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....
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-06-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922002063 |
| _version_ | 1818320880802988032 |
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| author | Kanad Mandke Sheila Flanagan Annabel Macfarlane Fiona Gabrielczyk Angela Wilson Joachim Gross Usha Goswami |
| author_facet | Kanad Mandke Sheila Flanagan Annabel Macfarlane Fiona Gabrielczyk Angela Wilson Joachim Gross Usha Goswami |
| author_sort | Kanad Mandke |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-13T10:32:02Z |
| format | Article |
| id | doaj.art-f207b9b9da574e57a53fa5b2037cb3bc |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-13T10:32:02Z |
| publishDate | 2022-06-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-f207b9b9da574e57a53fa5b2037cb3bc2022-12-21T23:50:50ZengElsevierNeuroImage1095-95722022-06-01253119077Neural sampling of the speech signal at different timescales by children with dyslexiaKanad Mandke0Sheila Flanagan1Annabel Macfarlane2Fiona Gabrielczyk3Angela Wilson4Joachim Gross5Usha Goswami6Centre for Neuroscience in Education, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom; Corresponding author.Centre for Neuroscience in Education, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United KingdomCentre for Neuroscience in Education, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United KingdomCentre for Neuroscience in Education, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United KingdomCentre for Neuroscience in Education, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United KingdomInstitute for Biomagnetism and Biosignal Analysis, University of Münster, Münster, GermanyCentre for Neuroscience in Education, Department of Psychology, University of Cambridge, Cambridge CB2 3EB, United KingdomPhonological 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.http://www.sciencedirect.com/science/article/pii/S1053811922002063DyslexiaMagnetoencephalographyNeural oscillationsSpeech processingPhonological deficit |
| spellingShingle | Kanad Mandke Sheila Flanagan Annabel Macfarlane Fiona Gabrielczyk Angela Wilson Joachim Gross Usha Goswami Neural sampling of the speech signal at different timescales by children with dyslexia NeuroImage Dyslexia Magnetoencephalography Neural oscillations Speech processing Phonological deficit |
| title | Neural sampling of the speech signal at different timescales by children with dyslexia |
| title_full | Neural sampling of the speech signal at different timescales by children with dyslexia |
| title_fullStr | Neural sampling of the speech signal at different timescales by children with dyslexia |
| title_full_unstemmed | Neural sampling of the speech signal at different timescales by children with dyslexia |
| title_short | Neural sampling of the speech signal at different timescales by children with dyslexia |
| title_sort | neural sampling of the speech signal at different timescales by children with dyslexia |
| topic | Dyslexia Magnetoencephalography Neural oscillations Speech processing Phonological deficit |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922002063 |
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