Altered effective connectivity on rapid automatized naming deficits in Chinese children with developmental dyslexia: An rs-fMRI study with Ganger causality analysis

Developmental dyslexia (DD) is a common neurodevelopmental disorder characterized by significant impairment in the development of specific reading skills. Individuals with DD struggle with reading words accurately and fluently, and they exhibit poor decoding and spelling abilities. It is important to note that these difficulties cannot be entirely attributed to intelligence level, vision problems, or improper education (A, 2013). Globally, the prevalence rate of DD ranges from 5% to 17.5% (Peterson and Pennington, 2012; Shaywitz, 1998), with a prevalence of approximately 5%–10% in China (Cai et al., 2020). The negative effects of DD are wide-ranging for children, including academic, behavioral, and psychological problems (Huang et al., 2020).

Rapid Automatized Naming (RAN) is considered a universal marker of DD in different cultures (Carioti et al., 2022). RAN is defined as the ability to quickly name visually presented stimuli like letters, digits, colors, and common objects (Denckla and Rudel, 1974). Numerous studies indicated that RAN is one of the best, perhaps universal, predictors of reading fluency across all known orthographies (Norton and Wolf, 2012). Moreover, literatures showed that children with DD exhibit deficits in RAN (Araujo and Faisca, 2019; Landerl et al., 2013). The deficits are characterized by significantly longer naming time in RAN tasks compared to age-matched groups (S. Silva et al., 2016; M. Yan et al., 2013). A meta-analysis showed that the RAN deficits is the core deficit of DD among Chinese children, with a pooled percentage of 44% (X. Li, Hu and Liang, 2022). However, it's still unclear on the brain mechanisms of RAN deficits in Chinese children with DD.

RAN tasks depend on a complex set of cognitive processes that must work together in perfect concert, such as eye saccades, working memory, orthographic and phonological representations, visual and motor processing, attention and on (Norton and Wolf, 2012). Similarly, imaging studies have revealed that RAN processing engages various brain areas, for example, the cerebellum for motor planning, the middle temporal gyrus for semantic access, the supplementary motor area and pre-motor regions for articulation, and the supramarginal gyrus for graphene-phoneme translation (Cummine et al., 2015). Additionally, RAN tasks recruit dorsal attention regions for visual attention and saccade control, including intraparietal gyrus (Al Dahhan, Kirby, Chen, Brien and Munoz, 2020; Zhou et al., 2019). From a neurobiological perspective, analyzing brain function connectivity can be used to explore how brain areas cooperate to fulfill RAN tasks. A study indicated that increased functional connectivity between left thalamus and right fusiform gyrus was associated with improved RAN ability. On the other hand, literature showed that functional connectivity between the left thalamus and right temporo-parietal regions had a negative association with RAN in children. The authors concluded that the functional coordination between left thalamus and right hemisphere fusiform regions was crucial for RAN, and the negative association could indicate an over-reliance on atypical functional connections in less proficient readers (Cross et al., 2021). Another study demonstrated a positive relationship between functional connectivity of left supramarginal gyrus and bilateral cerebellum VI with RAN in TD children, highlighting the involvement of the cerebellum in RAN (Ang et al., 2020).

However, there is still limited study about brain connectivity differences of RAN between children with DD and TD children. Roger et al. found that children with literacy difficulties have an altered functional connectivity in their reading and attentional networks at the beginning of the literacy acquisition (Mateu-Estivill et al., 2021), and Margolis et al. found that altered efficiency and integration of reading-related network was associated with reading problems (Margolis et al., 2020). A longitudinal study explored that the differences between DD and typically developing (TD) children were primarily observed in the connections between the inferior frontal gyrus and the occipito-temporal cortex. The authors concluded that children with DD exhibited either increased up-regulation (occipito-temporal connections) or down-regulation (inferior frontal gyrus connections) compared to TD children. Therefore, it is reasonable to hypothesize that RAN deficits in Chinese children with DD was associated with altered efficiency and integration of the RAN-related networks.

In clinic, it's difficult to set up targeted brain intervention measures when multiple brain areas are involved in a single task, such as RAN. Fortunately, granger causality analysis (GCA) can be used to calculate effective connectivity (EC). GCA can examine the time-lagged relationships between different brain areas, and provide valuable insights into the directionality of information flow within brain networks (Friston, 1994; Stephan and Friston, 2010). Effective connectivity is distinct from functional connectivity as it measures the effect of one brain region on another in a particular direction, providing crucial information on the causal processes that operate in brain function, revealing how one brain region influences another. One study revealed weaker connections from left inferior temporal gyrus (ITG) to left dorsal inferior frontal gyrus (dIFG) in children with DD, suggesting that the phonological deficits observed in the dIFG may result from weak input from the visuo-orthographic region (X. H. Yan et al., 2021). Unfortunately, it's still limited studies to use GCA to study EC among the brain areas associated with RAN deficits in children with DD.

The study aimed to investigate the differences in EC underlying RAN deficits between Chinese children with DD and TD children. The researchers used GCA methods to identify the brain areas involved in RAN processing and computed whole-brain EC patterns. They also examined the relationship between EC and RAN performance.

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