreport, 14, 2047–2051.PubMedCrossRefGoogle Scholar
  32. Gomot, M., Blanc, R., Clery, H., Roux, S., Barthelemy, C., & Bruneau, N. (2011). Candidate electrophysiological endophenotypes of hyper-reactivity to change in autism. Journal of Autism and Developmental Disorders, 41(6), 705–714.PubMedCrossRefGoogle Scholar
  33. Gomot, M., & Wicker, B. (2012). A challenging, unpredictable world for people with autism spectrum disorder. International Journal of Psychophysiology, 83(2), 240–747.PubMedCrossRefGoogle Scholar
  34. Gotham, K., Pickles, A., & Lord, C. (2009). Standardizing ADOS scores for a measure of severity in autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(5), 693–705.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Gotham, K., Risi, S., Pickles, A., & Lord, C. (2007). The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders, 37(4), 613–627.PubMedCrossRefGoogle Scholar
  36. 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.PubMedGoogle Scholar
  37. Harrison, J., & Hare, D. J. (2004). Brief report: Assessment of sensory abnormalities in people with autistic spectrum disorders. Journal of Autism and Developmental Disorders, 34(6), 727–730.PubMedCrossRefGoogle Scholar
  38. Hill, E. L. (2004). Executive dysfunction in autism. Trends in Cognitive Science, 8(1), 26–32.CrossRefGoogle Scholar
  39. Jansson-Verkasalo, E., Ruusuvirta, T., Huotilainen, M., Alku, P., Kushnerenko, E., Suominen, K., et al. (2010). Atypical perceptual narrowing in prematurely born infants is associated with compromised language acquisition at 2 years of age. BMC Neuroscience, 11, 88.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Jeste, S. S., & Nelson, C. A. (2009). Event related potentials in the understanding of autism spectrum disorders: An analytical review. Journal of Autism and Developmental Disorders, 39(3), 495–510.PubMedCrossRefGoogle Scholar
  41. Kemner, C., Verbaten, M. N., Cuperus, J. M., Camfferman, G., & van Engeland, H. (1995). Auditory event-related brain potentials in autistic children and three different control groups. Biological Psychiatry, 38(3), 150–165.PubMedCrossRefGoogle Scholar
  42. Key, A. P., Dove, G. O., & Maguire, M. J. (2005). Linking brainwaves to the brain: An ERP primer. Developmental Neuropsychology, 27(2), 183–215.PubMedCrossRefGoogle Scholar
  43. Kientz, M. A., & Dunn, W. (1997). A comparison of the performance of children with and without autism on the sensory profile. American Journal of Occupational Therapy, 51(7), 530–537.PubMedCrossRefGoogle Scholar
  44. 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.PubMedCrossRefGoogle Scholar
  45. Lepistö, T., Kujala, T., Vanhala, R., Alku, P., Huotilainen, M., & Näätänen, R. (2005). The discrimination of and orienting to speech and non-speech sounds in children with autism. Brain Research, 1066(1–2), 147–157.PubMedCrossRefGoogle Scholar
  46. Lincoln, A. J., Courchesne, E., Harms, L., & Allen, M. (1993). Contextual probability evaluation in autistic, receptive developmental language disorder, and control children: Event-related brain potential evidence. Journal of Autism and Developmental Disorders, 23(1), 37–58.PubMedCrossRefGoogle Scholar
  47. Lincoln, A. J., Courchesne, E., Harms, L., & Allen, M. (1995). Sensory modulation of auditory stimuli in children with autism and receptive developmental language disorder: Event-related brain potential evidence. Journal of Autism and Developmental Disorders, 25, 521–529.PubMedCrossRefGoogle Scholar
  48. Liss, M., Saulnier, C., Fein, D., & Kinsbourne, M. (2006). Sensory and attention abnormalities in autistic spectrum disorders. Autism, 10(2), 155–172.PubMedCrossRefGoogle Scholar
  49. Little, L. M., Freuler, A. C., Houser, M. B., Guckian, L., Carbine, K., David, F. J., et al. (2011). Psychometric validation of the Sensory Experiences Questionnaire. American Journal of Occupational Therapy, 65(2), 207–210.PubMedCentralPubMedCrossRefGoogle Scholar
  50. Lord, C., Risi, S., DiLavore, P. S., Shulman, C., Thurm, A., & Pickles, A. (2006). Autism from 2 to 9 years of age. Archives of General Psychiatry, 63(6), 694–701.PubMedCrossRefGoogle Scholar
  51. Lord, C., Rutter, M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. L. (2012). Autism diagnostic observation schedule (ADOS-2) (2nd ed.). Torrence, CA: Western Psychological Services.Google Scholar
  52. Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24(5), 659–685.PubMedCrossRefGoogle Scholar
  53. 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(5 Pt 2), 48R–54R.PubMedCentralPubMedCrossRefGoogle Scholar
  54. Mazurek, M. O., Vasa, R. A., Kalb, L. G., Kanne, S. M., Rosenberg, D., Keefer, A., et al. (2013). Anxiety, sensory over-responsivity, and gastrointestinal problems in children with autism spectrum disorders. Journal of Abnormal Child Psychology, 41(1), 165–176.PubMedCrossRefGoogle Scholar
  55. McManus, I. C., Sik, G., Cole, D. R., Mellon, A. F., Wong, J., & Kloss, J. (1988). The development of handedness in children. British Journal of Developmental Psychology, 6, 257–273.CrossRefGoogle Scholar
  56. Miller, L. J., Anzalone, M. E., Lane, S. J., Cermak, S. A., & Osten, E. T. (2007). Concept evolution in sensory integration: A proposed nosology for diagnosis. The American Journal of Occupational Therapy, 61(2), 135–140.PubMedCrossRefGoogle Scholar
  57. Mullen, E. M. (1995). Mullen scales of early learning (AGS edition). Los Angeles, CA: Western Psychological.Google Scholar
  58. Näätänen, R., Gaillard, A. W., & Mäntysalo, S. (1978). Early selective-attention effect on evoked potential reinterpreted. Acta Psychologica, 42(4), 313–329.PubMedCrossRefGoogle Scholar
  59. Oostenveld, R., Fries, P., Maris, E., & Schoffelen, J.-M. (2011). FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational Intelligence and Neuroscience, 2011, Art. ID 156869. doi:10.1155/2011/156869.
  60. Orekhova, E. V., Tsetlin, M. M., Butorina, A. V., Novikova, S. I., Gratchev, V. V., Sokolov, P. A, et al. (2012). Auditory cortex responses to clicks and sensory modulation difficulties in children with autism spectrum disorders (ASD). PLoS One, 7(6), e39906. doi:10.1371/journal.pone.0039906.
  61. Osterling, J., & Dawson, G. (1994). Early recognition of children with autism: A study of first birthday home videotapes. Journal of Autism and Developmental Disorders, 24(3), 247–257.PubMedCrossRefGoogle Scholar
  62. Reynolds, S., & Lane, S. J. (2008). Diagnostic validity of sensory over-responsivity: A review of the literature and case reports. Journal of Autism and Developmental Disorders, 38(3), 516–529.PubMedCrossRefGoogle Scholar
  63. Roberts, T. P., Khan, S. Y., Rey, M., Monroe, J. F., Cannon, K., Blaskey, L., et al. (2010). MEG detection of delayed auditory evoked responses in autism spectrum disorders: Towards an imaging biomarker for autism. Autism Research, 3(1), 8–18.PubMedCentralPubMedGoogle Scholar
  64. Roid, G. H. (2003). Stanford-Binet Intelligence Scales (SB5). Riverside, IL: Rolling Meadows.Google Scholar
  65. Roid, G. H., & Miller, L. J. (1997). Leiter International Performance Scale–Revised. Wood Dale, IL: Stoelting Co.Google Scholar
  66. Sable, J. J., Low, K. A., Maclin, E. L., Fabiani, M., & Gratton, G. (2004). Latent inhibition mediates N1 attenuation to repeating sounds. Psychophysiology, 41(4), 636–642.PubMedCrossRefGoogle Scholar
  67. Schopler, E., Reichler, R. J., & Renner, B. R. (1986). The Childhood Autism Rating Scale (CARS): For diagnostic screening and classification of autism. New York, NY: Irvington.Google Scholar
  68. Semlitsch, H. V., Anderer, P., Schuster, P., & Presslich, O. (1986). A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. Psychophysiology, 23(6), 695–703.PubMedCrossRefGoogle Scholar
  69. Sokhadze, E., Baruth, J., Tasman, A., Sears, L., Mathai, G., et al. (2009). Event-related potential study of novelty processing abnormalities in autism. Applied Psychophysiology and Biofeedback, 34, 37–51.PubMedCrossRefGoogle Scholar
  70. Sparrow, S. S., Balla, D. A., & Cichetti, D. V. (1984). Vineland Adaptive Behavior Scales: Interview edition, expanded form manual. Circle Pines, MN: American Guidance Service.Google Scholar
  71. Stone, W. L., & Hogan, K. L. (1993). A structured parent interview for identifying young children with autism. Journal of Autism and Developmental Disorders, 23(4), 639–652.PubMedCrossRefGoogle Scholar
  72. Sussman, E., Steinschneider, M., Gumenyuk, V., Grushko, J., & Lawson, K. (2008). The maturation of human evoked brain potentials to sounds presented at different stimulus rates. Hearing Research, 236(1–2), 61–79.PubMedCentralPubMedCrossRefGoogle Scholar
  73. Tonnquist-Uhlen, I. (1996). Topography of auditory evoked cortical potentials in children with severe language impairment. Scandinavian Audiology Supplement, 25(44), 1–40.Google Scholar
  74. Watson, L. R., Patten, E., Baranek, G. T., Poe, M., Boyd, B. A., Freuler, A., et al. (2011). Differential associations between sensory response patterns and language, social, and communication measures in children with autism or other developmental disabilities. Journal of Speech, Language, and Hearing Research, 54(6), 1562–1576.PubMedCentralPubMedCrossRefGoogle Scholar
  75. Whitehouse, A. J., & Bishop, D. V. (2008). Do children with autism ‘switch off’ to sounds? An investigation using event-related potentials. Developmental Science, 11(4), 516–524.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Franc C. L. Donkers
    • 1
    • 2
    • 3
  • Sarah E. Schipul
    • 1
    • 2
  • Grace T. Baranek
    • 2
    • 4
  • Katherine M. Cleary
    • 1
  • Michael T. Willoughby
    • 5
  • Anna M. Evans
    • 1
    • 2
  • John C. Bulluck
    • 4
  • Jeanne E. Lovmo
    • 4
  • Aysenil Belger
    • 1
    • 2
    • 6
  1. 1.Department of PsychiatryUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.Carolina Institute for Developmental DisabilitiesUniversity of North CarolinaChapel HillUSA
  3. 3.Department of PsychologyTilburg UniversityTilburgThe Netherlands
  4. 4.Department of Allied Health SciencesUniversity of North Carolina at Chapel HillChapel HillUSA
  5. 5.FPG Child Development InstituteUniversity of North Carolina at Chapel HillChapel HillUSA
  6. 6.Duke-UNC Brain Imaging and Analysis CenterDurhamUSA

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