Disruption of functional networks in dyslexia: a whole-brain, data-driven analysis of connectivity.
ABSTRACT: Functional connectivity analyses of functional magnetic resonance imaging data are a powerful tool for characterizing brain networks and how they are disrupted in neural disorders. However, many such analyses examine only one or a small number of a priori seed regions. Studies that consider the whole brain frequently rely on anatomic atlases to define network nodes, which might result in mixing distinct activation time-courses within a single node. Here, we improve upon previous methods by using a data-driven brain parcellation to compare connectivity profiles of dyslexic (DYS) versus non-impaired (NI) readers in the first whole-brain functional connectivity analysis of dyslexia.Whole-brain connectivity was assessed in children (n = 75; 43 NI, 32 DYS) and adult (n = 104; 64 NI, 40 DYS) readers.Compared to NI readers, DYS readers showed divergent connectivity within the visual pathway and between visual association areas and prefrontal attention areas; increased right-hemisphere connectivity; reduced connectivity in the visual word-form area (part of the left fusiform gyrus specialized for printed words); and persistent connectivity to anterior language regions around the inferior frontal gyrus.Together, findings suggest that NI readers are better able to integrate visual information and modulate their attention to visual stimuli, allowing them to recognize words on the basis of their visual properties, whereas DYS readers recruit altered reading circuits and rely on laborious phonology-based "sounding out" strategies into adulthood. These results deepen our understanding of the neural basis of dyslexia and highlight the importance of synchrony between diverse brain regions for successful reading.
Project description:Reading is a complex cognitive skill subserved by a distributed network of visual and language-related regions. Disruptions of connectivity within this network have been associated with developmental dyslexia but their relation to individual differences in the severity of reading problems remains unclear. Here we investigate whether dysfunctional connectivity scales with the level of reading dysfluency by examining EEG recordings during visual word and false font processing in 9-year-old typically reading children (TR) and two groups of dyslexic children: severely dysfluent (SDD) and moderately dysfluent (MDD) dyslexics. Results indicated weaker occipital to inferior-temporal connectivity for words in both dyslexic groups relative to TRs. Furthermore, SDDs exhibited stronger connectivity from left central to right inferior-temporal and occipital sites for words relative to TRs, and for false fonts relative to both MDDs and TRs. Importantly, reading fluency was positively related with forward and negatively with backward connectivity. Our results suggest disrupted visual processing of words in both dyslexic groups, together with a compensatory recruitment of right posterior brain regions especially in the SDDs during word and false font processing. Functional connectivity in the brain's reading network may thus depend on the level of reading dysfluency beyond group differences between dyslexic and typical readers.
Project description:Although an extensive literature exists on the neurobiological correlates of dyslexia (DYS), to date, no studies have examined the neurobiological profile of those who exhibit poor reading comprehension despite intact word-level abilities (specific reading comprehension deficits [S-RCD]). Here we investigated the word-level abilities of S-RCD as compared to typically developing readers (TD) and those with DYS by examining the blood oxygenation-level dependent response to words varying on frequency. Understanding whether S-RCD process words in the same manner as TD, or show alternate pathways to achieve normal word-reading abilities, may provide insights into the origin of this disorder. Results showed that as compared to TD, DYS showed abnormal covariance during word processing with right-hemisphere homologs of the left-hemisphere reading network in conjunction with left occipitotemporal underactivation. In contrast, S-RCD showed an intact neurobiological response to word stimuli in occipitotemporal regions (associated with fast and efficient word processing); however, inferior frontal gyrus (IFG) abnormalities were observed. Specifically, TD showed a higher-percent signal change within right IFG for low-versus-high frequency words as compared to both S-RCD and DYS. Using psychophysiological interaction analyses, a coupling-by-reading group interaction was found in right IFG for DYS, as indicated by a widespread greater covariance between right IFG and right occipitotemporal cortex/visual word-form areas, as well as bilateral medial frontal gyrus, as compared to TD. For S-RCD, the context-dependent functional interaction anomaly was most prominently seen in left IFG, which covaried to a greater extent with hippocampal, parahippocampal, and prefrontal areas than for TD for low- as compared to high-frequency words. Given the greater lexical access demands of low frequency as compared to high-frequency words, these results may suggest specific weaknesses in accessing lexical-semantic representations during word recognition. These novel findings provide foundational insights into the nature of S-RCD, and set the stage for future investigations of this common, but understudied, reading disorder.
Project description:The left ventral occipito-temporal cortex (LvOT) is thought to be essential for the rapid parallel letter processing that is required for skilled reading. Here we investigate whether rapid written word identification in skilled readers can be supported by neural pathways that do not involve LvOT. Hypotheses were derived from a stroke patient who acquired dyslexia following extensive LvOT damage. The patient followed a reading trajectory typical of that associated with pure alexia, re-gaining the ability to read aloud many words with declining performance as the length of words increased. Using functional MRI and dynamic causal modelling (DCM), we found that, when short (three to five letter) familiar words were read successfully, visual inputs to the patient's occipital cortex were connected to left motor and premotor regions via activity in a central part of the left superior temporal sulcus (STS). The patient analysis therefore implied a left hemisphere "reading-without-LvOT" pathway that involved STS. We then investigated whether the same reading-without-LvOT pathway could be identified in 29 skilled readers and whether there was inter-subject variability in the degree to which skilled reading engaged LvOT. We found that functional connectivity in the reading-without-LvOT pathway was strongest in individuals who had the weakest functional connectivity in the LvOT pathway. This observation validates the findings of our patient's case study. Our findings highlight the contribution of a left hemisphere reading pathway that is activated during the rapid identification of short familiar written words, particularly when LvOT is not involved. Preservation and use of this pathway may explain how patients are still able to read short words accurately when LvOT has been damaged.
Project description:Do the neural circuits for reading vary across culture? Reading of visually complex writing systems such as Chinese has been proposed to rely on areas outside the classical left-hemisphere network for alphabetic reading. Here, however, we show that, once potential confounds in cross-cultural comparisons are controlled for by presenting handwritten stimuli to both Chinese and French readers, the underlying network for visual word recognition may be more universal than previously suspected. Using functional magnetic resonance imaging in a semantic task with words written in cursive font, we demonstrate that two universal circuits, a shape recognition system (reading by eye) and a gesture recognition system (reading by hand), are similarly activated and show identical patterns of activation and repetition priming in the two language groups. These activations cover most of the brain regions previously associated with culture-specific tuning. Our results point to an extended reading network that invariably comprises the occipitotemporal visual word-form system, which is sensitive to well-formed static letter strings, and a distinct left premotor region, Exner's area, which is sensitive to the forward or backward direction with which cursive letters are dynamically presented. These findings suggest that cultural effects in reading merely modulate a fixed set of invariant macroscopic brain circuits, depending on surface features of orthographies.
Project description:Specific reading comprehension deficit (SRCD) affects up to 10 % of all children. SRCD is distinct from dyslexia (DYS) in that individuals with SRCD show poor comprehension despite adequate decoding skills. Despite its prevalence and considerable behavioral research, there is not yet a unified cognitive profile of SRCD. While its neuroanatomical basis is unknown, SRCD could be anomalous in regions subserving their commonly reported cognitive weaknesses in semantic processing or executive function. Here we investigated, for the first time, patterns of gray matter volume difference in SRCD as compared to DYS and typical developing (TD) adolescent readers (N?=?41). A linear support vector machine algorithm was applied to whole brain gray matter volumes generated through voxel-based morphometry. As expected, DYS differed significantly from TD in a pattern that included features from left fusiform and supramarginal gyri (DYS vs. TD: 80.0 %, p?<?0.01). SRCD was well differentiated not only from TD (92.5 %, p?<?0.001) but also from DYS (88.0 %, p?<?0.001). Of particular interest were findings of reduced gray matter volume in right frontal areas that were also supported by univariate analysis. These areas are thought to subserve executive processes relevant for reading, such as monitoring and manipulating mental representations. Thus, preliminary analyses suggest that SRCD readers possess a distinct neural profile compared to both TD and DYS readers and that these differences might be linked to domain-general abilities. This work provides a foundation for further investigation into variants of reading disability beyond DYS.
Project description:Learning to read involves associating abstract visual shapes with familiar meanings. Embodiment theories suggest that word meaning is at least partially represented in distributed sensorimotor networks in the brain (Barsalou, 2008; Pulvermueller, 2013). We explored how reading comprehension develops by tracking when and how printed words start activating these "semantic" sensorimotor representations as children learn to read. Adults and children aged 7-10 years showed clear category-specific cortical specialization for tool versus animal pictures during a one-back categorisation task. Thus, sensorimotor representations for these categories were in place at all ages. However, co-activation of these same brain regions by the visual objects' written names was only present in adults, even though all children could read and comprehend all presented words, showed adult-like task performance, and older children were proficient readers. It thus takes years of training and expert reading skill before spontaneous processing of printed words' sensorimotor meanings develops in childhood.
Project description:Reading is an important high-level cognitive function of the human brain, requiring interaction among multiple brain regions. Revealing differences between children's large-scale functional brain networks for reading tasks and those of adults helps us to understand how the functional network changes over reading development. Here we used functional magnetic resonance imaging data of 17 adults (19-28 years old) and 16 children (11-13 years old), and graph theoretical analyses to investigate age-related changes in large-scale functional networks during rhyming and meaning judgment tasks on pairs of visually presented Chinese characters. We found that: (1) adults had stronger inter-regional connectivity and nodal degree in occipital regions, while children had stronger inter-regional connectivity in temporal regions, suggesting that adults rely more on visual orthographic processing whereas children rely more on auditory phonological processing during reading. (2) Only adults showed between-task differences in inter-regional connectivity and nodal degree, whereas children showed no task differences, suggesting the topological organization of adults' reading network is more specialized. (3) Children showed greater inter-regional connectivity and nodal degree than adults in multiple subcortical regions; the hubs in children were more distributed in subcortical regions while the hubs in adults were more distributed in cortical regions. These findings suggest that reading development is manifested by a shift from reliance on subcortical to cortical regions. Taken together, our study suggests that Chinese reading development is supported by developmental changes in brain connectivity properties, and some of these changes may be domain-general while others may be specific to the reading domain.
Project description:The impact of learning to read in a mixed approach using both the global and phonics teaching methods on the emergence of left hemisphere neural specialization for word recognition is yet unknown in children. Taking advantage of a natural school context with such a mixed approach, we tested 42 first graders behaviorally and with Fast Periodic Visual Stimulation using electroencephalographic recordings (FPVS-EEG) to measure selective neural responses to letter strings. Letter strings were inserted periodically (1/5) in pseudofonts in 40 s sequences displayed at 6 Hz and were either words globally taught at school, that could therefore be processed by visual whole-word form recognition (global method), or control words/pseudowords eliciting grapheme-phoneme (GP) mappings (phonics method). Results show that selective responses (F/5, 1.2 Hz) were left lateralized for control stimuli that triggered GP mappings but bilateral for globally taught words. It implies that neural mechanisms recruited during visual word processing are influenced by the nature of the mapping between written and spoken word forms. GP mappings induce left hemisphere discrimination responses, and visual recognition of whole-word forms induce bilateral responses, probably because the right hemisphere is relatively more involved in holistic visual object recognition. Splitting the group as a function of the mastery of GP mappings into "good" and "poor" readers strongly suggests that good readers actually processed all stimuli (including global words) predominantly with their left hemisphere, while poor readers showed bilateral responses for global words. These results show that in a mixed approach of teaching to read, global method instruction may induce neural processes that differ from those specialized for reading in the left hemisphere. Furthermore, given their difficulties in automatizing GP mappings, poor readers are especially prone to rely on this alternative visual strategy. A preprint of this paper has been released on Biorxiv (van de Walle de Ghelcke et al., 2018).
Project description:Reading is a complex cognitive ability, which relies on visual and language processing as well as on executive functions (EFs). Recent studies have demonstrated that increased reading ability in children aged 7-17 years is related to greater activation of cognitive control regions during verb generation, a task which merges linguistic and cognitive control ability. The aim of the current study is to determine the relationships between neural circuits specifically related to EF and reading ability. We focused on functional connectivity between the dorsolateral prefrontal cortex (DLPFC), a region involved in EF and is part of the frontoparietal network during a verb generation task, and reading ability in seventeen 8-12-year-old typical readers. Results show positive functional connectivity between the left and right DLPFCs and regions related to cognitive control and visual processing while generating verbs. Increased reading ability was positively correlated with greater functional connectivity between the left and right DLPFCs and right-lateralized visual processing regions. The current study highlights the importance of neural circuits related to EF during both verb generation and reading and points to the role of the right occipital cortex in generating verbs as well as automatic word recognition in typical readers.
Project description:Word-selective neural responses in human ventral occipito-temporal cortex (VOTC) emerge as children learn to read, creating a visual word form area (VWFA) in the literate brain. It has been suggested that the VWFA arises through competition between pre-existing selectivity for other stimulus categories, changing the topography of VOTC to support rapid word recognition. Here, we hypothesized that competition between words and objects would be resolved as children acquire reading skill. Using functional magnetic resonance imaging (fMRI), we examined the relationship between responses to words and objects in VOTC in two ways. First, we defined the VWFA using a words?>?objects contrast and found that only skilled readers had a region that responded more to words than objects. Second, we defined the VWFA using a words?>?faces contrast and examined selectivity for words over objects in this region. We found that word selectivity strongly correlated with reading skill, suggesting reading skill-dependent tuning for words. Furthermore, we found that low word selectivity in struggling readers was not due to a lack of response to words, but to a high response to objects. Our results suggest that the fine-tuning of word-selective responses in VOTC is a critical component of skilled reading.