Atypical brain-to-brain synchronization 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 neural responses of dyslexic readers to real-life speech would be atypically synchronized compared to typical readers, and that the strength of brain-to-brain synchronization would 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 the cortically-constrained source space in six frequency bands. The resulting inter-subject correlations (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 reduced in dyslexic compared to typical readers in delta (0.5–4 Hz), alpha (8–12 Hz), and high gamma (55–90 Hz) frequency bands. In theta (4–8 Hz), beta (12–25 Hz), and low gamma (25–45 Hz) frequency bands, dyslexics had mainly enhanced ISC 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 brain-to-brain synchronization 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 be the reason for less accurate sampling of phonemes from speech in dyslexia. These irregularities in parsing speech are likely part of the complex neural factors contributing to dyslexia. The associations between neural coupling and reading-related skills further support this notion.

Declarations of Interest

None.

Research Highlights

• Brain-to-brain synchronization of dyslexics was atypical while listening to speech.

• Compared to typical readers, both stronger and weaker synchronization was found.

• Reading-related measures correlated with the strength of synchronization.