Subcortical auditory neural synchronization is deficient in pre-reading children who develop dyslexia.

Auditory processing of temporal information in speech is sustained by synchronized firing of neurons along the entire auditory pathway. In school-aged children and adults with dyslexia, neural synchronization deficits have been found at cortical levels of the auditory system, however, these deficits do not appear to be present in pre-reading children. An alternative role for subcortical synchronization in reading development and dyslexia has been suggested, but remains debated. By means of a longitudinal study, we assessed cognitive reading-related skills and subcortical auditory steady-state responses (80 Hz ASSRs) in a group of children before formal reading instruction (pre-reading), after 1 year of formal reading instruction (beginning reading), and after 3 years of formal reading instruction (more advanced reading). Children were retrospectively classified into three groups based on family risk and literacy achievement: typically developing children without a family risk for dyslexia, typically developing children with a family risk for dyslexia, and children who developed dyslexia. Our results reveal that children who developed dyslexia demonstrate decreased 80 Hz ASSRs at the pre-reading stage. This effect is no longer present after the onset of reading instruction, due to an atypical developmental increase in 80 Hz ASSRs between the pre-reading and the beginning reading stage. A forward stepwise logistic regression analysis showed that literacy achievement was predictable with an accuracy of 90.4% based on a model including three significant predictors, that is, family risk for dyslexia (R = .31), phonological awareness (R = .23), and 80 Hz ASSRs (R = .26). Given that (1) abnormalities in subcortical ASSRs preceded reading acquisition in children who developed dyslexia and (2) subcortical ASSRs contributed to the prediction of literacy achievement, subcortical auditory synchronization deficits may constitute a pre-reading risk factor in the emergence of dyslexia.

Hemispheric asymmetry in auditory processing of speech envelope modulations in prereading children.

The temporal envelope of speech is an important cue contributing to speech intelligibility. Theories about the neural foundations of speech perception postulate that the left and right auditory cortices are functionally specialized in analyzing speech envelope information at different time scales: the right hemisphere is thought to be specialized in processing syllable rate modulations, whereas a bilateral or left hemispheric specialization is assumed for phoneme rate modulations. Recently, it has been found that this functional hemispheric asymmetry is different in individuals with language-related disorders such as dyslexia. Most studies were, however, performed in adults and school-aged children, and only a little is known about how neural auditory processing at these specific rates manifests and develops in very young children before reading acquisition. Yet, studying hemispheric specialization for processing syllable and phoneme rate modulations in preliterate children may reveal early neural markers for dyslexia. In the present study, human cortical evoked potentials to syllable and phoneme rate modulations were measured in 5-year-old children at high and low hereditary risk for dyslexia. The results demonstrate a right hemispheric preference for processing syllable rate modulations and a symmetric pattern for phoneme rate modulations, regardless of hereditary risk for dyslexia. These results suggest that, while hemispheric specialization for processing syllable rate modulations seems to be mature in prereading children, hemispheric specialization for phoneme rate modulation processing may still be developing. These findings could have important implications for the development of phonological and reading skills.

The relation between neurofunctional and neurostructural determinants of phonological processing in pre-readers.

Phonological processing skills are known as the most robust cognitive predictor of reading ability. Therefore, the neural determinants of phonological processing have been extensively investigated by means of either neurofunctional or neurostructural techniques. However, to fully understand how the brain represents and processes phonological information, there is need for studies that combine both methods. The present study applies such a multimodal approach with the aim of investigating the pre-reading relation between neural measures of auditory temporal processing, white matter properties of the reading network and phonological processing skills. We administered auditory steady-state responses, diffusion-weighted MRI scans and phonological awareness tasks in 59 pre-readers. Our results demonstrate that a stronger rightward lateralization of syllable-rate (4 Hz) processing coheres with higher fractional anisotropy in the left fronto-temporoparietal arcuate fasciculus. Both neural features each in turn relate to better phonological processing skills. As such, the current study provides novel evidence for the existence of a pre-reading relation between functional measures of syllable-rate processing, structural organization of the arcuate fasciculus and cognitive precursors of reading development. Moreover, our findings demonstrate the value of combining different neural techniques to gain insight in the underlying neural systems for reading (dis)ability.

Do prereaders' auditory processing and speech perception predict later literacy?

Developmental dyslexia has frequently been linked to deficits in auditory processing and speech perception. However, the presence and precise nature of these deficits and the direction of their relation with reading, remains debated. In this longitudinal study, 87 five-year-olds at high and low family risk for dyslexia were followed before and during different stages of reading acquisition. The processing of different auditory cues was investigated, together with performance on speech perception and phonology and reading. Results show no effect of family risk for dyslexia on prereading auditory processing and speech perception skills. However, a relation is present between the performance on these skills in kindergarten and later phonology and literacy. In particular, links are found with the auditory processing of cues characteristic for the temporal speech amplitude envelope, rather than with other auditory cues important for speech intelligibility. Hereby, cues embedded in the speech amplitude envelope show to be related to a broad range of phonological precursors for reading. In addition, speech-in-noise perception demonstrates to operate as the most contributing factor for later phonological awareness and to be a predictor for reading mediated by the association with phonology. This study provides behavioral support for the link between prereading speech amplitude envelope processing and speech perception for future phonology and reading.

A longitudinal study investigating neural processing of speech envelope modulation rates in children with (a family risk for) dyslexia.

Recent evidence suggests that a fundamental deficit in the synchronization of neural oscillations to temporal information in speech may underlie phonological processing problems in dyslexia. Since previous studies were performed cross-sectionally in school-aged children or adults, developmental aspects of neural auditory processing in relation to reading acquisition and dyslexia remain to be investigated. The present longitudinal study followed 68 children during development from pre-reader (5 years old) to beginning reader (7 years old) and more advanced reader (9 years old). Thirty-six children had a family risk for dyslexia and 14 children eventually developed dyslexia. EEG recordings of auditory steady-state responses to 4 and 20 Hz modulations, corresponding to syllable and phoneme rates, were collected at each point in time. Our results demonstrate an increase in neural synchronization to phoneme-rate modulations around the onset of reading acquisition. This effect was negatively correlated with later reading and phonological skills, indicating that children who exhibit the largest increase in neural synchronization to phoneme rates, develop the poorest reading and phonological skills. Accordingly, neural synchronization to phoneme-rate modulations was found to be significantly higher in beginning and more advanced readers with dyslexia. We found no developmental effects regarding neural synchronization to syllable rates, nor any effects of a family risk for dyslexia. Altogether, our findings suggest that the onset of reading instruction coincides with an increase in neural responsiveness to phoneme-rate modulations, and that the extent of this increase is related to (the outcome of) reading development. Hereby, dyslexic children persistently demonstrate atypically high neural synchronization to phoneme rates from the beginning of reading acquisition onwards.

Atypical neural synchronization to speech envelope modulations in dyslexia.

A fundamental deficit in the synchronization of neural oscillations to temporal information in speech could underlie phonological processing problems in dyslexia. In this study, the hypothesis of a neural synchronization impairment is investigated more specifically as a function of different neural oscillatory bands and temporal information rates in speech. Auditory steady-state responses to 4, 10, 20 and 40Hz modulations were recorded in normal reading and dyslexic adolescents to measure neural synchronization of theta, alpha, beta and low-gamma oscillations to syllabic and phonemic rate information. In comparison to normal readers, dyslexic readers showed reduced non-synchronized theta activity, reduced synchronized alpha activity and enhanced synchronized beta activity. Positive correlations between alpha synchronization and phonological skills were found in normal readers, but were absent in dyslexic readers. In contrast, dyslexic readers exhibited positive correlations between beta synchronization and phonological skills. Together, these results suggest that auditory neural synchronization of alpha and beta oscillations is atypical in dyslexia, indicating deviant neural processing of both syllabic and phonemic rate information. Impaired synchronization of alpha oscillations in particular demonstrated to be the most prominent neural anomaly possibly hampering speech and phonological processing in dyslexic readers.

Theta, beta and gamma rate modulations in the developing auditory system.

In the brain, the temporal analysis of many important auditory features relies on the synchronized firing of neurons to the auditory input rhythm. These so-called neural oscillations play a crucial role in sensory and cognitive processing and deviances in oscillatory activity have shown to be associated with neurodevelopmental disorders. Given the importance of neural auditory oscillations in normal and impaired sensory and cognitive functioning, there has been growing interest in their developmental trajectory from early childhood on. In the present study, neural auditory processing was investigated in typically developing young children (n = 40) and adults (n = 27). In all participants, auditory evoked theta, beta and gamma responses were recorded. The results of this study show maturational differences between children and adults in neural auditory processing at cortical as well as at brainstem level. Neural background noise at cortical level was shown to be higher in children compared to adults. In addition, higher theta response amplitudes were measured in children compared to adults. For beta and gamma rate modulations, different processing asymmetry patterns were observed between both age groups. The mean response phase was also shown to differ significantly between children and adults for all rates. Results suggest that cortical auditory processing of beta develops from a general processing pattern into a more specialized asymmetric processing preference over age. Moreover, the results indicate an enhancement of bilateral representation of monaural sound input at brainstem with age. A dissimilar efficiency of auditory signal transmission from brainstem to cortex along the auditory pathway between children and adults is suggested. These developmental differences might be due to both functional experience-dependent as well as anatomical changes. The findings of the present study offer important information about maturational differences between children and adults for responses to theta, beta and gamma rates. The current study can have important implications for the understanding of developmental disorders which are known to be associated with deviances in neural auditory processing.

A DTI tractography study in pre-readers at risk for dyslexia.

In adults and school-aged children, phonological aspects of reading seem to be sustained by left dorsal regions, while ventral regions seem to be involved in orthographic word recognition. Yet, given that the brain reorganises during reading acquisition, it is unknown when and how these reading routes emerge and whether neural deficits in dyslexia predate reading onset. Using diffusion MRI in 36 pre-readers with a family risk for dyslexia (FRD(+)) and 35 well matched pre-readers without a family risk (FRD(-)), our results show that phonological predictors of reading are sustained bilaterally by both ventral and dorsal tracts. This suggests that a dorsal and left-hemispheric specialisation for phonological aspects of reading, as observed in adults, is presumably gradually formed throughout reading development. Second, our results indicate that FRD(+) pre-readers display mainly white matter differences in left ventral tracts. This suggests that atypical white matter organisation previously found in dyslexic adults may be causal rather than resulting from a lifetime of reading difficulties, and that the location of such a deficit may vary throughout development. While this study forms an important starting point, longitudinal follow-up of these children will allow further investigation of the dynamics between emerging literacy development and white matter connections.