Journal of Autism and Developmental Disorders

, Volume 47, Issue 10, pp 3125–3138 | Cite as

Differences in Neural Correlates of Speech Perception in 3 Month Olds at High and Low Risk for Autism Spectrum Disorder

  • Laura A. Edwards
  • Jennifer B. Wagner
  • Helen Tager-Flusberg
  • Charles A. Nelson
Original Paper

Abstract

In this study, we investigated neural precursors of language acquisition as potential endophenotypes of autism spectrum disorder (ASD) in 3-month-old infants at high and low familial ASD risk. Infants were imaged using functional near-infrared spectroscopy while they listened to auditory stimuli containing syllable repetitions; their neural responses were analyzed over left and right temporal regions. While female low risk infants showed initial neural activation that decreased over exposure to repetition-based stimuli, potentially indicating a habituation response to repetition in speech, female high risk infants showed no changes in neural activity over exposure. This finding may indicate a potential neural endophenotype of language development or ASD specific to females at risk for the disorder.

Keywords

Autism spectrum disorders Near infrared spectroscopy Speech processing Infancy Endophenotype Language 

Supplementary material

10803_2017_3222_MOESM1_ESM.docx (228 kb)
Supplementary material 1 (DOCX 228 KB)

References

  1. American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders: DSM-5. Washington, D.C: American Psychiatric Association.CrossRefGoogle Scholar
  2. Baio, J., 010 Principal, et al. (2014). Prevalence of autism spectrum disorder among children aged 8 years-autism and developmental disabilities monitoring network, 11 sites, United States, 2010. Morbidity and Mortality Weekly Report. Surveillance Summaries (Washington, DC: 2002), 63(2), 1.Google Scholar
  3. Bauer, D. J., Goldfield, B. A., & Reznick, J. S. (2002). Alternative approaches to analyzing individual differences in the rate of early vocabulary development. Applied Psycholinguistics, doi:10.1017/S0142716402003016.Google Scholar
  4. Boddaert, N., Belin, P., Chabane, N., Poline, J.-B., Barthélémy, C., Mouren-Simeoni, M.-C., … Zilbovicius, M. (2003). Perception of complex sounds: abnormal pattern of cortical activation in autism. The American Journal of Psychiatry, 160(11), 2057–2060.CrossRefPubMedGoogle Scholar
  5. Bornstein, M. H., Hahn, C.-S., & Haynes, O. M. (2004). Specific and general language performance across early childhood: Stability and gender considerations. First Language, 24(3), 267–304. doi:10.1177/0142723704045681.CrossRefGoogle Scholar
  6. Bosl, W., Tierney, A., Tager-Flusberg, H., & Nelson, C. (2011). EEG complexity as a biomarker for autism spectrum disorder risk. BMC Medicine, 9, 18. doi:10.1186/1741-7015-9-18.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Byers-Heinlein, K., & Werker, J. F. (2013). Lexicon structure and the disambiguation of novel words: Evidence from bilingual infants. Cognition, 128(3), 407–416. doi:10.1016/j.cognition.2013.05.010.CrossRefPubMedGoogle Scholar
  8. Cohen, J. (1969). Statistical power analysis for the behavioral sciences. Academic Press.Google Scholar
  9. De Giacomo, A., & Fombonne, E. (1998). Parental recognition of developmental abnormalities in autism. European Child & Adolescent Psychiatry, 7(3), 131–136.CrossRefGoogle Scholar
  10. Devor, A., Ulbert, I., Dunn, A. K., Narayanan, S. N., Jones, S. R., Andermann, M. L., … Dale, A. M. (2005). Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. In Proceedings of the National Academy of Sciences of the United States of America, 102(10), 3822–3827.CrossRefGoogle Scholar
  11. Elsabbagh, M., & Johnson, M. H. (2010). Getting answers from babies about autism. Trends in Cognitive Sciences, 14(2), 81–87. doi:10.1016/j.tics.2009.12.005.CrossRefPubMedGoogle Scholar
  12. Elsabbagh, M., Volein, A., Csibra, G., Holmboe, K., Garwood, H., Tucker, L., … Johnson, M. H. (2009). Neural correlates of eye gaze processing in the infant broader autism phenotype. Biological Psychiatry, 65(1), 31–38. doi:10.1016/j.biopsych.2008.09.034.CrossRefPubMedGoogle Scholar
  13. Emberson, L. L., Cannon, G., Palmeri, H., Richards, J. E., & Aslin, R. N. (2017). Using fNIRS to examine occipital and temporal responses to stimulus repetition in young infants: Evidence of selective frontal cortex involvement. Developmental Cognitive Neuroscience, 23, 26–38. doi:10.1016/j.dcn.2016.11.002.CrossRefPubMedGoogle Scholar
  14. Eriksson, M., Marschik, P. B., Tulviste, T., Almgren, M., Pérez Pereira, M., Wehberg, S., … Gallego, C. (2012). Differences between girls and boys in emerging language skills: Evidence from 10 language communities. The British Journal of Developmental Psychology, 30(Pt 2), 326–343. doi:10.1111/j.2044-835X.2011.02042.x.CrossRefPubMedGoogle Scholar
  15. Eyler, L. T., Pierce, K., & Courchesne, E. (2012). A failure of left temporal cortex to specialize for language is an early emerging and fundamental property of autism. Brain: A Journal of Neurology, 135(3), 949–960. doi:10.1093/brain/awr364.CrossRefGoogle Scholar
  16. Fantz, R. L. (1964). Visual experience in infants: Decreased attention to familiar patterns relative to novel ones. Science, 146(3644), 668–670.CrossRefPubMedGoogle Scholar
  17. Fenson, L., Marchman, V. A., Thal, D. J., Dale, P. S., Reznick, J. S., & Bates, E. (2007). MacArthur-Bates communicative development inventories: User’s guide and technical manual (2nd ed.). Baltimore, MD: Brookes.Google Scholar
  18. Flagg, E. J., Cardy, J. E. O., Roberts, W., & Roberts, T. P. L. (2005). Language lateralization development in children with autism: Insights from the late field magnetoencephalogram. Neuroscience Letters, 386(2), 82–87. doi:10.1016/j.neulet.2005.05.037.CrossRefPubMedGoogle Scholar
  19. Fox, S. E., Wagner, J. B., Shrock, C. L., Tager-Flusberg, H., & Nelson, C. A. (2013). Neural processing of facial identity and emotion in infants at high-risk for autism spectrum disorders. Frontiers in Human Neuroscience, 7, 89. doi:10.3389/fnhum.2013.00089.PubMedPubMedCentralGoogle Scholar
  20. Gabard-Durnam, L., Tierney, A. L., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. A. (2015). Alpha asymmetry in infants at risk for autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(2), 473–480. doi:10.1007/s10803-013-1926-4.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gervain, J., Macagno, F., Cogoi, S., Peña, M., & Mehler, J. (2008). The neonate brain detects speech structure. Proceedings of the National Academy of Sciences of the United States of America, 105(37), 14222–14227.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gleason, J. B., & Ely, R. (2002). Gender differences in language development. Biology, Society, and Behavior: The Development of Sex Differences in Cognition, 21, 127–154.Google Scholar
  23. Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: Etymology and strategic intentions. American Journal of Psychiatry, 160(4), 636–645.CrossRefPubMedGoogle Scholar
  24. Grill-Spector, K., Henson, R., & Martin, A. (2006). Repetition and the brain: neural models of stimulus-specific effects. Trends in Cognitive Sciences, 10(1), 14–23. doi:10.1016/j.tics.2005.11.006.CrossRefPubMedGoogle Scholar
  25. Guiraud, J. A., Kushnerenko, E., Tomalski, P., Davies, K., Ribeiro, H., Johnson, M. H., & BASIS Team. (2011). Differential habituation to repeated sounds in infants at high risk for autism. Neuroreport, 22(16), 845–849. doi:10.1097/WNR.0b013e32834c0bec.PubMedGoogle Scholar
  26. Halladay, A. K., Bishop, S., Constantino, J. N., Daniels, A. M., Koenig, K., Palmer, K., … Szatmari, P. (2015). Sex and gender differences in autism spectrum disorder: summarizing evidence gaps and identifying emerging areas of priority. Molecular Autism. doi:10.1186/s13229-015-0019-y.PubMedPubMedCentralGoogle Scholar
  27. Huppert, T. J., Diamond, S. G., Franceschini, M. A., & Boas, D. A. (2009). HomER: A review of time-series analysis methods for near-infrared spectroscopy of the brain. Applied Optics, 48(10), D280–D298.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Iverson, J. M. (2010). Developing language in a developing body: the relationship between motor development and language development. Journal of Child Language, 37(2), 229–261. doi:10.1017/S0305000909990432.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kameyama, M., Fukuda, M., Uehara, T., & Mikuni, M. (2004). Sex and age dependencies of cerebral blood volume changes during cognitive activation: a multichannel near-infrared spectroscopy study. NeuroImage, 22(4), 1715–1721.CrossRefPubMedGoogle Scholar
  30. Keehn, B., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. A. (2015). Atypical hemispheric specialization for faces in infants at risk for autism spectrum disorder. Autism Research, 8(2), 187–198.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Keehn, B., Wagner, J. B., Tager-Flusberg, H., & Nelson, C. A. (2013). Functional connectivity in the first year of life in infants at-risk for autism: a preliminary near-infrared spectroscopy study. Frontiers in Human Neuroscience, 7, 444. doi:10.3389/fnhum.2013.00444.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Key, A. P. F., & Stone, W. L. (2012). Same but different: 9-month-old infants at average and high risk for autism look at the same facial features but process them using different brain mechanisms. Autism Research: Official Journal of the International Society for Autism Research, 5(4), 253–266. doi:10.1002/aur.1231.CrossRefGoogle Scholar
  33. Kleinhans, N. M., Müller, R.-A., Cohen, D. N., & Courchesne, E. (2008). Atypical functional lateralization of language in autism spectrum disorders. Brain Research, 1221, 115–125. doi:10.1016/j.brainres.2008.04.080.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Knaus, T. A., Silver, A. M., Kennedy, M., Lindgren, K. A., Dominick, K. C., Siegel, J., & Tager-Flusberg, H. (2010). Language laterality in autism spectrum disorder and typical controls: A functional, volumetric, and diffusion tensor MRI study. Brain and Language, 112(2), 113–120. doi:10.1016/j.bandl.2009.11.005.CrossRefPubMedGoogle Scholar
  35. Kuhl, P. K. (2004). Early language acquisition: Cracking the speech code. Nature Reviews Neuroscience, 5(11), 831–843. doi:10.1038/nrn1533.CrossRefPubMedGoogle Scholar
  36. Lai, M.-C., Lombardo, M. V., Pasco, G., Ruigrok, A. N. V., Wheelwright, S. J., Sadek, S. A., … Baron-Cohen, S. (2011). A behavioral comparison of male and female adults with high functioning autism spectrum conditions. PLoS ONE. doi:10.1371/journal.pone.0020835.Google Scholar
  37. Little, V. M., Thomas, D. G., & Letterman, M. R. (1999). Single-trial analyses of developmental trends in infant auditory event-related potentials. Developmental Neuropsychology, 16(3), 455–478.CrossRefGoogle Scholar
  38. Lloyd-Fox, S., Blasi, A., Elwell, C. E., Charman, T., Murphy, D., & Johnson, M. H. (2013). Reduced neural sensitivity to social stimuli in infants at risk for autism. Proceedings of Royal Society B, 280(1758), 20123026. doi:10.1098/rspb.2012.3026.
  39. Lombardo, M. V., Pierce, K., Eyler, L. T., Carter Barnes, C., Ahrens-Barbeau, C., Solso, S., … Courchesne, E. (2015). Different functional neural substrates for good and poor language outcome in autism. Neuron, 86(2), 567–577. doi:10.1016/j.neuron.2015.03.023.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Luyster, R. J., Powell, C., Tager-Flusberg, H., & Nelson, C. A. (2014). Neural measures of social attention across the first years of life: characterizing typical development and markers of autism risk. Developmental Cognitive Neuroscience, 8, 131–143. doi:10.1016/j.dcn.2013.09.006.CrossRefPubMedGoogle Scholar
  41. Marcus, G. F., Vijayan, S., Rao, S. B., & Vishton, P. M. (1999). Rule learning by seven-month-old infants. Science, 283(5398), 77–80. doi:10.1126/science.283.5398.77.CrossRefPubMedGoogle Scholar
  42. McCleery, J. P., Akshoomoff, N., Dobkins, K. R., & Carver, L. J. (2009). Atypical face versus object processing and hemispheric asymmetries in 10-month-old infants at risk for autism. Biological Psychiatry, 66(10), 950–957. doi:10.1016/j.biopsych.2009.07.031.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Messinger, D., Young, G. S., Ozonoff, S., Dobkins, K., Carter, A., Zwaigenbaum, L., … Sigman, M. (2013). Beyond autism: A baby siblings research consortium study of high-risk children at three years of age. Journal of the American Academy of Child and Adolescent Psychiatry, 52(3), 300–308.e1. doi:10.1016/j.jaac.2012.12.011.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mullen, E. M. (1995). Mullen scales of early learning (AGS ed.). Circle Pines, MN: American Guidance Service Inc.Google Scholar
  45. Newschaffer, C. J., Croen, L. A., Daniels, J., Giarelli, E., Grether, J. K., Levy, S. E., et al. (2007). The epidemiology of autism spectrum disorders*. Annual Review of Public Health, 28, 235–258.CrossRefPubMedGoogle Scholar
  46. Okamoto, M., Dan, H., Sakamoto, K., Takeo, K., Shimizu, K., Kohno, S., … Dan, I. (2004). Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping. NeuroImage, 21(1), 99–111.CrossRefPubMedGoogle Scholar
  47. Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., … Stone, W. L. (2011). Recurrence risk for autism spectrum disorders: a Baby Siblings Research Consortium study. Pediatrics, 128(3), e488–e495. doi:10.1542/peds.2010-2825.PubMedPubMedCentralGoogle Scholar
  48. Parke, R., & Gauvain, M. (2008). Child psychology: a contemporary view point (7 ed.). Boston: McGraw-Hill Education.Google Scholar
  49. Peña, M., Maki, A., Kovacić, D., Dehaene-Lambertz, G., Koizumi, H., Bouquet, F., & Mehler, J. (2003). Sounds and silence: An optical topography study of language recognition at birth. Proceedings of the National Academy of Sciences of the United States of America, 100(20), 11702–11705. doi:10.1073/pnas.1934290100.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Perani, D., Saccuman, M. C., Scifo, P., Anwander, A., Spada, D., Baldoli, C., … Friederici, A. D. (2011). Neural language networks at birth. Proceedings of the National Academy of Sciences of the United States of America, 108(38), 16056–16061. doi:10.1073/pnas.1102991108.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Righi, G., Tierney, A. L., Tager-Flusberg, H., & Nelson, C. A. (2014). Functional connectivity in the first year of life in infants at risk for autism spectrum disorder: An EEG study. PLoS ONE, 9(8), e105176. doi:10.1371/journal.pone.0105176.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Seery, A., Tager-Flusberg, H., & Nelson, C. A. (2014). Event-related potentials to repeated speech in 9-month-old infants at risk for autism spectrum disorder. Journal of Neurodevelopmental Disorders, 6(1), 43. doi:10.1186/1866-1955-6-43.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Seery, A. M., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. A. (2013). Atypical lateralization of ERP response to native and non-native speech in infants at risk for autism spectrum disorder. Developmental Cognitive Neuroscience, 5, 10–24. doi:10.1016/j.dcn.2012.11.007.CrossRefPubMedGoogle Scholar
  54. Sinha, P., Kjelgaard, M. M., Gandhi, T. K., Tsourides, K., Cardinaux, A. L., Pantazis, D., … Held, R. M. (2014). Autism as a disorder of prediction. Proceedings of the National Academy of Sciences USA, 111(42), 15220–15225. doi:10.1073/pnas.1416797111.CrossRefGoogle Scholar
  55. Sommerville, J. A., Woodward, A. L., & Needham, A. (2005). Action experience alters 3-month-old infants’ perception of others’ actions. Cognition, 96, 1. doi:10.1016/j.cognition.2004.07.004.CrossRefGoogle Scholar
  56. Tager-Flusberg, H. (2010). The origins of social impairments in autism spectrum disorder: Studies of infants at risk. Neural Networks, 23(8–9), 1072–1076. doi:10.1016/j.neunet.2010.07.008.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Thomas, D. G., & Lykins, M. S. (1995). Event-related potential measures of 24-hour retention in 5-month-old infants. Developmental Psychology, 31(6), 946.CrossRefGoogle Scholar
  58. Tierney, A. L., Gabard-Durnam, L., Vogel-Farley, V., Tager-Flusberg, H., & Nelson, C. A. (2012). Developmental trajectories of resting EEG power: An endophenotype of autism spectrum disorder. PLoS ONE, 7(6), e39127. doi:10.1371/journal.pone.0039127.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tong, Y., & Frederick, B. D. (2010). Time lag dependent multimodal processing of concurrent fMRI and near-infrared spectroscopy (NIRS) data suggests a global circulatory origin for low-frequency oscillation signals in human brain. Neuroimage, 53, 553–564. doi:10.1016/j.neuroimage.2010.06.049.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Turk-Browne, N. B., Scholl, B. J., & Chun, M. M. (2008). Babies and brains: habituation in infant cognition and functional neuroimaging. Frontiers in Human Neuroscience. doi:10.3389/neuro.09.016.2008.PubMedPubMedCentralGoogle Scholar
  61. Vander Maelen, A. L., Strauss, M. E., & Starr, R. H. (1975). Influence of obstetric medication on auditory habituation in the newborn. Developmental Psychology, 11(6), 711–714. doi:10.1037/0012-1649.11.6.711.CrossRefGoogle Scholar
  62. Vannasing, P., Florea, O., González-Frankenberger, B., Tremblay, J., Paquette, N., Safi, D., … Gallagher, A. (2016). Distinct hemispheric specializations for native and non-native languages in one-day-old newborns identified by fNIRS. Neuropsychologia, 84, 63–69. doi:10.1016/j.neuropsychologia.2016.01.038.CrossRefPubMedGoogle Scholar
  63. Viding, E., & Blakemore, S.-J. (2007). Endophenotype approach to developmental psychopathology: Implications for autism research. Behavior Genetics, 37(1), 51–60. doi:10.1007/s10519-006-9105-4.CrossRefPubMedGoogle Scholar
  64. Wagner, J. B., Fox, S. E., Tager-Flusberg, H., & Nelson, C. A. (2011). Neural processing of repetition and non-repetition grammars in 7- and 9-month-old infants. Frontiers in Psychology, 2, 168. doi:10.3389/fpsyg.2011.00168.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wan, C. Y., Marchina, S., Norton, A., & Schlaug, G. (2012). Atypical hemispheric asymmetry in the arcuate fasciculus of completely nonverbal children with autism. Annals of the New York Academy of Sciences, 1252(1), 332–337. doi:10.1111/j.1749-6632.2012.06446.x.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Watanabe, A., & Kato, T. (2004). Cerebrovascular response to cognitive tasks in patients with schizophrenia measured by near-infrared spectroscopy. Schizophrenia Bulletin, 30(2), 435–444.CrossRefPubMedGoogle Scholar
  67. Wetherby, A., Woods, J., Allen, L., Cleary, J., Dickinson, H., & Lord, C. (2004). Early indicators of autism spectrum disorders in the second year of life. Journal of Autism & Developmental Disorders, 34(5), 473–493.CrossRefGoogle Scholar
  68. Wolff, J. J., Gerig, G., Lewis, J. D., Soda, T., Styner, M. A., Vachet, C., … IBIS Network. (2015). Altered corpus callosum morphology associated with autism over the first 2 years of life. Brain: A Journal of Neurology, 138(Pt 7), 2046–2058. doi:10.1093/brain/awv118.CrossRefGoogle Scholar
  69. Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., & Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience, 23(2–3), 143–152. doi:10.1016/j.ijdevneu.2004.05.001.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Laura A. Edwards
    • 1
    • 4
    • 5
  • Jennifer B. Wagner
    • 2
  • Helen Tager-Flusberg
    • 3
  • Charles A. Nelson
    • 4
    • 5
  1. 1.Marcus Autism CenterAtlantaUSA
  2. 2.College of Staten Island, City University of New YorkNew YorkUSA
  3. 3.Boston UniversityBostonUSA
  4. 4.Boston Children’s HospitalHarvard UniversityBostonUSA
  5. 5.Harvard Graduate School of EducationCambridgeUSA

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