Atypical MEG inter-subject correlation during listening to continuous natural speech in dyslexia

Abstract

Listening to speech elicits brain activity time-locked to the speech sounds. This so-called neural entrainment to speech was found to be atypical in dyslexia, a reading impairment associated with neural speech processing deficits. We hypothesized that the brain responses of dyslexic vs. normal readers to real-life speech would be different, and thus the strength of inter-subject correlation (ISC) would differ from that of typical readers and be reflected in reading-related measures. We recorded magnetoencephalograms (MEG) of 23 dyslexic and 21 typically-reading adults during listening to ~10 ​min of natural Finnish speech consisting of excerpts from radio news, a podcast, a self-recorded audiobook chapter and small talk. The amplitude envelopes of band-pass-filtered MEG source signals were correlated between subjects in a cortically-constrained source space in six frequency bands. The resulting ISCs of dyslexic and typical readers were compared with a permutation-based t-test. Neuropsychological measures of phonological processing, technical reading, and working memory were correlated with the ISCs utilizing the Mantel test. During listening to speech, ISCs were mainly reduced in dyslexic compared to typical readers in delta (0.5–4 ​Hz) and high gamma (55–90 ​Hz) frequency bands. In the theta (4–8 ​Hz), beta (12–25 ​Hz), and low gamma (25–45 ​Hz) bands, dyslexics had enhanced ISCs to speech compared to controls. Furthermore, we found that ISCs across both groups were associated with phonological processing, technical reading, and working memory. The atypical ISCs to natural speech in dyslexics supports the temporal sampling deficit theory of dyslexia. It also suggests over-synchronization to phoneme-rate information in speech, which could indicate more effort-demanding sampling of phonemes from speech in dyslexia. These irregularities in parsing speech are likely some of the complex neural factors contributing to dyslexia. The associations between neural coupling and reading-related skills further support this notion.