The time-locked neurodynamics of semantic processing in autism spectrum disorder: an EEG study

Abstract

Language processing is often an area of difficulty in Autism Spectrum Disorder (ASD). Semantic processing-the ability to add meaning to a stimulus-is thought to be especially affected in ASD. However, the neurological origin of these deficits, both structurally and temporally, have yet to be discovered. To further previous behavioral findings on language differences in ASD, the present study used an implicit semantic priming paradigm and electroencephalography (EEG) to compare the level of theta coherence throughout semantic processing, between typically developing (TD) and ASD participants. Theta coherence is an indication of synchronous EEG oscillations and was of particular interest due to its previous links with semantic processing. Theta coherence was analyzed in response to semantically related or unrelated pairs of words and pictures across bilateral short, medium, and long electrode connections. We found significant results across a variety of conditions, but most notably, we observed reduced coherence for language stimuli in the ASD group at a left fronto-parietal connection from 100 to 300 ms. This replicates previous findings of underconnectivity in left fronto-parietal language networks in ASD. Critically, the early time window of this underconnectivity, from 100 to 300 ms, suggests that impaired semantic processing of language in ASD may arise during pre-semantic processing, during the initial communication between lower-level linguistic processing and higher-level semantic processing. Our results suggest that language processing functions are unique in ASD compared to TD, and that subjects with ASD might rely on a temporally different language processing loop altogether.

Keywords: Autism spectrum disorder; EEG coherence; Language; Semantic processing.

Fig. 1

Theoretical model of lexico-semantic difficulties in ASD. a) One possibility is that the language processing system is impaired; however, findings of intact lower-level linguistic processing rule out this scenario. b) Another option is that the semantic processing system is impaired; however, findings of intact visuo-semantic processing rule out this scenario. c) A third option is that the connections between the language and semantic systems are impaired, which we propose to test in the current study

Fig. 2

Examples of stimuli from the experimental paradigm. Participants were shown pairs of related or unrelated words and pictures on the outlined timeline. The catch stimuli included a string of capital consonant letter (word condition) or a smiley face (picture condition)

Fig. 3

Electrode montage showing the 12 electrode pairs used for coherence analyses. Red lines indicate short-distance connections (left hemisphere: F3-C3, C3-P3, and P3-O1; right hemisphere: F4-C4, C4-P4, and P4-O2); green lines indicate medium-distance connections (left hemisphere: F3-P3 and C3-O1; right hemisphere: F4-P4 and C4-O2); and blue lines indicate long-distance connections (left hemisphere: F3-O1; right hemisphere: F4-O2)

Fig. 4

Line graphs of theta coherence (averaged over all frequencies between 3 and 7.5 Hz) after the second stimulus at all intrahemispheric electrode pairs for each group and condition in the word modality. Shading represents the standard error of the mean.

Fig. 5

Line graphs of theta coherence (averaged over all frequencies between 3 and 7.5 Hz) after the second stimulus at all intrahemispheric electrode pairs for each group and condition in the picture modality. Shading represents the standard error of the mean

Fig. 6

Line graphs of theta coherence (averaged over all frequencies between 3 and 7.5 Hz) after the first stimulus at all intrahemispheric electrode pairs for each group in the word modality, averaged over related/unrelated conditions. Shading represents the standard error of the mean

Fig. 7

Line graphs of theta coherence (averaged over all frequencies between 3 and 7.5 Hz) after the first stimulus at all intrahemispheric electrode pairs for each group in the picture modality, averaged over related/unrelated conditions. Shading represents the standard error of the mean