Atypical processing in neural source analysis of speech envelope modulations in adolescents with dyslexia.

Different studies have suggested that language and developmental disorders such as dyslexia are associated with a disturbance of auditory entrainment and of the functional hemispheric asymmetries during speech processing. These disorders typically result from an issue in the phonological component of language that causes problems to represent and manipulate the phonological structure of words at the syllable and/or phoneme level. We used Auditory Steady-State Responses (ASSRs) in EEG recordings to investigate the brain activation and hemisphere asymmetry of theta, alpha, beta and low-gamma range oscillations in typical readers and readers with dyslexia. The aim was to analyse whether the group differences found in previous electrode level studies were caused by a different source activation pattern or conversely was an effect that could be found on the active brain sources. We could not find differences in the brain locations of the main active brain sources. However, we observed differences in the extracted waveforms. The group average of the first DSS component of all signal-to-noise ratios of ASSR at source level was higher than the group averages at the electrode level. These analyses included a lower alpha synchronisation in adolescents with dyslexia and the possibility of compensatory mechanisms in theta, beta and low-gamma frequency bands. The main brain auditory sources were located in cortical regions around the auditory cortex. Thus, the differences observed in auditory EEG experiments would, according to our findings, have their origin in the intrinsic oscillatory mechanisms of the brain cortical sources related to speech perception.

The identification of predominant auditory steady-state response brain sources in electroencephalography using denoising source separation.

Different approaches have been used to extract auditory steady-state responses (ASSRs) from electroencephalography (EEG) recordings, including region-related electrode configurations (electrode level) and the manual placement of equivalent current dipoles (source level). Inherent limitations of these approaches are the assumption of the anatomical origin and the omission of activity generated by secondary sources. Data-driven methods such as independent component analysis (ICA) seem to avoid these limitations but only to face new others such as the presence of ASSRs with similar properties in different components and the manual selection protocol to select and classify the most relevant components carrying ASSRs. We propose the novel approach of applying a spatial filter to these components in order to extract the most relevant information. We aimed to develop a method based on the reproducibility across trials that performs reliably in low-signal-to-noise ratio (SNR) scenarios using denoising source separation (DSS). DSS combined with ICA successfully reduced the number of components and extracted the most relevant ASSR at 4, 10 and 20 Hz stimulation in group and individual level studies of EEG adolescent data. The anatomical brain location for these low stimulation frequencies showed results in cortical areas with relatively small dispersion. However, for 40 and 80 Hz, results with regard to the number of components and the anatomical origin were less clear. At all stimulation frequencies the outcome measures were consistent with literature, and the partial rejection of inter-subject variability led to more accurate results and higher SNRs. These findings are promising for future applications in group comparison involving pathologies.

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.

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.

Grapheme-Phoneme Learning in an Unknown Orthography: A Study in Typical Reading and Dyslexic Children.

In this study, we examined the learning of new grapheme-phoneme correspondences in individuals with and without dyslexia. Additionally, we investigated the relation between grapheme-phoneme learning and measures of phonological awareness, orthographic knowledge and rapid automatized naming, with a focus on the unique joint variance of grapheme-phoneme learning to word and non-word reading achievement. Training of grapheme-phoneme associations consisted of a 20-min training program in which eight novel letters (Hebrew) needed to be paired with speech sounds taken from the participant's native language (Dutch). Eighty-four third grade students, of whom 20 were diagnosed with dyslexia, participated in the training and testing. Our results indicate a reduced ability of dyslexic readers in applying newly learned grapheme-phoneme correspondences while reading words which consist of these novel letters. However, we did not observe a significant independent contribution of grapheme-phoneme learning to reading outcomes. Alternatively, results from the regression analysis indicate that failure to read may be due to differences in phonological and/or orthographic knowledge but not to differences in the grapheme-phoneme-conversion process itself.

Neural organization of ventral white matter tracts parallels the initial steps of reading development: A DTI tractography study.

Insight in the developmental trajectory of the neuroanatomical reading correlates is important to understand related cognitive processes and disorders. In adults, a dual pathway model has been suggested encompassing a dorsal phonological and a ventral orthographic white matter system. This dichotomy seems not present in pre-readers, and the specific role of ventral white matter in reading remains unclear. Therefore, the present longitudinal study investigated the relation between ventral white matter and cognitive processes underlying reading in children with a broad range of reading skills (n = 61). Ventral pathways of the reading network were manually traced using diffusion tractography: the inferior fronto-occipital fasciculus (IFOF), inferior longitudinal fasciculus (ILF) and uncinate fasciculus (UF). Pathways were examined pre-reading (5-6 years) and after two years of reading acquisition (7-8 years). Dimension reduction for the cognitive measures resulted in one component for pre-reading cognitive measures and a separate phonological and orthographic component for the early reading measures. Regression analyses revealed a relation between the pre-reading cognitive component and bilateral IFOF and left ILF. Interestingly, exclusively the left IFOF was related to the orthographic component, whereas none of the pathways was related to the phonological component. Hence, the left IFOF seems to serve as the lexical reading route, already in the earliest reading stages.

Atypical Structural Asymmetry of the Planum Temporale is Related to Family History of Dyslexia.

Research on the neural correlates of developmental dyslexia indicates atypical anatomical lateralization of the planum temporale, a higher-order cortical auditory region. Yet whether this atypical lateralization precedes reading acquisition and is related to a familial risk for dyslexia is not currently known. In this study, we address these questions in 2 separate cohorts of young children and adolescents with and without a familial risk for dyslexia. Planum temporale surface area was manually labeled bilaterally, on the T1-weighted MR brain images of 54 pre-readers (mean age: 6.2 years, SD: 3.2 months; 33 males) and 28 adolescents (mean age: 14.7 years, SD: 3.3 months; 11 males). Half of the pre-readers and adolescents had a familial risk for dyslexia. In both pre-readers and adolescents, group comparisons of left and right planum temporale surface area showed a significant interaction between hemisphere and family history of dyslexia, with participants who had no family risk for dyslexia showing greater leftward asymmetry of the planum temporale. This effect was confirmed when analyses were restricted to normal reading participants. Altered planum temporale asymmetry thus seems to be related to family history of dyslexia.

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.

Source analysis of auditory steady-state responses in acoustic and electric hearing.

Speech is a complex signal containing a broad variety of acoustic information. For accurate speech reception, the listener must perceive modulations over a range of envelope frequencies. Perception of these modulations is particularly important for cochlear implant (CI) users, as all commercial devices use envelope coding strategies. Prolonged deafness affects the auditory pathway. However, little is known of how cochlear implantation affects the neural processing of modulated stimuli. This study investigates and contrasts the neural processing of envelope rate modulated signals in acoustic and CI listeners. Auditory steady-state responses (ASSRs) are used to study the neural processing of amplitude modulated (AM) signals. A beamforming technique is applied to determine the increase in neural activity relative to a control condition, with particular attention paid to defining the accuracy and precision of this technique relative to other tomographies. In a cohort of 44 acoustic listeners, the location, activity and hemispheric lateralisation of ASSRs is characterised while systematically varying the modulation rate (4, 10, 20, 40 and 80Hz) and stimulation ear (right, left and bilateral). We demonstrate a complex pattern of laterality depending on both modulation rate and stimulation ear that is consistent with, and extends, existing literature. We present a novel extension to the beamforming method which facilitates source analysis of electrically evoked auditory steady-state responses (EASSRs). In a cohort of 5 right implanted unilateral CI users, the neural activity is determined for the 40Hz rate and compared to the acoustic cohort. Results indicate that CI users activate typical thalamic locations for 40Hz stimuli. However, complementary to studies of transient stimuli, the CI population has atypical hemispheric laterality, preferentially activating the contralateral hemisphere.

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.