Evolution of reading and face circuits during the first three years of reading acquisition.

Although words and faces activate neighboring regions in the fusiform gyrus, we lack an understanding of how such category selectivity emerges during development. To investigate the organization of reading and face circuits at the earliest stage of reading acquisition, we measured the fMRI responses to words, faces, houses, and checkerboards in three groups of 60 French children: 6-year-old pre-readers, 6-year-old beginning readers and 9-year-old advanced readers. The results showed that specific responses to written words were absent prior to reading, but emerged in beginning readers, irrespective of age. Likewise, specific responses to faces were barely visible in pre-readers and continued to evolve in the 9-year-olds, yet primarily driven by age rather than by schooling. Crucially, the sectors of ventral visual cortex that become specialized for words and faces harbored their own functional connectivity prior to reading acquisition: the VWFA with left-hemispheric spoken language areas, and the FFA with the contralateral region and the amygdalae. The results support the view that reading acquisition occurs through the recycling of a pre-existing but plastic circuit which, in pre-readers, already connects the VWFA site to other distant language areas. We argue that reading acquisition does not compete with the face system directly, through a pruning of preexisting face responses, but indirectly, by hindering the slow growth of face responses in the left hemisphere, thus increasing a pre-existing right hemispheric bias.

A universal reading network and its modulation by writing system and reading ability in French and Chinese children.

Are the brain mechanisms of reading acquisition similar across writing systems? And do similar brain anomalies underlie reading difficulties in alphabetic and ideographic reading systems? In a cross-cultural paradigm, we measured the fMRI responses to words, faces, and houses in 96 Chinese and French 10-year-old children, half of whom were struggling with reading. We observed a reading circuit which was strikingly similar across languages and consisting of the left fusiform gyrus, superior temporal gyrus/sulcus, precentral and middle frontal gyri. Activations in some of these areas were modulated either by language or by reading ability, but without interaction between those factors. In various regions previously associated with dyslexia, reading difficulty affected activation similarly in Chinese and French readers, including the middle frontal gyrus, a region previously described as specifically altered in Chinese. Our analyses reveal a large degree of cross-cultural invariance in the neural correlates of reading acquisition and reading impairment.

Neuroanatomy of dyslexia: An allometric approach.

Despite evidence for a difference in total brain volume between dyslexic and good readers, no previous neuroimaging study examined differences in allometric scaling (i.e. differences in the relationship between regional and total brain volumes) between dyslexic and good readers. The present study aims to fill this gap by testing differences in allometric scaling and regional brain volume differences in dyslexic and good readers. Object-based morphometry analysis was used to determine grey and white matter volumes of the four lobes, the cerebellum and limbic structures in 130 dyslexic and 106 good readers aged 8-14 years. Data were collected across three countries (France, Poland and Germany). Three methodological approaches were used as follows: principal component analysis (PCA), linear regression and multiple-group confirmatory factor analysis (MGCFA). Difference in total brain volume between good and dyslexic readers was Cohen's d = 0.39. We found no difference in allometric scaling, nor in regional brain volume between dyslexic and good readers. Results of our three methodological approaches (PCA, linear regression and MGCFA) were consistent. This study provides evidence for total brain volume differences between dyslexic and control children, but no evidence for differences in the volumes of the four lobes, the cerebellum or limbic structures, once allometry is taken into account. It also finds no evidence for a difference in allometric relationships between the groups. We highlight the methodological interest of the MGCFA approach to investigate such research issues.

Connectivity between the visual word form area and the parietal lobe improves after the first year of reading instruction: a longitudinal MRI study in children.

Shortly after reading instruction, a region in the ventral occipital temporal cortex (vOTC) of the left hemisphere, the Visual Word Form Area (VWFA), becomes specialized for written words. Its reproducible location across scripts suggests important anatomical constraints, such as specific patterns of connectivity, notably to spoken language areas. Here, we explored the structural connectivity of the emerging VWFA in terms of its specificity relative to other ventral visual regions and its stability throughout the process of reading instruction in ten children studied longitudinally over 2 years. Category-specific regions for words, houses, faces, and tools were identified in the left vOTC of each subject with functional MRI. With diffusion MRI and tractography, we reconstructed the connections of these regions at two time points (mean age ± standard deviation: 6.2 ± 0.3, 7.2 ± 0.4 years). We first showed that the regions for each visual category harbor their own specific connectivity, all of which precede reading instruction and remain stable throughout development. The most specific connections of the VWFA were to the dorsal posterior parietal cortex. We then showed that microstructural changes in these connections correlated with improvements in reading scores over the first year of instruction but not 1 year later in a subsample of eight children (age: 8.4 ± 0.3 years). These results suggest that the VWFA location depends on its connectivity to distant regions, in particular, the left inferior parietal region which may play a crucial role in visual field maps and eye movement dynamics in addition to attentional control in letter-by-letter reading and disambiguation of mirror-letters during the first stages of learning to read.

The emergence of the visual word form: Longitudinal evolution of category-specific ventral visual areas during reading acquisition.

How does education affect cortical organization? All literate adults possess a region specialized for letter strings, the visual word form area (VWFA), within the mosaic of ventral regions involved in processing other visual categories such as objects, places, faces, or body parts. Therefore, the acquisition of literacy may induce a reorientation of cortical maps towards letters at the expense of other categories such as faces. To test this cortical recycling hypothesis, we studied how the visual cortex of individual children changes during the first months of reading acquisition. Ten 6-year-old children were scanned longitudinally 6 or 7 times with functional magnetic resonance imaging (fMRI) before and throughout the first year of school. Subjects were exposed to a variety of pictures (words, numbers, tools, houses, faces, and bodies) while performing an unrelated target-detection task. Behavioral assessment indicated a sharp rise in grapheme-phoneme knowledge and reading speed in the first trimester of school. Concurrently, voxels specific to written words and digits emerged at the VWFA location. The responses to other categories remained largely stable, although right-hemispheric face-related activity increased in proportion to reading scores. Retrospective examination of the VWFA voxels prior to reading acquisition showed that reading encroaches on voxels that are initially weakly specialized for tools and close to but distinct from those responsive to faces. Remarkably, those voxels appear to keep their initial category selectivity while acquiring an additional and stronger responsivity to words. We propose a revised model of the neuronal recycling process in which new visual categories invade weakly specified cortex while leaving previously stabilized cortical responses unchanged.

Multi-parameter machine learning approach to the neuroanatomical basis of developmental dyslexia.

Despite decades of research, the anatomical abnormalities associated with developmental dyslexia are still not fully described. Studies have focused on between-group comparisons in which different neuroanatomical measures were generally explored in isolation, disregarding potential interactions between regions and measures. Here, for the first time a multivariate classification approach was used to investigate grey matter disruptions in children with dyslexia in a large (N = 236) multisite sample. A variety of cortical morphological features, including volumetric (volume, thickness and area) and geometric (folding index and mean curvature) measures were taken into account and generalizability of classification was assessed with both 10-fold and leave-one-out cross validation (LOOCV) techniques. Classification into control vs. dyslexic subjects achieved above chance accuracy (AUC = 0.66 and ACC = 0.65 in the case of 10-fold CV, and AUC = 0.65 and ACC = 0.64 using LOOCV) after principled feature selection. Features that discriminated between dyslexic and control children were exclusively situated in the left hemisphere including superior and middle temporal gyri, subparietal sulcus and prefrontal areas. They were related to geometric properties of the cortex, with generally higher mean curvature and a greater folding index characterizing the dyslexic group. Our results support the hypothesis that an atypical curvature pattern with extra folds in left hemispheric perisylvian regions characterizes dyslexia. Hum Brain Mapp 38:900-908, 2017. © 2016 Wiley Periodicals, Inc.

New human-specific brain landmark: the depth asymmetry of superior temporal sulcus.

Identifying potentially unique features of the human cerebral cortex is a first step to understanding how evolution has shaped the brain in our species. By analyzing MR images obtained from 177 humans and 73 chimpanzees, we observed a human-specific asymmetry in the superior temporal sulcus at the heart of the communication regions and which we have named the "superior temporal asymmetrical pit" (STAP). This 45-mm-long segment ventral to Heschl's gyrus is deeper in the right hemisphere than in the left in 95% of typical human subjects, from infanthood till adulthood, and is present, irrespective of handedness, language lateralization, and sex although it is greater in males than in females. The STAP also is seen in several groups of atypical subjects including persons with situs inversus, autistic spectrum disorder, Turner syndrome, and corpus callosum agenesis. It is explained in part by the larger number of sulcal interruptions in the left than in the right hemisphere. Its early presence in the infants of this study as well as in fetuses and premature infants suggests a strong genetic influence. Because this asymmetry is barely visible in chimpanzees, we recommend the STAP region during midgestation as an important phenotype to investigate asymmetrical variations of gene expression among the primate lineage. This genetic target may provide important insights regarding the evolution of the crucial cognitive abilities sustained by this sulcus in our species, namely communication and social cognition.

Organising white matter in a brain without corpus callosum fibres.

Isolated corpus callosum dysgenesis (CCD) is a congenital malformation which occurs during early development of the brain. In this study, we aimed to identify and describe its consequences beyond the lack of callosal fibres, on the morphology, microstructure and asymmetries of the main white matter bundles with diffusion imaging and fibre tractography. Seven children aged between 9 and 13 years old and seven age- and gender-matched control children were studied. First, we focused on bundles within the mesial region of the cerebral hemispheres: the corpus callosum, Probst bundles and cingulum which were selected using a conventional region-based approach. We demonstrated that the Probst bundles have a wider connectivity than the previously described rostrocaudal direction, and a microstructure rather distinct from the cingulum but relatively close to callosal remnant fibres. A sigmoid bundle was found in two partial ageneses. Second, the corticospinal tract, thalamic radiations and association bundles were extracted automatically via an atlas of adult white matter bundles to overcome bias resulting from a priori knowledge of the bundles' anatomical morphology and trajectory. Despite the lack of callosal fibres and the colpocephaly observed in CCD, all major white matter bundles were identified with a relatively normal morphology, and preserved microstructure (i.e. fractional anisotropy, mean diffusivity) and asymmetries. Consequently the bundles' organisation seems well conserved in brains with CCD. These results await further investigations with functional imaging before apprehending the cognition variability in children with isolated dysgenesis.

Planum temporale asymmetry in developmental dyslexia: Revisiting an old question.

Among the various asymmetrical structures of the human brain, the planum temporale, an anatomical region associated with a variety of auditory and language-related processes, has received particular attention. While its surface area has been shown to be greater in the left hemisphere compared to the right in about two-thirds of the general population, altered patterns of asymmetry were revealed by post mortem analyses in individuals with developmental dyslexia. These findings have been inconsistently replicated in magnetic resonance imaging studies of this disorder. In this report, we attempt to resolve past inconsistencies by analyzing the T1-weighted MR images of 81 children (mean age: 11 years, sd: 17 months), including 46 control (25 boys) and 35 dyslexic children (20 boys). We manually outlined Heschl's gyri, the planum temporale and the posterior rami of the Sylvian fissure on participants' brain images, using the same anatomical criteria as in post mortem studies. Results revealed an altered pattern of asymmetry of the planum temporale surface area in dyslexic boys only, with a greater proportion of rightward asymmetrical cases among dyslexic boys compared to control boys. Additionally, analyses of cortical thickness showed no asymmetry differences between groups for any of the regions of interest. Finally, a greater number of Heschl's gyrus full duplications emerged for the right hemisphere of dyslexic boys compared to controls. The present findings confirm and extend early post mortem observations. They also stress the importance of taking gender into account in studies of developmental dyslexia.

How reading acquisition changes children's spoken language network.

To examine the influence of age and reading proficiency on the development of the spoken language network, we tested 6- and 9-years-old children listening to native and foreign sentences in a slow event-related fMRI paradigm. We observed a stable organization of the peri-sylvian areas during this time period with a left dominance in the superior temporal sulcus and inferior frontal region. A year of reading instruction was nevertheless sufficient to increase activation in regions involved in phonological representations (posterior superior temporal region) and sentence integration (temporal pole and pars orbitalis). A top-down activation of the left inferior temporal cortex surrounding the visual word form area, was also observed but only in 9year-olds (3years of reading practice) listening to their native language. These results emphasize how a successful cultural practice, reading, slots in the biological constraints of the innate spoken language network.

A functionally guided approach to the morphometry of occipitotemporal regions in developmental dyslexia: evidence for differential effects in boys and girls.

Developmental dyslexia is a learning disability that specifically affects reading acquisition. Cortical anomalies and gray matter volume differences in various temporal regions have been reported in dyslexic subjects compared with controls. However, consistency between studies is lacking. In the present experiments, we focused our structural analyses on the ventral occipitotemporal regions, defined by their functional response to visual categories. We applied a subject-by-subject functionally guided approach on a total of 76 participants (31 dyslexic children). Cortical thickness was estimated for each participant around his/her peak of specific functional activation to visual words, faces, or places. Results from two independent datasets showed a reduction in thickness in dyslexic children compared with controls in the region responsive to words, in the left hemisphere. Additionally, a gender-by-diagnosis interaction was observed at the same location, due to differences in girls only. To avoid the potential confound of reading level, we also contrasted dyslexic and control children matched for reading performance, and we observed a similar difference, although in a smaller extent of cortex. The present study thus provides the first account of a focal cortical thickness reduction in dyslexia in the subregion of ventral occipitotemporal cortex specifically responsive to visual words, when age, gender, and reading performance are taken into account.

The influence of socioeconomic status on children's brain structure.

Children's cognitive abilities and school achievements are deeply affected by parental socioeconomic status (SES). Numerous studies have reported lower cognitive performance in relation to unfavorable environments, but little is known about the effects of SES on the child's neural structures. Here, we systematically explore the association between SES and brain anatomy through MRI in a group of 23 healthy 10-year-old children with a wide range of parental SES. We confirm behaviorally that language is one of the cognitive domains most affected by SES. Furthermore, we observe widespread modifications in children's brain structure. A lower SES is associated with smaller volumes of gray matter in bilateral hippocampi, middle temporal gyri, left fusiform and right inferior occipito-temporal gyri, according to both volume- and surface-based morphometry. Moreover, we identify local gyrification effects in anterior frontal regions, supportive of a potential developmental lag in lower SES children. In contrast, we found no significant association between SES and white matter architecture. These findings point to the potential neural mediators of the link between unfavourable environmental conditions and cognitive skills.

Cortical networks for vision and language in dyslexic and normal children of variable socio-economic status.

In dyslexia, anomalous activations have been described in both left temporo-parietal language cortices and in left ventral visual occipito-temporal cortex. However, the reproducibility, task-dependency, and presence of these brain anomalies in childhood rather than adulthood remain debated. We probed the large-scale organization of ventral visual and spoken language areas in dyslexic children using minimal target-detection tasks that were performed equally well by all groups. In 23 normal and 23 dyslexic 10-year-old children from two different socio-economic status (SES) backgrounds, we compared fMRI activity to visually presented houses, faces, and written strings, and to spoken sentences in the native or in a foreign language. Our results confirm a disorganization of both ventral visual and spoken language areas in dyslexic children. Visually, dyslexic children showed a normal lateral-to-medial mosaic of preferences, as well as normal responses to houses and checkerboards, but a reduced activation to words in the visual word form area (VWFA) and to faces in the right fusiform face area (FFA). Auditorily, dyslexic children exhibited reduced responses to speech in posterior temporal cortex, left insula and supplementary motor area, as well as reduced responses to maternal language in subparts of the planum temporale, left basal language area and VWFA. By correlating these two findings, we identify spoken-language predictors of VWFA activation to written words, which differ for dyslexic and normal readers. Similarities in fMRI deficits in both SES groups emphasize the existence of a core set of brain activation anomalies in dyslexia, regardless of culture, language and SES, without however resolving whether these anomalies are a cause or a consequence of impaired reading.