Results of this exploratory study suggest that the dynamic neural network for auditory sentence comprehension in typically developing children and adolescents changes in distinct ways as a function of sentence length and syntactic complexity. Increased bilateral temporal activation was associated with sentence length. Increased activation of the left posterior temporal lobe, right superior temporal gyrus and right insula was associated with syntactic complexity, though this effect was small and must be considered tentative until confirmed with a larger investigation. Our results further suggest that regions of the frontal cortex become more active in response to increasing task demands in children with superior receptive language skills than in children with average language abilities, when receptive language abilities are indexed by either standard scores on formal tests or processing speed on a computerized comprehension task outside of the scanner.
The sentence-verification task was designed to characterize dynamic properties of the language system and identify neural responses associated with individual differences in functional communications skills. This task, popular in the adult aphasia literature, is more natural and less meta-linguistic than other candidate tasks, such as grammaticality judgment. It is useful for demonstrating individual differences on a trial-by-trial basis because it allows for performance monitoring in terms of both accuracy and reaction time. We used three different syntactic structures in each of the stimulus categories. By extending the range of constructions we are likely to extend the range of behavioral and neural responses. Our paradigm was not designed to map specific cognitive functions to specific regions; rather it was designed to detect changes in the overall network response to varying stimulus and subject characteristics.
Sentence comprehension (compared to fixation) activated a bilateral network of cortical regions. Left lateralization for language processing tends to be greater in verbal fluency, verbal working memory and reading tasks than it is in auditory sentence and story comprehension (Gaillard et al., 2004
; Gaillard et al., 2000
; Holland et al., 2001
; Schmithorst et al., 2006
). These findings suggest that under naturalistic circumstances, the right hemisphere is actively involved, possibly equally to the left, in language comprehension. What is as yet unclear is to what extent the two hemispheres are redundant or processing in distinctive manners.
Though still an area of considerable debate, left lateralization, particularly in the inferior frontal gyrus, is often found in comprehension tasks that examine the processing of specific complex syntactic constructions (Ben-Shachar et al., 2003
; Ben-Shachar et al., 2004
), require detection of syntactic violations,(Friederici et al., 2003
) or place high demands on verbal memory (Fiebach, Schlesewsky, Lohmann, von Cramon, & Friederici, 2005
). In general the inferior frontal gyrus is implicated in language tasks with high processing demands. Though we did not find inferior frontal gyrus activation at the group level, the individual differences analysis demonstrated that children with better receptive language skills showed a greater increase in activation in the inferior frontal gyrus on complex sentences than children with average receptive language skills. This finding suggests that the children with the strongest language abilities are activating higher order brain functions when performing a more complex task.
Main effects of both length and difficulty were present in both hemispheres suggesting that increasing task demands draw upon greater resources from both the left and right hemisphere. Many fMRI studies of syntactic complexity hold sentence length constant (Friederici et al., 2003
; Just et al., 1996
; Keller et al., 2001
). In this study we included the sentence length manipulation as a comparison condition for syntactic complexity to determine whether sentence length, in and of itself, would be associated with increased activations in superior and middle temporal lobes and/or parietal and frontal regions, relating to increased processing or memory requirements. We found long sentences increased activation only within the temporal lobe, probably due to increased auditory, linguistic and semantic processing. We found no overlap between areas associated with length and areas associated with complexity. Wernicke’s area showed increased activation in response to complex versus easy sentences, suggesting that irrespective of individual differences in strategy that likely arise from this multimodal paradigm, the left posterior superior temporal lobe is important for the comprehension of syntactically complex sentences in children. Along with Wernicke’s area, a right hemisphere homologue showed a significant effect of sentence complexity at the group level, highlighting that language comprehension in our task required both hemispheres to dynamically adapt to the stimuli.
We found significant negative associations between age and responses to task difficulty in the right fusiform gyrus and right middle frontal gyrus, even though we did not find age effects in the analyses of behavioral data in the laboratory or in the scanner. Age effects on patterns of activation in sentence or narrative processing have been found in some small studies (Booth et al., 2000
; Karunanayaka et al., 2007
; Schmithorst, Holland, & Plante, 2007
; Szaflarski et al., 2006
) though none have specifically examined the relationship between age and adaptability. Our results suggest that as the task demands increase younger children rely more heavily on the fusiform gyrus and middle frontal gyrus to handle the increased difficulty. Increased responses in the fusiform gyrus could indicate that younger children in comparison to older children rely more heavily on visual and semantic information for comprehension as the sentences become more difficult (Schmithorst, Holland, Plante et al., 2007
). This interpretation is consistent with Booth et al (2000)
in which increased activation of visual association areas in children compare to adults was attributed to children relying more heavily on visualization to comprehend language. Given that task performance was not associated with age, the negative association between age and adaptability appears to reflect that the alternative strategy that younger children use is not incompatible with accurate comprehension.
In this sentence comprehension paradigm, we found that two of the measures—PPVT-III and reaction time on TROG-2--were associated with change in the extent of activation for hard versus easy sentences. The regions where changes were related to receptive language abilities included a left hemisphere perisylvian and a right hemisphere deep gray matter area. Processing speed was negatively associated with changes in response to task difficulty in the anterior cingulate and medial frontal gyrus. These were not regions identified in the general task-related maps probably because the participants with relatively weaker language abilities were not activating them differentially in comprehending hard versus easy sentences. Interestingly, these frontal lobe regions are often associated with memory, error monitoring and attention (Badre & Wagner, 2002
; Love et al., 2006
; Rushworth, Walton, Kennerley, & Bannerman, 2004
; van Veen & Carter, 2002
). Processing speed was positively associated changes in response to task difficulty in the right hemisphere, including right inferior frontal gyrus (BA44, 45). This result is analogous with findings in the reading literature; poor readers show greater activation in right hemisphere BA 44, 45 than do good readers (Simos et al., 2002
) Thus, slow language processors, like poor readers, may be recruiting superfluous, suboptimal or compensatory regions in response to increasing task difficulty (Shaywitz & Shaywitz, 2008
). We recognize that the associations between skill level and activation patterns do not necessarily establish a cause-effect relationship; both processes may be related to another underlying process. To elucidate the underlying mechanisms that explain individual differences in children’s language abilities it will be important to measure variations in the neural response to difficulty on a variety of linguistic tasks using ROIs defined on individual brains.
This study was limited by its small sample size and the restricted range of cognitive abilities and relatively high socioeconomic status of the participants. Because we were unable to use corrected p-values these exploratory results should be interpreted cautiously. We plan to attempt to confirm these findings in a larger sample of typically developing children with a greater range of cognitive and language abilities. However, the implications of this study provide an intriguing account of the relationship between individual differences in brain activity and individual differences in receptive language abilities. Based on these findings, future studies employing individual brain analysis methods and larger samples will allow for the investigation of the specific brain regions in which neural responses to task difficulty is related to language skills.
In summary, we have shown that sentence comprehension in children and adolescents is served by a dynamic and distributed network that varies as a function of stimulus demands, receptive language abilities and age. In future work we will extend the methods to include clinical populations, particularly children with language disorders, to determine the degree of network adaptability and sources of individual variation. We also recognize that a dynamic network must rely on rapid communication among brain regions. Though we found bilateral activations, we do not know to what extent the left and right hemisphere are functioning in parallel and to what extent information is being sent from one hemisphere to the other. In the future, we will study children with white matter lesions to begin to address this issue. Finally, we are intrigued to learn if the sentence comprehension network changes as a function of education or interventions for children with poor receptive language skills.