Top

Journal of Autism and Developmental Disorders

Gepubliceerd in:

20-11-2020 | Original Paper

Lifelong Tone Language Experience does not Eliminate Deficits in Neural Encoding of Pitch in Autism Spectrum Disorder

Auteurs: Joseph C. Y. Lau, Carol K. S. To, Judy S. K. Kwan, Xin Kang, Molly Losh, Patrick C. M. Wong

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 9/2021

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.

vorige artikel A Pilot Study of Responses to Interparental Conflict in Children with Autism Spectrum Disorder

volgende artikel ‘At the End of the Day, It’s Love’: An Exploration of Relationships in Neurodiverse Couples

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.CrossRef

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.PubMedCrossRef

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.CrossRefPubMed

Bishop, D. V. (2010). Overlaps between autism and language impairment: phenomimicry or shared etiology? Behavior Genetics, 40(5), 618–629.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Chandrasekaran, B., & Kraus, N. (2010). The scalp-recorded brainstem response to speech: neural origins and plasticity. Psychophysiology, 47(2), 236–246.PubMedCrossRef

Chandrasekaran, B., Skoe, E., & Kraus, N. (2014). An integrative model of subcortical auditory plasticity. Brain Topography, 27(4), 539–552.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.CrossRef

Ciocca, V., & Lui, J. (2003). The development of the perception of Cantonese lexical tones. Journal of Multilingual Communication Disorders, 1(2), 141–147.CrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.CrossRef

Heaton, P. (2003). Pitch memory, labelling and disembedding in autism. Journal of Child Psychology and Psychiatry, 44(4), 543–551.PubMedCrossRef

Heaton, P. (2005). Interval and contour processing in autism. Journal of Autism and Developmental Disorders, 35(6), 787.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

Ingvalson, E. M., & Wong, P. (2013). Training to improve language outcomes in cochlear implant recipients. Frontiers in Psychology, 4, 263.PubMedPubMedCentralCrossRef

Jarvinen-Pasley, A., & Heaton, P. (2007). Evidence for reduced domain-specificity in auditory processing in autism. Developmental Science, 10(6), 786–793.PubMedCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Krizman, J., Bonacina, S., & Kraus, N. (2019). Sex differences in subcortical auditory processing emerge across development. Hearing Research, 380, 166–174.PubMedCrossRef

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.PubMedCrossRef

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.CrossRefPubMed

Lenth, R. V. (2016). Least-squares means: The R package lsmeans. Journal of Statistical Software, 69(1), 1–33.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.CrossRef

Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: an open-source toolbox for the analysis of eventrelated potentials. Frontiers in Human Neuroscience, 8, 213.PubMedPubMedCentralCrossRef

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.CrossRef

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.PubMedPubMedCentralCrossRef

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.CrossRef

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.PubMedPubMedCentralCrossRef

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.CrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.CrossRef

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.CrossRef

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.PubMedCrossRef

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.CrossRefPubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

O’Connor, K. (2012). Auditory processing in autism spectrum disorder: a review. Neuroscience & Biobehavioral Reviews, 36(2), 836–854.CrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.CrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

Russo, N., Nicol, T., Musacchia, G., & Kraus, N. (2004). Brainstem responses to speech syllables. Clinical Neurophysiology, 115(9), 2021–2030.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

Singh, L., & Fu, C. S. (2016). A new view of language development: the acquisition of lexical tone. Child Development, 87(3), 834–854.PubMedCrossRef

Skoe, E., & Kraus, N. (2010). Auditory brainstem response to complex sounds: a tutorial. Ear and Hearing, 31(3), 302.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

Yip, M. (2002). Tone. Cambridge: Cambridge University Press.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Titel: Lifelong Tone Language Experience does not Eliminate Deficits in Neural Encoding of Pitch in Autism Spectrum Disorder
Auteurs: Joseph C. Y. Lau
Carol K. S. To
Judy S. K. Kwan
Xin Kang
Molly Losh
Patrick C. M. Wong
Publicatiedatum: 20-11-2020
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 9/2021
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-020-04796-7

Bohn Stafleu van Loghum

Deel dit onderdeel of sectie (kopieer de link)

Abstract

Log in om toegang te krijgen

Andere artikelen Uitgave 9/2021

Brief Report: Social Behavior and Special Interests in the Stigmatization of Autistic College Students

Risk for Premature Mortality and Intentional Self-harm in Autism Spectrum Disorders

Observed Social Emotional Behavior at 22 Months Predicts a Later ASD Diagnosis in High-Risk Siblings

An Investigation of Functional Communication Training and Schedule Thinning Using a Multiple Schedule on Elopement to Access Stereotypy

Brief Report: Classification of Autistic Traits According to Brain Activity Recoded by fNIRS Using ε-Complexity Coefficients

Assessing Video Enhanced Activity Schedules to Teach Social Skills to Children with Autism Spectrum Disorder