Abstract
Atypical pitch processing is a feature of Autism Spectrum Disorder (ASD), which affects non-tone language speakers’ communication. Lifelong auditory experience has been demonstrated to modify genetically-predisposed risks for pitch processing. We examined individuals with ASD to test the hypothesis that lifelong auditory experience in tone language may eliminate impaired pitch processing in ASD. We examined children’s and adults’ Frequency-following Response (FFR), a neurophysiological component indexing early neural sensory encoding of pitch. Univariate and machine-learning-based analytics suggest less robust pitch encoding and diminished pitch distinctions in the FFR from individuals with ASD. Contrary to our hypothesis, results point to a linguistic pitch encoding impairment associated with ASD that may not be eliminated even by lifelong sensory experience.
Similar content being viewed by others
Data Availability
The numeric data and analysis scripts are available on https://osf.io/nqpka/?view_only=851f70775d8e4659b81cd8d0084df62f.
References
Antoniou, M., To, C. K., & Wong, P. C. (2015). Auditory cues that drive language development are language specific: evidence from Cantonese. Applied Psycholinguistics, 36(6), 1493.
Baltaxe, C. A. and Simmons, J. Q. (1985). Prosodic development in normal and autistic children. In Communication problems in autism, pages 95–125. Springer.
Bates, D., Machler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software Articles, 67(1), 1–48.
Bidelman, G. M. (2018). Subcortical sources dominate the neuroelectric auditory frequency-following response to speech. Neuroimage, 175, 56–69.
Bidelman, G. M., Krishnan, A., & Gandour, J. T. (2011). Enhanced brainstem encoding predicts musicians’ perceptual advantages with pitch. European Journal of Neuroscience, 33(3), 530–538.
Bishop, D. V. (2010). Overlaps between autism and language impairment: phenomimicry or shared etiology? Behavior Genetics, 40(5), 618–629.
Bonnel, A., McAdams, S., Smith, B., Berthiaume, C., Bertone, A., Ciocca, V., et al. (2010). Enhanced pure-tone pitch discrimination among persons with autism but not Asperger syndrome. Neuropsychologia, 48(9), 2465–2475.
Bonnel, A., 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(2), 226–235.
Chandrasekaran, B., & Kraus, N. (2010). The scalp-recorded brainstem response to speech: neural origins and plasticity. Psychophysiology, 47(2), 236–246.
Chandrasekaran, B., Skoe, E., & Kraus, N. (2014). An integrative model of subcortical auditory plasticity. Brain Topography, 27(4), 539–552.
Chang, C.-C., & Lin, C.-J. (2011). LIBSVM: A library for support vector machines. ACM Transactions on Intelligent Systems and Technology (TIST), 2(3), 27.
Cheng, S. T., Lam, G. Y., & To, C. K. (2017). Pitch perception in tone language-speaking adults with and without autism spectrum disorders. i-Perception, 8(3), 2041669517711200.
Chevallier, C., Noveck, I., Happe, F., & Wilson, D. (2009). From acoustics to grammar: Perceiving and interpreting grammatical prosody in adolescents with Asperger syndrome. Research in Autism Spectrum Disorders, 3(2), 502–516.
Ciocca, V., & Lui, J. (2003). The development of the perception of Cantonese lexical tones. Journal of Multilingual Communication Disorders, 1(2), 141–147.
Coffey, E. B., Nicol, T., White-Schwoch, T., Chandrasekaran, B., Krizman, J., Skoe, E., et al. (2019). Evolving perspectives on the sources of the frequency-following response. Nature Communications, 10(1), 1–10.
Crystal, D. (1969). Prosodic systems and intonation in English (Vol. 1). Cambridge: Cambridge University Press.
Davids, N., Segers, E., Van den Brink, D., Mitterer, H., van Balkom, H., Hagoort, P., & Verhoeven, L. (2011). The nature of auditory discrimination problems in children with specific language impairment: An MMN study. Neuropsychologia, 49(1), 19–28.
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.
Diehl, J. J., Bennetto, L., Watson, D., Gunlogson, C., & McDonough, J. (2008). Resolving ambiguity: a psycholinguistic approach to understanding prosody processing in high-functioning autism. Brain and Language, 106(2), 144–152.
Gockley, J., Willsey, A. J., Dong, S., Dougherty, J. D., Constantino, J. N., & Sanders, S. J. (2015). The female protective effect in autism spectrum disorder is not mediated by a single genetic locus. Molecular Autism, 6(1), 25.
Grossman, R. B., Bemis, R. H., Skwerer, D. P., and Tager-Flusberg, H. (2010). Lexical and affective prosody in children with high-functioning autism. Journal of Speech, Language, and Hearing Research.
Haesen, B., Boets, B., & Wagemans, J. (2011). A review of behavioural and electrophysiological studies on auditory processing and speech perception in autism spectrum disorders. Research in Autism Spectrum Disorders, 5(2), 701–714.
Heaton, P. (2003). Pitch memory, labelling and disembedding in autism. Journal of Child Psychology and Psychiatry, 44(4), 543–551.
Heaton, P. (2005). Interval and contour processing in autism. Journal of Autism and Developmental Disorders, 35(6), 787.
Heaton, P., Hermelin, B., & Pring, L. (1998). Autism and pitch processing: A precursor for savant musical ability? Music Perception: An Interdisciplinary Journal, 15(3), 291–305.
Heaton, P., Hudry, K., Ludlow, A., & Hill, E. (2008). Superior discrimination of speech pitch and its relationship to verbal ability in autism spectrum disorders. Cognitive Neuropsychology, 25(6), 771–782.
Hesling, I., Dilharreguy, B., Peppe, S., Amirault, M., Bouvard, M., & Allard, M. (2010). The integration of prosodic speech in high functioning autism: a preliminary fMRI study. PLoS ONE, 5(7), e11571.
Ingvalson, E. M., & Wong, P. (2013). Training to improve language outcomes in cochlear implant recipients. Frontiers in Psychology, 4, 263.
Jarvinen-Pasley, A., & Heaton, P. (2007). Evidence for reduced domain-specificity in auditory processing in autism. Developmental Science, 10(6), 786–793.
Kargas, N., Lopez, B., Reddy, V., & Morris, P. (2015). The relationship between auditory processing and restricted, repetitive behaviors in adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(3), 658–668.
Kraus, N., Anderson, S., and White-Schwoch, T. (2017). The frequency-following response: a window into human communication. In The Frequency-Following Response, pages 1–15. Springer.
Krishnan, A., & Gandour, J. T. (2009). The role of the auditory brainstem in processing linguistically relevant pitch patterns. Brain and Language, 110(3), 135–148.
Krishnan, A., Gandour, J. T., & Bidelman, G. M. (2010). The effects of tone language experience on pitch processing in the brainstem. Journal of Neurolinguistics, 23(1), 81–95.
Krishnan, A., Xu, Y., Gandour, J., & Cariani, P. (2005). Encoding of pitch in the human brainstem is sensitive to language experience. Brain Research. Cognitive Brain Research, 25(1), 161–168.
Krishnan, A., Xu, Y., Gandour, J. T., & Cariani, P. A. (2004). Human frequency-following response: representation of pitch contours in Chinese tones. Hearing Research, 189(1), 1–12.
Krizman, J., Bonacina, S., & Kraus, N. (2019). Sex differences in subcortical auditory processing emerge across development. Hearing Research, 380, 166–174.
Lau, J. C., Wong, P. C., & Chandrasekaran, B. (2017). Context-dependent plasticity in the subcortical encoding of linguistic pitch patterns. Journal of Neurophysiology, 117(2), 594–603.
Lehmann, A., Skoe, E., Moreau, P., Peretz, I., & Kraus, N. (2015). Impairments in musical abilities reflected in the auditory brainstem: evidence from congenital amusia. European Journal of Neuroscience, 42(1), 1644–1650.
Lenth, R. V. (2016). Least-squares means: The R package lsmeans. Journal of Statistical Software, 69(1), 1–33.
Lepisto, 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.
Lim, H. A. (2010). Effect of “developmental speech and language training through music” on speech production in children with autism spectrum disorders. Journal of Music Therapy, 47(1), 2–26.
Lim, H. A., & Draper, E. (2011). The effects of music therapy incorporated with applied behavior analysis verbal behavior approach for children with autism spectrum disorders. Journal of Music Therapy, 48(4), 532–550.
Liu, F., Maggu, A. R., Lau, J. C., & Wong, P. C. (2014). Brainstem encoding of speech and musical stimuli in congenital amusia: evidence from Cantonese speakers. Frontiers in Human Neuroscience, 8, 1029.
Loomes, R., Hull, L., & Mandy, W. P. L. (2017). What is the male-to-female ratio in autism spectrum disorder? a systematic review and meta-analysis. Journal of the American Academy of Child & Adolescent Psychiatry, 56(6), 466–474.
Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: an open-source toolbox for the analysis of eventrelated potentials. Frontiers in Human Neuroscience, 8, 213.
Losh, M., Klusek, J., Martin, G. E., Sideris, J., Parlier, M., & Piven, J. (2012). Defining genetically meaningful language and personality traits in relatives of individuals with fragile x syndrome and relatives of individuals with autism. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 159(6), 660–668.
Losh, M., Martin, G. E., Lee, M., Klusek, J., Sideris, J., Barron, S., & Wassink, T. (2017). Developmental markers of genetic liability to autism in parents: A longitudinal, multigenerational study. Journal of Autism and Developmental Disorders, 47(3), 834–845.
Losh, M., Sullivan, P. F., Trembath, D., & Piven, J. (2008). Current developments in the genetics of autism: from phenome to genome. Journal of Neuropathology & Experimental Neurology, 67(9), 829–837.
Maggu, A. R., Liu, F., Antoniou, M., & Wong, P. C. (2016). Neural correlates of indicators of sound change in Cantonese: evidence from cortical and subcortical processes. Frontiers in Human Neuroscience, 10, 652.
Maggu, A. R., Wong, P. C., Antoniou, M., Bones, O., Liu, H., & Wong, F. C. (2018). Effects of combination of linguistic and musical pitch experience on subcortical pitch encoding. Journal of Neurolinguistics, 47, 145–155.
Marmel, F., Linley, D., Carlyon, R., Gockel, H., Hopkins, K., & Plack, C. (2013). Subcortical neural synchrony and absolute thresholds predict frequency discrimination independently. Journal of the Association for Research in Otolaryngology, 14(5), 757–766.
Mayer, J. L., Hannent, I., & Heaton, P. F. (2016). Mapping the developmental trajectory and correlates of enhanced pitch perception on speech processing in adults with ASD. Journal of Autism and Developmental Disorders, 46(5), 1562–1573.
McCann, J., Peppe, S., Gibbon, F. E., O’Hare, A., & Rutherford, M. (2007). Prosody and its relationship to language in school-aged children with high-functioning autism. International Journal of Language & Communication Disorders, 42(6), 682–702.
Mok, P. P., Zuo, D., & Wong, P. W. (2013). Production and perception of a sound change in progress: tone merging in Hong Kong Cantonese. Language Variation and Change, 25(03), 341–370.
Mottron, L., Dawson, M., Soulieres, I., Hubert, B., & Burack, J. (2006). Enhanced perceptual functioning in autism: an update, and eight principles of autistic perception. Journal of Autism and Developmental Disorders, 36(1), 27–43.
Mottron, L., Peretz, I., & Menard, E. (2000). Local and global processing of music in high-functioning persons with autism: beyond central coherence? The Journal of Child Psychology and Psychiatry and Allied Disciplines, 41(8), 1057–1065.
Näätänen, R., Lehtokoski, A., Lennes, M., Cheour, M., Huotilainen, M., Iivonen, A., et al. (1997). Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature, 385, 432–434.
Näätänen, R., Paavilainen, P., Rinne, T., & Alho, K. (2007). The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clinical Neurophysiology, 118(12), 2544–2590.
Naigles, L. R. (2013). Input and language development in children with autism. In Seminars in speech and language, volume 34, pages 237–248. Thieme Medical Publishers.
Otto-Meyer, S., Krizman, J., White-Schwoch, T., & Kraus, N. (2018). Children with autism spectrum disorder have unstable neural responses to sound. Experimental Brain Research, 236(3), 733–743.
O’Connor, K. (2012). Auditory processing in autism spectrum disorder: a review. Neuroscience & Biobehavioral Reviews, 36(2), 836–854.
Patel, S. P., Kim, J. H., Larson, C. R., & Losh, M. (2019). Mechanisms of voice control related to prosody in autism spectrum disorder and first-degree relatives. Autism Research, 12(8), 1192–1210.
Paul, R., Augustyn, A., Klin, A., & Volkmar, F. R. (2005). Perception and production of prosody by speakers with autism spectrum disorders. Journal of Autism and Developmental Disorders, 35(2), 205–220.
Peppe, S., & McCann, J. (2003). Assessing intonation and prosody in children with atypical language development: the peps-c test and the revised version. Clinical Linguistics & Phonetics, 17(4–5), 345–354.
Peppe, S., McCann, J., Gibbon, F., O’Hare, A., & Rutherford, M. (2006). Assessing prosodic and pragmatic ability in children with high-functioning autism. Journal of Pragmatics, 38(10), 1776–1791.
Peretz, I., Cummings, S., & Dube, M.-P. (2007). The genetics of congenital amusia (tone deafness): a family-aggregation study. The American Journal of Human Genetics, 81(3), 582–588.
R Core Team. (2020). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rinker, T., Kohls, G., Richter, C., Maas, V., Schulz, E., & Schecker, M. (2007). Abnormal frequency discrimination in children with sli as indexed by mismatch negativity (mmn). Neuroscience Letters, 413(2), 99–104.
Roberts, T. P., Cannon, K. M., Tavabi, K., Blaskey, L., Khan, S. Y., Monroe, J. F., et al. (2011). Auditory magnetic mismatch field latency: a biomarker for language impairment in autism. Biological Psychiatry, 70(3), 263–269.
Russo, N., Nicol, T., Musacchia, G., & Kraus, N. (2004). Brainstem responses to speech syllables. Clinical Neurophysiology, 115(9), 2021–2030.
Russo, N., Skoe, E., Trommer, B., Nicol, T., Zecker, S., Bradlow, A., & Kraus, N. (2008). Deficient brainstem encoding of pitch in children with autism spectrum disorders. Clinical Neurophysiology, 119(8), 1720–1731.
Singh, L., & Fu, C. S. (2016). A new view of language development: the acquisition of lexical tone. Child Development, 87(3), 834–854.
Skoe, E., & Kraus, N. (2010). Auditory brainstem response to complex sounds: a tutorial. Ear and Hearing, 31(3), 302.
Skoe, E., Krizman, J., & Kraus, N. (2013). The impoverished brain: disparities in maternal education affect the neural response to sound. Journal of Neuroscience, 33(44), 17221–17231.
Song, J. H., Skoe, E., Wong, P. C., & Kraus, N. (2008). Plasticity in the adult human auditory brainstem following short-term linguistic training. Journal of Cognitive Neuroscience, 20(10), 1892–1902.
Tang, P., Xu Rattanasone, N., Yuen, I., & Demuth, K. (2017). Phonetic enhancement of mandarin vowels and tones: Infant-directed speech and lombard speech. The Journal of the Acoustical Society of America, 142(2), 493–503.
Tecoulesco, L., Skoe, E., & Naigles, L. R. (2020). Phonetic discrimination mediates the relationship between auditory brainstem response stability and syntactic performance. Brain and Language, 208, 104810.
Troyb, E., Knoch, K., and Barton, M. (2011). Phenomenology of ASD: definition, syndromes, and major features. The neuropsychology of autism, 9–34.
Tsou, B., Lee, T., Tung, P., Man, Y., Chan, A., To, C., & Chan, Y. (2006). Hong Kong Cantonese oral language assessment scale. Hong Kong: City University of Hong Kong.
Uwer, R., Albrecht, R., & Von Suchodoletz, W. (2002). Automatic processing of tones and speech stimuli in children with specific language impairment. Developmental Medicine and Child Neurology, 44(8), 527–532.
Voss, P., Thomas, M. E., Cisneros-Franco, J. M., & de Villers-Sidani, E. (2017). Dynamic brains and the changing rules of neuroplasticity: implications for learning and recovery. Frontiers in Psychology, 8, 1657.
Wang, X., Wang, S., Fan, Y., Huang, D., & Zhang, Y. (2017). Speech-specific categorical perception deficit in autism: an event-related potential study of lexical tone processing in Mandarin-speaking children. Scientific Reports, 7, 43254.
Wong, P. C., Ciocca, V., Chan, A. H., Ha, L. Y., Tan, L.-H., & Peretz, I. (2012). Effects of culture on musical pitch perception. PLoS One, 7(4), e33424.
Wong, P. C., & Diehl, R. L. (2003). Perceptual normalization for inter-and intratalker variation in Cantonese level tones. Journal of Speech, Language, and Hearing Research, 46(2), 413–421.
Wong, P. C., Kang, X., Wong, K. H., So, H.-C., Choy, K. W., & Geng, X. (2020). Aspm-lexical tone association in speakers of a tone language: direct evidence for the genetic-biasing hypothesis of language evolution. Science Advances, 6(22), eaba5090.
Wong, P. C., Skoe, E., Russo, N. M., Dees, T., & Kraus, N. (2007). Musical experience shapes human brainstem encoding of linguistic pitch patterns. Nature Neuroscience, 10(4), 420–422.
Xie, Z., Reetzke, R., & Chandrasekaran, B. (2018). Taking attention away from the auditory modality: context-dependent effects on early sensory representation of speech. Neuroscience, 384, 64–75.
Xie, Z., Reetzke, R., & Chandrasekaran, B. (2019). Machine learning approaches to analyze speech-evoked neurophysiological responses. Journal of Speech, Language, and Hearing Research, 62(3), 587–601.
Yip, M. (2002). Tone. Cambridge: Cambridge University Press.
Yu, L., Fan, Y., Deng, Z., Huang, D., Wang, S., & Zhang, Y. (2015). Pitch processing in tonal-language speaking children with autism: an event-related potential study. Journal of Autism and Developmental Disorders, 45(11), 3656–3667.
Zhang, J., Meng, Y., Wu, C., Xiang, Y.-T., & Yuan, Z. (2019). Non-speech and speech pitch perception among Cantonese-speaking children with autism spectrum disorder: an erp study. Neuroscience Letters, 703, 205–212.
Acknowledgements
We thank CUHK-NTU-WSU Joint Laboratory for Infant Research and CUHK-UU Joint Centre for Language, Mind and Brain for supporting our research. We also thank Gangyi Feng for his advice on Support Vector Machine. We would also like to thank families who participated in this research study.
Funding
This work is supported by funding from the Health and Medical Research Fund (HKSAR) [02130846], the University Grants Committee (HKSAR) (RGC/HSSPFS) [34000118], the Global Parent Child Resource Centre Limited, and Dr Stanley Ho Medical Development Foundation to P.W.
Author information
Authors and Affiliations
Contributions
PW designed the study; JK, JL, CT, and XK performed research; JL and XK analysed data; JL and PW wrote the paper; CT, JK, XK, and ML edited the paper and provided general comments on the study.
Corresponding author
Ethics declarations
Conflict of Interest
P.W. and C.T. declare that they are owners of two separate startup companies supported by a Hong Kong Government technology startup scheme. The research reported here is not associated with these two companies. The other authors declare no conflict of interests.
Ethical Approval
All procedures have been approved by The Joint Chinese University of Hong Kong—New Territories East Cluster Clinical Research Ethics Committee and are in accordance with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed Consent
Informed assent (from each child participant’s parent or legal guardian) or informed consent (from each adult participant) approved by The Joint Chinese University of Hong Kong—New Territories East Cluster Clinical Research Ethics Committee was obtained.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lau, J.C.Y., To, C.K.S., Kwan, J.S.K. et al. Lifelong Tone Language Experience does not Eliminate Deficits in Neural Encoding of Pitch in Autism Spectrum Disorder. J Autism Dev Disord 51, 3291–3310 (2021). https://doi.org/10.1007/s10803-020-04796-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-020-04796-7