Atypical low-frequency cortical encoding of speech identifies children with developmental dyslexia.

Slow cortical oscillations play a crucial role in processing the speech amplitude envelope, which is perceived atypically by children with developmental dyslexia. Here we use electroencephalography (EEG) recorded during natural speech listening to identify neural processing patterns involving slow oscillations that may characterize children with dyslexia. In a story listening paradigm, we find that atypical power dynamics and phase-amplitude coupling between delta and theta oscillations characterize dyslexic versus other child control groups (typically-developing controls, other language disorder controls). We further isolate EEG common spatial patterns (CSP) during speech listening across delta and theta oscillations that identify dyslexic children. A linear classifier using four delta-band CSP variables predicted dyslexia status (0.77 AUC). Crucially, these spatial patterns also identified children with dyslexia when applied to EEG measured during a rhythmic syllable processing task. This transfer effect (i.e., the ability to use neural features derived from a story listening task as input features to a classifier based on a rhythmic syllable task) is consistent with a core developmental deficit in neural processing of speech rhythm. The findings are suggestive of distinct atypical neurocognitive speech encoding mechanisms underlying dyslexia, which could be targeted by novel interventions.

Atypical beta-band effects in children with dyslexia in response to rhythmic audio-visual speech.

OBJECTIVE: Previous studies have reported atypical delta phase in children with dyslexia, and that delta phase modulates the amplitude of the beta-band response via delta-beta phase-amplitude coupling (PAC). Accordingly, the atypical delta-band effects in children with dyslexia may imply related atypical beta-band effects, particularly regarding delta-beta PAC. Our primary objective was to explore beta-band oscillations in children with and without dyslexia, to explore potentially atypical effects in the beta band in dyslexic children. METHODS: We collected EEG data during a rhythmic speech paradigm from 51 children (21 control; 30 dyslexia). We then assessed beta-band phase entrainment, beta-band angular velocity, beta-band power responses and delta-beta PAC. RESULTS: We found significant beta-band phase entrainment for control children but not for dyslexic children. Furthermore, children with dyslexia exhibited significantly faster beta-band angular velocity and significantly greater beta-band power. Delta-beta PAC was comparable in both groups. CONCLUSION: Atypical beta-band effects were observed in children with dyslexia. However, delta-beta PAC was comparable in both dyslexic and control children. SIGNIFICANCE: These findings offer further insights into the neurophysiological basis of atypical rhythmic speech processing by children with dyslexia, suggesting the involvement of a wide range of frequency bands.

Atypical speech production of multisyllabic words and phrases by children with developmental dyslexia.

The prevalent "core phonological deficit" model of dyslexia proposes that the reading and spelling difficulties characterizing affected children stem from prior developmental difficulties in processing speech sound structure, for example, perceiving and identifying syllable stress patterns, syllables, rhymes and phonemes. Yet spoken word production appears normal. This suggests an unexpected disconnect between speech input and speech output processes. Here we investigated the output side of this disconnect from a speech rhythm perspective by measuring the speech amplitude envelope (AE) of multisyllabic spoken phrases. The speech AE contains crucial information regarding stress patterns, speech rate, tonal contrasts and intonational information. We created a novel computerized speech copying task in which participants copied aloud familiar spoken targets like "Aladdin." Seventy-five children with and without dyslexia were tested, some of whom were also receiving an oral intervention designed to enhance multi-syllabic processing. Similarity of the child's productions to the target AE was computed using correlation and mutual information metrics. Similarity of pitch contour, another acoustic cue to speech rhythm, was used for control analyses. Children with dyslexia were significantly worse at producing the multi-syllabic targets as indexed by both similarity metrics for computing the AE. However, children with dyslexia were not different from control children in producing pitch contours. Accordingly, the spoken production of multisyllabic phrases by children with dyslexia is atypical regarding the AE. Children with dyslexia may not appear to listeners to exhibit speech production difficulties because their pitch contours are intact. RESEARCH HIGHLIGHTS: Speech production of syllable stress patterns is atypical in children with dyslexia. Children with dyslexia are significantly worse at producing the amplitude envelope of multi-syllabic targets compared to both age-matched and reading-level-matched control children. No group differences were found for pitch contour production between children with dyslexia and age-matched control children. It may be difficult to detect speech output problems in dyslexia as pitch contours are relatively accurate.

Neural responses to natural and enhanced speech edges in children with and without dyslexia.

Sensory-neural studies indicate that children with developmental dyslexia show impairments in processing acoustic speech envelope information. Prior studies suggest that this arises in part from reduced sensory sensitivity to amplitude rise times (ARTs or speech "edges") in the envelope, accompanied by less accurate neural encoding of low-frequency envelope information. Accordingly, enhancing these characteristics of the speech envelope may enhance neural speech processing in children with dyslexia. Here we applied an envelope modulation enhancement (EME) algorithm to a 10-min story read in child-directed speech (CDS), enhancing ARTs and also enhancing low-frequency envelope information. We compared neural speech processing (as measured using MEG) for the EME story with the same story read in natural CDS for 9-year-old children with and without dyslexia. The EME story affected neural processing in the power domain for children with dyslexia, particularly in the delta band (0.5-4 Hz) in the superior temporal gyrus. This may suggest that prolonged experience with EME speech could ameliorate some of the impairments shown in natural speech processing by children with dyslexia.

Decoding of speech information using EEG in children with dyslexia: Less accurate low-frequency representations of speech, not "Noisy" representations.

The amplitude envelope of speech carries crucial low-frequency acoustic information that assists linguistic decoding. The sensory-neural Temporal Sampling (TS) theory of developmental dyslexia proposes atypical encoding of speech envelope information < 10 Hz, leading to atypical phonological representations. Here a backward linear TRF model and story listening were employed to estimate the speech information encoded in the electroencephalogram in the canonical delta, theta and alpha bands by 9-year-old children with and without dyslexia. TRF decoding accuracy provided an estimate of how faithfully the children's brains encoded low-frequency envelope information. Between-group analyses showed that the children with dyslexia exhibited impaired reconstruction of speech information in the delta band. However, when the quality of speech encoding for each child was estimated using child-by-child decoding models, then the dyslexic children did not differ from controls. This suggests that children with dyslexia encode neither "noisy" nor "normal" representations of the speech signal, but different representations.

Atypical delta-band phase consistency and atypical preferred phase in children with dyslexia during neural entrainment to rhythmic audio-visual speech.

According to the sensory-neural Temporal Sampling theory of developmental dyslexia, neural sampling of auditory information at slow rates (<10 Hz, related to speech rhythm) is atypical in dyslexic individuals, particularly in the delta band (0.5-4 Hz). Here we examine the underlying neural mechanisms related to atypical sampling using a simple repetitive speech paradigm. Fifty-one children (21 control children [15M, 6F] and 30 children with dyslexia [16M, 14F]) aged 9 years with or without developmental dyslexia watched and listened as a 'talking head' repeated the syllable "ba" every 500 ms, while EEG was recorded. Occasionally a syllable was "out of time", with a temporal delay calibrated individually and adaptively for each child so that it was detected around 79.4% of the time by a button press. Phase consistency in the delta (rate of stimulus delivery), theta (speech-related) and alpha (control) bands was evaluated for each child and each group. Significant phase consistency was found for both groups in the delta and theta bands, demonstrating neural entrainment, but not the alpha band. However, the children with dyslexia showed a different preferred phase and significantly reduced phase consistency compared to control children, in the delta band only. Analysis of pre- and post-stimulus angular velocity of group preferred phases revealed that the children in the dyslexic group showed an atypical response in the delta band only. The delta-band pre-stimulus angular velocity (-130 ms to 0 ms) for the dyslexic group appeared to be significantly faster compared to the control group. It is concluded that neural responding to simple beat-based stimuli may provide a unique neural marker of developmental dyslexia. The automatic nature of this neural response may enable new tools for diagnosis, as well as opening new avenues for remediation.

Neural sampling of the speech signal at different timescales by children with dyslexia.

Phonological difficulties characterize individuals with dyslexia across languages. Currently debated is whether these difficulties arise from atypical neural sampling of (or entrainment to) auditory information in speech at slow rates (<10 Hz, related to speech rhythm), faster rates, or neither. MEG studies with adults suggest that atypical sampling in dyslexia affects faster modulations in the neurophysiological gamma band, related to phoneme-level representation. However, dyslexic adults have had years of reduced experience in converting graphemes to phonemes, which could itself cause atypical gamma-band activity. The present study was designed to identify specific linguistic timescales at which English children with dyslexia may show atypical entrainment. Adopting a developmental focus, we hypothesized that children with dyslexia would show atypical entrainment to the prosodic and syllable-level information that is exaggerated in infant-directed speech and carried primarily by amplitude modulations <10 Hz. MEG was recorded in a naturalistic story-listening paradigm. The modulation bands related to different types of linguistic information were derived directly from the speech materials, and lagged coherence at multiple temporal rates spanning 0.9-40 Hz was computed. Group differences in lagged speech-brain coherence between children with dyslexia and control children were most marked in neurophysiological bands corresponding to stress and syllable-level information (<5 Hz in our materials), and phoneme-level information (12-40 Hz). Functional connectivity analyses showed network differences between groups in both hemispheres, with dyslexic children showing significantly reduced global network efficiency. Global network efficiency correlated with dyslexic children's oral language development and with control children's reading development. These developmental data suggest that dyslexia is characterized by atypical neural sampling of auditory information at slower rates. They also throw new light on the nature of the gamma band temporal sampling differences reported in MEG dyslexia studies with adults.

Development of binaural temporal fine structure sensitivity in children.

The highest frequency for which the temporal fine structure (TFS) of a sinewave can be compared across ears varies between listeners with an upper limit of about 1400 Hz for young normal-hearing adults (YNHA). In this study, binaural TFS sensitivity was investigated for 63 typically developing children, aged 5 years, 6 months to 9 years, 4 months using the temporal fine structure-adaptive frequency (TFS-AF) test of Füllgrabe, Harland, Sek, and Moore [Int. J. Audiol. 56, 926-935 (2017)]. The test assesses the highest frequency at which an interaural phase difference (IPD) of ϕ° can be distinguished from an IPD of 0°. The values of ϕ were 30° and 180°. The starting frequency was 200 Hz. The thresholds for the children were significantly lower (worse) than the thresholds reported by Füllgrabe, Harland, Sek, and Moore [Int. J. Audiol. 56, 926-935 (2017)] for YNHA. For both values of ϕ, the median age at which children performed above chance level was significantly higher (p < 0.001) than for those who performed at chance. For the subgroup of 40 children who performed above chance for ϕ = 180°, the linear regression analyses showed that the thresholds for ϕ = 180° increased (improved) significantly with increasing age (p < 0.001) with adult-like thresholds predicted to be reached at 10 years, 2 months of age. The implications for spatial release from masking are discussed.