Journal of Autism and Developmental Disorders

, Volume 47, Issue 3, pp 795–812 | Cite as

Linguistic and Non-Linguistic Semantic Processing in Individuals with Autism Spectrum Disorders: An ERP Study

  • Emily L. CoderreEmail author
  • Mariya Chernenok
  • Barry Gordon
  • Kerry Ledoux
Original Paper


Individuals with autism spectrum disorders (ASD) experience difficulties with language, particularly higher-level functions like semantic integration. Yet some studies indicate that semantic processing of non-linguistic stimuli is not impaired, suggesting a language-specific deficit in semantic processing. Using a semantic priming task, we compared event-related potentials (ERPs) in response to lexico-semantic processing (written words) and visuo-semantic processing (pictures) in adults with ASD and adults with typical development (TD). The ASD group showed successful lexico-semantic and visuo-semantic processing, indicated by similar N400 effects between groups for word and picture stimuli. However, differences in N400 latency and topography in word conditions suggested different lexico-semantic processing mechanisms: an expectancy-based strategy for the TD group but a controlled post-lexical integration strategy for the ASD group.


Autism spectrum disorders Semantic processing ERP Language Pictures 



The authors would like to thank Nancy Grund for her help with editing and Joseph Dien, Ph.D. for helpful discussions and for his review of an early draft of this manuscript. This research was supported by the Therapeutic Cognitive Neuroscience Fund and the Benjamin and Adith Miller Family Endowment on Aging, Alzheimer’s, and Autism Research. Preliminary analyses of these data were presented at the 2015 meeting of the Cognitive Neuroscience Society in San Francisco, California.

Author Contributions

EC conceived of the study, participated in its design and coordination, collected data, performed the statistical analysis, interpreted the data, and drafted the manuscript. MC participated in the design and coordination of the study, collected data, and helped draft the manuscript. BG participated in the coordination of the study and helped draft the manuscript. KL participated in the design of the study and helped draft the manuscript. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.


  1. Anderson, J. S., Druzgal, T. J., Froehlich, A., DuBray, M. B., Lange, N., Alexander, A. L., et al. (2011). Decreased interhemispheric functional connectivity in autism. Cerebral Cortex, 21(5), 1134–1146.CrossRefPubMedGoogle Scholar
  2. APA. (2013). Diagnostic and statistical manual of mental disorders: DSM-5. Washington, DC: American Psychiatric Association.Google Scholar
  3. Barttfeld, P., Wicker, B., Cukier, S., Navarta, S., Lew, S., & Sigman, M. (2011). A big-world network in ASD: dynamical connectivity analysis reflects a deficit in long-range connections and an excess of short-range connections. Neuropsychologia, 49(2), 254–263.CrossRefPubMedGoogle Scholar
  4. Bookheimer, S. (2002). Functional MRI of language: New approaches to understanding the cortical organization of semantic processing. Annual Review of Neuroscience, 25, 151–188.CrossRefPubMedGoogle Scholar
  5. Braeutigam, S., Swithenby, S. J., & Bailey, A. J. (2008). Contextual integration the unusual way: A magnetoencephalographic study of responses to semantic violation in individuals with autism spectrum disorders. European Journal of Neuroscience, 27, 1026–1036.CrossRefPubMedGoogle Scholar
  6. Brock, J., Brown, C., Boucher, J., & Rippon, G. (2002). The temporal binding deficit hypothesis of autism. Development and Psychopathology, 14, 209–224.CrossRefPubMedGoogle Scholar
  7. Brouwer, H., Fitz, H., & Hoeks, J. (2012). Getting real about Semantic Illusions: Rethinking the functional role of the P600 in language comprehension. Brain Research, 1446, 127–143.CrossRefPubMedGoogle Scholar
  8. Brysbaert, M., & New, B. (2009). Moving beyond Kucera and Francis: A critical evaluation of current word frequency norms and the introduction of a new and improved word frequency measure for American English. Behavior Research Methods, 41(4), 977–990.CrossRefPubMedGoogle Scholar
  9. Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12(1), 1–47.CrossRefPubMedGoogle Scholar
  10. Catarino, A., Andrade, A., Churches, O., Wagner, A. P., Baron-Cohen, S., & Ring, H. (2013). Task-related functional connectivity in autism spectrum conditions: An EEG study using wavelet transform coherence. Molecular Autism, 4(1), 1.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chee, M. W., Weekes, B., Lee, K. M., Soon, C. S., Schreiber, A., Hoon, J. J., & Chee, M. (2000). Overlap and dissociation of semantic processing of Chinese characters, English words, and pictures: Evidence from fMRI. NeuroImage, 12(4), 392–403.CrossRefPubMedGoogle Scholar
  12. Cherkassky, V., Kana, R., Keller, T., & Just, M. (2006). Functional connectivity in a baseline resting-state network in autism. Neuroreport, 17(16), 1687–1690.CrossRefPubMedGoogle Scholar
  13. Coben, R., Clarke, A. R., Hudspeth, W., & Barry, R. J. (2008). EEG power and coherence in autistic spectrum disorder. Clinical Neurophysiology, 119(5), 1002–1009.CrossRefPubMedGoogle Scholar
  14. Dien, J., Franklin, M. S., & May, C. J. (2006). Is “Blank” a suitable neutral prime for event-related potential experiments? Brain and Language, 97, 91–101.CrossRefPubMedGoogle Scholar
  15. Dunn, M. A., & Bates, J. C. (2005). Developmental change in neutral processing of words by children with autism. Journal of Autism and Developmental Disorders, 35(3), 361–376.CrossRefPubMedGoogle Scholar
  16. Dunn, M. A., Gaughan, H. Jr., Kreuzer, J., & Kurtzberg, D. (1999). Electrophysiologic correlates of semantic classification in autistic and normal children. Developmental Neuropsychology, 16(1), 79–99.CrossRefGoogle Scholar
  17. Franklin, M. S., Dien, J., Neely, J. H., Huber, E., & Waterson, L. D. (2007). Semantic priming modulates the N400, N300, and N400RP. Clinical Neurophysiology, 118(5), 1053–1068.CrossRefPubMedGoogle Scholar
  18. Frishkoff, G. A. (2007). Hemispheric differences in strong versus weak semantic priming: Evidence from event-related brain potentials. Brain and Language, 100, 23–43.CrossRefPubMedGoogle Scholar
  19. Frishkoff, G. A., Perfetti, C. A., & Collins-Thompson, K. (2010). Lexical quality in the brain: ERP evidence for robust word learning from context. Developmental Neuropsychology, 35(4), 376–403.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Frishkoff, G. A., Tucker, D. M., Davey, C., & Scherg, M. (2004). Frontal and posterior sources of event-related potentials in semantic comprehension. Cognitive Brain Research, 20, 329–354.CrossRefPubMedGoogle Scholar
  21. Frith, U. (1989). Autism: Explaining the enigma. Oxford: Blackwell.Google Scholar
  22. Gaffrey, M. S., Kleinhans, N. M., Haist, F., Akshoomoff, N., Campbell, A., Courchesne, E., & Müller, R.-A. (2008). Atypical participation of visual cortex during word processing in autism: an fMRI study of semantic decision. Neuropsychologia, 45(8), 1672–1684.CrossRefGoogle Scholar
  23. Ganis, G., Kutas, M., & Sereno, M. I. (1996). The search for “common sense”: an electrophysiological study of the comprehension of words and pictures in reading. Journal of Cognitive Neuroscience, 8(2), 89–106.CrossRefPubMedGoogle Scholar
  24. Groen, W. B., Zwiers, M. P., van der Gaag, R.-J., & Buitelaar, J. K. (2008). The phenotype and neural correlates of language in autism: An integrative review. Neuroscience and Biobehavioral Reviews, 32, 1416–1425.CrossRefPubMedGoogle Scholar
  25. Groppe, D. M., Makeig, S., & Kutas, M. (2009). Identifying reliable independent components via split-half comparisons. Neuroimage, 45(4), 1199–1211.CrossRefPubMedGoogle Scholar
  26. Groppe, D. M., Urbach, T. P., & Kutas, M. (2011). Mass univariate analysis of event-related brain potentials/fields I: A critical tutorial review. Psychophysiology, 48, 1711–1725.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hagoort, P. (2005). On Broca, brain, and binding: a new framework. Trends in Cognitive Sciences, 9(9), 416–423.CrossRefPubMedGoogle Scholar
  28. Hamm, J. P., Johnson, B. W., & Kirk, I. J. (2002). Comparison of the N300 and N400 ERPs to picture stimuli in congruent and incongruent contexts. Clinical Neurophysiology, 113, 1339–1350.CrossRefPubMedGoogle Scholar
  29. Harris, G. J., Chabris, C. F., Clark, J., Urban, T., Aharon, I., Steele, S., et al. (2006). Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging. Brain and Cognition, 61, 54–68.CrossRefPubMedGoogle Scholar
  30. Jones, T. B., Bandettini, P. A., Kenworthy, L., Case, L. K., Milleville, S. C., Martin, A., & Birn, R. M. (2010). Sources of group differences in functional connectivity: An investigation applied to autism spectrum disorder. Neuroimage, 49(1), 401–414.CrossRefPubMedGoogle Scholar
  31. Just, M. A., Cherkassky, V. L., Keller, T. A., & Minshew, N. J. (2004). Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain: A Journal of Neurology, 127, 1811–1821.CrossRefGoogle Scholar
  32. Kamio, Y., & Toichi, M. (2000). Dual access to semantics in autism: is pictorial access superior to verbal access? Journal of Child Psychology and Psychiatry, 41(7), 859–867.CrossRefPubMedGoogle Scholar
  33. Kana, R. K., Keller, T. A., Cherkassky, V. L., Minshew, N. J., & Just, M. A. (2006). Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain: A Journal of Neurology, 129, 2484–2493.CrossRefGoogle Scholar
  34. Keil, A., Debener, S., Gratton, G., Junghöfer, M., Kappenman, E. S., Luck, S. J., et al. (2014). Committee report: Publication guidelines and recommendations for studies using electroencephalography and magnetoencephalography. Psychophysiology, 51(1), 1–21.CrossRefPubMedGoogle Scholar
  35. Koolen, S., Vissers, C. T. W. M., Egger, J. I. M., & Verhoeven, L. (2014). Monitoring in language perception in high-functioning adults with autism spectrum disorder: evidence from event-related potentials. Clinical Neurophysiology, 125(1), 108–123.CrossRefPubMedGoogle Scholar
  36. Kutas, M., & Federmeier, K. D. (2011). Thirty years and counting: Finding meaning in the N400 component of the event-related brain potential (ERP). Annual Review of Psychology, 62, 621–647.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kutas, M., & Hillyard, S. (1980). Reading senseless sentences: Brain potentials reflect semantic incongruity. Science, 207(4427), 203–205.CrossRefPubMedGoogle Scholar
  38. Lau, E. F., Holcomb, P. J., & Kuperberg, G. R. (2013). Dissociating N400 effects of prediction from association in single-word contexts. Journal of Cognitive Neuroscience, 25(3), 484–502.CrossRefPubMedGoogle Scholar
  39. Lau, E. F., Phillips, C., & Poeppel, D. (2008). A cortical network for semantics: (de)Constructing the N400. Nature Reviews Neuroscience, 9(12), 920–933.CrossRefPubMedGoogle Scholar
  40. Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: An open-source toolbox for the analysis of event-related potentials. Frontiers in Human Neuroscience, 8, 1–14.CrossRefGoogle Scholar
  41. Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule—generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRefPubMedGoogle Scholar
  42. Lord, C., Rutter, M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. L. (2012). Autism diagnostic observation schedule, second edition (ADOS-2) manual (Part 1): Modules 1–4. Torrance, CA: Western Psychological Services.Google Scholar
  43. Martin, A., & Chao, L. L. (2001). Semantic memory and the brain: Structure and processes. Current Opinion in Neurobiology, 11(2), 194–201.CrossRefPubMedGoogle Scholar
  44. McCleery, J. P., Ceponiene, R., Burner, K. M., Townsend, J., Kinnear, M., & Schreibman, L. (2010). Neural correlates of verbal and nonverbal semantic integration in children with autism spectrum disorders. Journal of Child Psychology and Psychiatry, 51(3), 277–286.CrossRefPubMedGoogle Scholar
  45. McPherson, W. B., & Holcomb, P. J. (1999). An electrophysiological investigation of semantic priming with pictures of real objects. Psychophysiology, 36, 53–65.CrossRefPubMedGoogle Scholar
  46. Murias, M., Webb, S., Greenson, J., & Dawson, G. (2007). Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biological Psychiatry, 62(3), 270–273.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nobre, A. C., & McCarthy, G. (1994). Language-related ERPs: Scalp distributions and modulation by word type and semantic priming. Journal of Cognitive Neuroscience, 6(3), 233–255.CrossRefPubMedGoogle Scholar
  48. O’Hare, A. J., Dien, J., Waterson, L. D., & Savage, C. R. (2008). Activation of the posterior cingulate by semantic priming: A co-registered ERP/fMRI study. Brain Research, 1189, 97–114.CrossRefPubMedGoogle Scholar
  49. Pijnacker, J., Geurts, B., van Lambalgen, M., Buitelaar, J., & Hagoort, P. (2010). Exceptions and anomalies: An ERP study on context sensitivity in autism. Neuropsychologia, 48(10), 2940–2951.CrossRefPubMedGoogle Scholar
  50. Price, C. J. (2010). The anatomy of language: a review of 100 fMRI studies published in 2009. Annals of the New York Academy of Sciences, 1191, 62–88.CrossRefPubMedGoogle Scholar
  51. Sahyoun, C. P., Belliveau, J. W., Soulières, I., Schwartz, S., & Mody, M. (2010). Neuroimaging of the functional and structural networks underlying visuospatial vs. linguistic reasoning in high-functioning autism. Neuropsychologia, 48(1), 86–95.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sahyoun, C. P., Soulières, I., Belliveau, J. W., Mottron, L., & Mody, M. (2009). Cognitive differences in pictorial reasoning between high-functioning autism and Asperger’s syndrome. Journal of Autism and Developmental Disorders, 39(7), 1014–1023.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Samson, F., Mottron, L., Soulières, I., & Zeffiro, T. A. (2012). Enhanced visual functioning in autism: An ALE meta-analysis. Human Brain Mapping, 33(7), 1553–1581.CrossRefPubMedGoogle Scholar
  54. Strandburg, R. J., Marsh, J. T., Brown, W. S., Asarnow, R. F., Guthrie, D., & Higa, J. (1993). Event-related potentials in high-functioning adult autistics: Linguistic and nonlinguistic visual information processing tasks. Neuropsychologia, 31(5), 413–434.CrossRefPubMedGoogle Scholar
  55. Tager-Flusberg, H., Paul, R., & Lord, C. (2005). Language and communication in autism. In F. Volkmar, R. Paul, A. Klin & D. Cohen (eds.), Handbook of autism and pervasive developmental disorders (3rd edn., pp. 335–364). New York: Wiley.Google Scholar
  56. van de Meerendonk, N., Kolk, H. H. J., Vissers, C. T. W. M., & Chwilla, D. J. (2010). Monitoring in language perception: Mild and strong conflicts elicit different ERP patterns. Journal of Cognitive Neuroscience, 22(1), 67–82.CrossRefPubMedGoogle Scholar
  57. Vandenberghe, R., Price, C. J., & Wise, R. (1996). Functional anatomy of a common semantic system for words and pictures. Nature, 383, 254–256.CrossRefPubMedGoogle Scholar
  58. Verbaten, M. N., Roelofs, J. W., van Engeland, H., Kenemans, J. K., & Slangen, J. L. (1991). Abnormal visual event-related potentials of autistic children. Journal of Autism and Developmental Disorders, 21(4), 449–470.CrossRefPubMedGoogle Scholar
  59. West, W. C., & Holcomb, P. J. (2002). Event-related potentials during discourse-level semantic integration of complex pictures. Cognitive Brain Research, 13, 363–375.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Emily L. Coderre
    • 1
    Email author
  • Mariya Chernenok
    • 1
    • 2
  • Barry Gordon
    • 1
    • 3
  • Kerry Ledoux
    • 1
  1. 1.Division of Cognitive Neurology/Neuropsychology, Department of NeurologyThe Johns Hopkins University School of MedicineBaltimoreUSA
  2. 2.Center for Mind and BrainUniversity of California, DavisDavisUSA
  3. 3.Department of Cognitive ScienceThe Johns Hopkins UniversityBaltimoreUSA

Personalised recommendations