Emerging neural specialization of the ventral occipitotemporal cortex to characters through phonological association learning in preschool children.

The ventral occipitotemporal (vOT) cortex serves as a core region for visual processing, and specific areas of this region show preferential activation for various visual categories such as faces and print. The emergence of such functional specialization in the human cortex represents a pivotal developmental process, which provides a basis for targeted and efficient information processing. For example, functional specialization to print in the left vOT is an important prerequisite for fluent reading. However, it remains unclear, which processes initiate the preferential cortical activations to characters arising in the vOT during child development. Using a multimodal neuroimaging approach with preschool children at familial risk for developmental dyslexia, we demonstrate how varying levels of expertise modulate the neural response to single characters, which represent the building blocks of print units. The level of expertise to characters was manipulated firstly through brief training of false-font speech-sound associations and secondly by comparing characters for which children differed in their level of familiarity and expertise accumulated through abundant exposure in their everyday environment. Neural correlates of character processing were tracked with simultaneous high-density electroencephalography and functional magnetic resonance imaging in a target detection task. We found training performance and expertise-dependent modulation of the visual event-related potential around 220 ms (N1) and the corresponding vOT activation. Additionally, trained false-font characters revealed stronger functional connectivity between the left fusiform gyrus (FFG) seed and left superior parietal/lateral occipital cortex regions with higher training performance. In sum, our results demonstrate that learning artificial-character speech-sound associations enhances activation to trained characters in the vOT and that the magnitude of this activation and the functional connectivity of the left FFG to the parieto-occipital cortex depends on learning performance. This pattern of results suggests emerging development of the reading network after brief training that parallels network specialization during reading acquisition.

Neural initialization of audiovisual integration in prereaders at varying risk for developmental dyslexia.

Learning letter-speech sound correspondences is a major step in reading acquisition and is severely impaired in children with dyslexia. Up to now, it remains largely unknown how quickly neural networks adopt specific functions during audiovisual integration of linguistic information when prereading children learn letter-speech sound correspondences. Here, we simulated the process of learning letter-speech sound correspondences in 20 prereading children (6.13-7.17 years) at varying risk for dyslexia by training artificial letter-speech sound correspondences within a single experimental session. Subsequently, we acquired simultaneously event-related potentials (ERP) and functional magnetic resonance imaging (fMRI) scans during implicit audiovisual presentation of trained and untrained pairs. Audiovisual integration of trained pairs correlated with individual learning rates in right superior temporal, left inferior temporal, and bilateral parietal areas and with phonological awareness in left temporal areas. In correspondence, a differential left-lateralized parietooccipitotemporal ERP at 400 ms for trained pairs correlated with learning achievement and familial risk. Finally, a late (650 ms) posterior negativity indicating audiovisual congruency of trained pairs was associated with increased fMRI activation in the left occipital cortex. Taken together, a short (<30 min) letter-speech sound training initializes audiovisual integration in neural systems that are responsible for processing linguistic information in proficient readers. To conclude, the ability to learn grapheme-phoneme correspondences, the familial history of reading disability, and phonological awareness of prereading children account for the degree of audiovisual integration in a distributed brain network. Such findings on emerging linguistic audiovisual integration could allow for distinguishing between children with typical and atypical reading development. Hum Brain Mapp 38:1038-1055, 2017. © 2016 Wiley Periodicals, Inc.

Visual Occipito-Temporal N1 Sensitivity to Digits Across Elementary School.

Number processing abilities are important for academic and personal development. The course of initial specialization of ventral occipito-temporal cortex (vOTC) sensitivity to visual number processing is crucial for the acquisition of numeric and arithmetic skills. We examined the visual N1, the electrophysiological correlate of vOTC activation across five time points in kindergarten (T1, mean age 6.60 years), middle and end of first grade (T2, 7.38 years; T3, 7.68 years), second grade (T4, 8.28 years), and fifth grade (T5, 11.40 years). A combination of cross-sectional and longitudinal EEG data of a total of 62 children (35 female) at varying familial risk for dyslexia were available to form groups of 23, 22, 27, 27, and 42 participants for each of the five time points. The children performed a target detection task which included visual presentation of single digits (DIG), false fonts (FF), and letters (LET) to derive measures for coarse (DIG vs. FF) and fine (DIG vs. LET) digit sensitive processing across development. The N1 amplitude analyses indicated coarse and fine sensitivity characterized by a stronger N1 to digits than false fonts across all five time points, and stronger N1 to digits than letters at all but the second (T2) time point. In addition, lower arithmetic skills were associated with stronger coarse N1 digit sensitivity over the left hemisphere in second grade (T4), possibly reflecting allocation of more attentional resources or stronger reliance on the verbal system in children with poorer arithmetic skills. To summarize, our results show persistent visual N1 sensitivity to digits that is already present early on in pre-school and remains stable until fifth grade. This pattern of digit sensitivity development clearly differs from the relatively sharp rise and fall of the visual N1 sensitivity to words or letters between kindergarten and middle of elementary school and suggests unique developmental trajectories for visual processing of written characters that are relevant to numeracy and literacy.

Developmental Trajectories of Letter and Speech Sound Integration During Reading Acquisition.

Reading acquisition in alphabetic languages starts with learning the associations between speech sounds and letters. This learning process is related to crucial developmental changes of brain regions that serve visual, auditory, multisensory integration, and higher cognitive processes. Here, we studied the development of audiovisual processing and integration of letter-speech sound pairs with an audiovisual target detection functional MRI paradigm. Using a longitudinal approach, we tested children with varying reading outcomes before the start of reading acquisition (T1, 6.5 yo), in first grade (T2, 7.5 yo), and in second grade (T3, 8.5 yo). Early audiovisual integration effects were characterized by higher activation for incongruent than congruent letter-speech sound pairs in the inferior frontal gyrus and ventral occipitotemporal cortex. Audiovisual processing in the left superior temporal gyrus significantly increased from the prereading (T1) to early reading stages (T2, T3). Region of interest analyses revealed that activation in left superior temporal gyrus (STG), inferior frontal gyrus and ventral occipitotemporal cortex increased in children with typical reading fluency skills, while poor readers did not show the same development in these regions. The incongruency effect bilaterally in parts of the STG and insular cortex at T1 was significantly associated with reading fluency skills at T3. These findings provide new insights into the development of the brain circuitry involved in audiovisual processing of letters, the building blocks of words, and reveal early markers of audiovisual integration that may be predictive of reading outcomes.

The rise and fall of rapid occipito-temporal sensitivity to letters: Transient specialization through elementary school.

Letters, foundational units of alphabetic writing systems, are quintessential to human culture. The ability to read, indispensable to perform in today's society, necessitates a reorganization of visual cortex for fast letter recognition, but the developmental course of this process has not yet been characterized. Here, we show the emergence of visual sensitivity to letters across five electroencephalography measurements from kindergarten and throughout elementary school and relate this development to emerging reading skills. We examined the visual N1, the electrophysiological correlate of ventral occipito-temporal cortex activation in 65 children at varying familial risk for dyslexia. N1 letter sensitivity emerged in first grade, when letter sound knowledge gains were most pronounced and decayed shortly after when letter knowledge is consolidated, showing an inverted U-shaped development. This trajectory can be interpreted within an interactive framework that underscores the influence of top-down predictions. While the N1 amplitudes to letters correlated with letter sound knowledge at the beginning of learning, no association between the early N1 letter response and later reading skills was found. In summary, the current findings provide an important reference point for our neuroscientific understanding of learning trajectories and the process of visual specialization during skill learning.

Development of Print-Speech Integration in the Brain of Beginning Readers With Varying Reading Skills.

Learning print-speech sound correspondences is a crucial step at the beginning of reading acquisition and often impaired in children with developmental dyslexia. Despite increasing insight into audiovisual language processing, it remains largely unclear how integration of print and speech develops at the neural level during initial learning in the first years of schooling. To investigate this development, 32 healthy, German-speaking children at varying risk for developmental dyslexia (17 typical readers and 15 poor readers) participated in a longitudinal study including behavioral and fMRI measurements in first (T1) and second (T2) grade. We used an implicit audiovisual (AV) non-word target detection task aimed at characterizing differential activation to congruent (AVc) and incongruent (AVi) audiovisual non-word pairs. While children's brain activation did not differ between AVc and AVi pairs in first grade, an incongruency effect (AVi > AVc) emerged in bilateral inferior temporal and superior frontal gyri in second grade. Of note, pseudoword reading performance improvements with time were associated with the development of the congruency effect (AVc > AVi) in the left posterior superior temporal gyrus (STG) from first to second grade. Finally, functional connectivity analyses indicated divergent development and reading expertise dependent coupling from the left occipito-temporal and superior temporal cortex to regions of the default mode (precuneus) and fronto-temporal language networks. Our results suggest that audiovisual integration areas as well as their functional coupling to other language areas and areas of the default mode network show a different development in poor vs. typical readers at varying familial risk for dyslexia.

(Swiss) GraphoLearn: an app-based tool to support beginning readers.

We assessed the Swiss-German version of GraphoLearn, a computer game designed to support reading by training grapheme-phoneme correspondences. A group of 34 children at risk for dyslexia trained three times a week during 14 weeks, on top of their standard school instruction. The sample was divided into two groups of 18 and 16 children, who started training at either the middle or the end of first grade. We found beneficial training effects in pseudoword reading in both training groups and for rapid automatized naming skills in the group that trained earlier. Our results suggest that both the efficiency in phonological decoding and rapid access to verbal representations are susceptible to facilitation by GraphoLearn. These findings confirm the utility of the training software as a tool to support school instruction and reading-related abilities in beginning readers. We discuss ideas to improve the content and outcomes of future versions of the training software.

Simultaneous EEG and fMRI reveals stronger sensitivity to orthographic strings in the left occipito-temporal cortex of typical versus poor beginning readers.

The level of reading skills in children and adults is reflected in the strength of preferential neural activation to print. Such preferential activation appears in the N1 event-related potential (ERP) over the occipitotemporal scalp after around 150-250 ms and the corresponding blood oxygen level dependent (BOLD) signal in the ventral occipitotemporal (vOT) cortex. Here, orthography-sensitive (print vs. false font) processing was examined using simultaneous EEG-fMRI in 38 first grade children with poor and typical reading skills, and at varying familial risk for developmental dyslexia. Coarse orthographic sensitivity was observed as an increased activation to print in the N1 ERP and in the BOLD signal of individually varying vOT regions in 57% of beginning readers. Finer differentiation in processing orthographic strings (words vs. nonwords) further occurred in specific vOT clusters. Neither method alone showed robust differences in orthography-sensitive processing between typical and poor reading children. Importantly, using single-trial N1 ERP-informed fMRI analysis, we found differential modulation of the orthography-sensitive BOLD response in the left vOT for typical readers only. This result, thus, confirms subtle functional alterations in a brain structure known to be critical for fluent reading at the very beginning of reading instruction.

Simulating reading acquisition: The link between reading outcome and multimodal brain signatures of letter-speech sound learning in prereaders.

During reading acquisition, neural reorganization of the human brain facilitates the integration of letters and speech sounds, which enables successful reading. Neuroimaging and behavioural studies have established that impaired audiovisual integration of letters and speech sounds is a core deficit in individuals with developmental dyslexia. This longitudinal study aimed to identify neural and behavioural markers of audiovisual integration that are related to future reading fluency. We simulated the first step of reading acquisition by performing artificial-letter training with prereading children at risk for dyslexia. Multiple logistic regressions revealed that our training provides new precursors of reading fluency at the beginning of reading acquisition. In addition, an event-related potential around 400 ms and functional magnetic resonance imaging activation patterns in the left planum temporale to audiovisual correspondences improved cross-validated prediction of future poor readers. Finally, an exploratory analysis combining simultaneously acquired electroencephalography and hemodynamic data suggested that modulation of temporoparietal brain regions depended on future reading skills. The multimodal approach demonstrates neural adaptations to audiovisual integration in the developing brain that are related to reading outcome. Despite potential limitations arising from the restricted sample size, our results may have promising implications both for identifying poor-reading children and for monitoring early interventions.

Native and non-native speech sound processing and the neural mismatch responses: A longitudinal study on classroom-based foreign language learning.

Learning a foreign language in a natural immersion context with high exposure to the new language has been shown to change the way speech sounds of that language are processed at the neural level. It remains unclear, however, to what extent this is also the case for classroom-based foreign language learning, particularly in children. To this end, we presented a mismatch negativity (MMN) experiment during EEG recordings as part of a longitudinal developmental study: 38 monolingual (Swiss-) German speaking children (7.5 years) were tested shortly before they started to learn English at school and followed up one year later. Moreover, 22 (Swiss-) German adults were recorded. Instead of the originally found positive mismatch response in children, an MMN emerged when applying a high-pass filter of 3 Hz. The overlap of a slow-wave positivity with the MMN indicates that two concurrent mismatch processes were elicited in children. The children's MMN in response to the non-native speech contrast was smaller compared to the native speech contrast irrespective of foreign language learning, suggesting that no additional neural resources were committed to processing the foreign language speech sound after one year of classroom-based learning.