Children with reading disorder show modality independent brain abnormalities during semantic tasks

Abstract

Neuroimaging studies have suggested that left inferior frontal gyrus, left inferior parietal lobule and left middle temporal gyrus are critical for semantic processing in normal children. The goal of the present functional magnetic resonance imaging (fMRI) study was to determine whether these regions are systematically related to semantic processing in children (9- to 15-year-old) diagnosed with reading disorders (RD). Semantic judgments required participants to indicate whether two words were related in meaning. The strength of semantic association varied continuously from higher association pairs (e.g., king–queen) to lower association pairs (e.g. net–ship). We found that the correlation between association strength and activation was significantly weaker for RD children compared to controls in left middle temporal gyrus and left inferior parietal lobule for both the auditory and the visual modalities and in left inferior frontal gyrus for the visual modality. These results suggest that the RD children have abnormalities in semantic search/retrieval in the inferior frontal gyrus, integration of semantic information in the inferior parietal lobule and semantic lexical representations in the middle temporal gyrus. These deficits appear to be general to the semantic system and independent of modality.

Introduction

Examining how the difficulty of a semantic task systematically relates to brain activation allows one to be more confident that particular brain region is involved in a specific cognitive process. For example, one study with adults compared brain activation patterns to semantic judgments involving closely related pairs (e.g., king–queen) versus distantly related pairs (e.g., net–ship). Distantly related pairs with weaker semantic association produced more activation in left inferior frontal gyrus as compared to closely related pairs with stronger semantic association. The greater activation in left inferior frontal gyrus was interpreted as evidence for the difficulty of searching/retrieving appropriate semantic features because distantly related pairs shared few semantic features (Fletcher et al., 2000). Indeed, there are many studies showing greater inferior frontal gyrus activation in more difficult semantic tasks and in other cases of increasing retrieval or selection demands (Gurd et al., 2002, Seger et al., 2000, Thompson-Schill et al., 1999, Whatmough et al., 2002). Consistent with previous findings in adults, Chou et al., 2006a, Chou et al., 2006b demonstrated that weaker semantic association in children was correlated with greater activation in left inferior frontal gyrus (BA 45, 47) (Chou et al., 2006a, Chou et al., 2006b). Chou et al., 2006a, Chou et al., 2006b also showed that weaker semantic association in children was correlated with greater activation in left middle temporal gyrus (BA 21). Activation in this region has been implicated in the representation of verbal semantic information when words are presented auditorily or visually (Chee et al., 1999) and semantic priming studies have shown modulation of activation in this region (Devlin et al., 2004, Gold et al., 2006, Rissman et al., 2003). Greater activation in this region for low association pairs may result from more extensive access to semantic representations in order to identify overlapping features.

Chou et al., 2006a, Chou et al., 2006b also showed that stronger semantic association was correlated with greater activation in left inferior parietal lobule (BA 40). Activation in this region has previously been identified in semantic tasks, including associative judgments (Binder et al., 1997), similarity judgments (Price et al., 1999), category judgments (Pugh et al., 1996) and concrete versus abstract word judgments (Chee et al., 1999). Some studies have interpreted the left inferior parietal lobule activation as related to feature integration and semantic categorization to form a coherent concept so that semantic relationships between words can be determined (Grossman et al., 2003). Neuro-anatomical connectivity patterns also suggest that semantic lexical integrative processes involve heteromodal association cortices in the inferior parietal lobule (Mesulam, 1998). High association pairs may involve greater integration because there are more overlapping features between the words or because the shared features are more characteristic of each of the words (Fletcher et al., 2000). Greater integration for high association word pairs may account for the increase in left inferior parietal lobule activation with increasing association strength.

Few studies have used semantic tasks to examine neural activity differences between those with and without reading disorders. Several studies measured brain activation differences between controls and patients with dyslexia during a semantic category judgment task in which single words were presented in the visual modality. Shaywitz et al. (1998) reported that dyslexic adults show less activation in bilateral angular gyrus and more activation in bilateral inferior frontal gyrus (Shaywitz et al., 1998). Shaywitz et al. (2002) later reported that dyslexic children showed less activation than control children in left angular gyrus and bilateral middle temporal gyrus (Shaywitz et al., 2002). Furthermore, higher accuracy across both groups of children was associated with greater activation in bilateral angular gyrus and bilateral middle temporal gyrus. Shaywitz et al. (2003) later investigated differences between persistently poor adult readers and accuracy-improved adult readers (compensated) (Shaywitz et al., 2003). They reported that persistently poor readers showed less activation than accuracy-improved readers in left middle temporal gyrus and control readers showed greater activation than accuracy-improved readers in left middle temporal gyrus. Another study by Pugh et al. (2000) examined functional connectivity in adults with and without reading disorders. They found that left angular gyrus activation was correlated with activation posterior left superior temporal gyrus for the control subjects, but not for patients with dyslexia (Pugh et al., 2000). Altogether, research using the semantic category judgment task shows disruption of the left inferior parietal cortex, left inferior frontal gyrus and left superior/middle temporal cortex in patients with dyslexia.

Other studies have examined the neural correlates of semantic processing in patients with dyslexia using different tasks. Using magnetoencephalography (MEG), Helenius et al. (1999) presented sentences in the visual modality that either ended in a semantically anomalous word or not (Helenius et al., 1999). They found no differences between patients with dyslexia and controls in the location of activation in left superior/middle temporal gyrus, but activation was weaker and delayed by about 100 ms in patients with dyslexia. Using positron emission tomography (PET), Rumsey et al. (1994) presented sentences in the auditory modality and asked control adults and patients with dyslexia to make judgments as to whether two sentences with different syntactic structure had the same meaning (Rumsey et al., 1994). During rest, patients with dyslexia showed less activation in inferior parietal cortex around the angular/supramarginal gyrus. Patients with dyslexia showed greater activation in a right lateral frontal region and were less left lateralized in the same inferior parietal region that produced a group difference during rest. These studies are consistent with the fMRI studies implicating abnormalities in the frontal and temporo-parietal cortices in patients with dyslexia.

Many have argued that the central deficit in reading disorder is phonological processing (Paulesu et al., 2001, Pugh et al., 2000, Shaywitz et al., 1998, Temple et al., 2001) and less attention has been given to whether children with reading disorders have deficits in semantic processing. The goal of the current study was to examine the neural correlates of semantic processing in reading disorder (RD) children by using a parametric manipulation of semantic association to determine if RD children (9- to 15-year-old) exhibit the same correlation between association strength and activation as do age-match control children. If RD children show weaker correlations between association and activation, it would suggest abnormal semantic search/retrieval in the inferior frontal gyrus, integration of semantic information in the inferior parietal lobule and semantic lexical representations in middle temporal gyrus. The advantage of using a parametric manipulation of semantic association is to more precisely determine regions critical for processing meaning-based representations. Furthermore, the examination of semantic processing in RD and normal children in both visual and auditory modalities enables the determination of whether abnormal activation is domain general or modality-dependent.