Fronto-temporal brain systems supporting spoken language comprehension

Abstract

The research described here combines psycholinguistically well-motivated questions about different aspects of human language comprehension with behavioural and neuroimaging studies of normal performance, incorporating both subtractive analysis techniques and functional connectivity methods, and applying these tasks and techniques to the analysis of the functional and neural properties of brain-damaged patients with selective linguistic deficits in the relevant domains. The results of these investigations point to a set of partially dissociable sub-systems supporting three major aspects of spoken language comprehension, involving regular inflectional morphology, sentence-level syntactic analysis and sentence-level semantic interpretation. Differential patterns of fronto-temporal connectivity for these three domains confirm that the core aspects of language processing are carried out in a fronto-temporo-parietal language system which is modulated in different ways as a function of different linguistic processing requirements. No one region or sub-region holds the key to a specific language function; each requires the coordination of activity within a number of different regions. Functional connectivity analysis plays the critical role of indicating the regions which directly participate in a given sub-process, by virtue of their joint time-dependent activity. By revealing these codependencies, connectivity analysis sharpens the pattern of structure-function relations underlying specific aspects of language performance.

Figure 1

Classical model of the LH language system.

Figure 2

Structural correlates of regular inflection. Three-dimensional reconstructions of a T1-weighted MRI image showing brain areas where variations in signal density correlate with priming for regularly inflected words at: (a) p<0.001, (b) p<0.01 and (c) p<0.05 voxel thresholds. The clusters shown survived correction at p<0.05 cluster level adjusted for the entire brain. The statistical peak (−55, 36, −1) is in the left inferior frontal gyrus (BA 47), and the cluster extends superiorly into BA 45. At lower thresholds, the cluster extends from Broca's to Wernicke's areas and includes the arcuate fasciculus. The scatter plot shows the relationship between variations in signal density at the most significant voxel (see asterisk on (a)) and individual behavioural scores in the regular and the non-morphological phonological conditions. Adapted from Tyler et al. (2005a).

Figure 3

Functional correlates of regular inflection. The activations are superimposed on the mean T1 image of 18 volunteers. (a) Significant activations for the overall contrast of regulars (real, pseudo and non-word) minus irregulars (real, pseudo and non-word). Clusters were found in the RSTG, LSTG and LIFC. Activation peaks are given in brackets. (b) Significant activations for the contrast of real regulars minus real irregulars. Clusters were found in the RSTG, LSTG, LACC and LIFC. (c) Significant activations for the contrast of regulars (real and non-word) versus additional phoneme (real and non-word). Clusters were found in the RSTG, LSTG and LIFC. Adapted with permission from Tyler et al. (2005c). Copyright © Elsevier.

Figure 4

Functional connectivity analysis of regular inflection. Connectivity analysis in a group of healthy volunteers (20–40 years; based on data reported in Stamatakis et al. 2005). (a) The three-way interaction showing that the LACC predicts greater fronto-temporal interaction (LIFG and LMTG) in the context of regularly inflected when compared with irregularly inflected words. (b) The three-way interaction showing clusters in the RMTG that interact with activity in the RACC and RIFG in the context of regular versus irregular inflected forms. (c) The LMTG cluster predicted by the joint activity of RACC, RIFG for regular versus irregular inflected forms.

Figure 5

Functional connectivity for regular inflection following LH lesion. Connectivity analysis in (a,b) an age-matched control group and (c) patient P1, with extensive perisylvian damage. (a) The three-way interaction for a group of 40–60-year-olds between the two time series derived from the LH peak voxels in the subtractive analysis and the experimental condition (regulars versus irregulars). Predictor time series, derived from maxima in group activation patterns, are shown with asterisks in the LIFG and LACC. These regions predict activity in LMTG in the context of the experimental condition (regulars versus irregulars). (b) RH connectivity (for the contrast regulars–irregulars) for the 40–60 year-olds. Predictor time series are shown here with asterisks in the RIFG and RACC. These regions predict activity in LMTG as well as in the RH. (c) RH connectivity (i.e. three-way interaction between the two time series for the contrast between regulars and irregulars) for patient P1. Predictor time series, derived from maxima in P1's activation patterns (regulars–irregulars), are shown here with asterisks in the RIFG and RINS. The RH connectivity results from the controls (as in (b)) are shown in blue.

Figure 6

Contrasting effects of syntactic and semantic ambiguities. Significant activations (cluster threshold p<0.05 corrected for the entire brain, voxel threshold p<0.01 uncorrected) in LH and RH for (a) the contrast of semantically ambiguous–semantically unambiguous sentences (red) and (b) for the effect of syntactic dominance (blue; based on data reported in Rodd et al. 2004). The x coordinates are shown under each slice.

Figure 7

Functional connectivity analysis of syntactic and semantic ambiguity effects. Connectivity analysis using a predictor time series (marked by asterisks) found to be a statistical peak in the group (young normal) analysis. (a) The contrast of semantically ambiguous–unambiguous activity in the LIFG positively predicts activity in L anterior STG. (b) For syntactic dominance, activity in the LIFG positively predicts activity in bilateral anterior MTG/STG, L posterior MTG/STG and LIPL.

Figure 8

LH connectivity effects for regular inflection and for syntax. Results of connectivity analysis for syntactic dominance (red), from figure 7b, contrasted with parallel results for real regulars versus real irregulars (blue), from figure 4a, both for young controls (p=0.05). Predictor time series for both analyses were located in the LIFG.

Figure 9

Syntactic ambiguity effects for patient P1. (a) LH and RH syntactic ambiguity activations, overlaid on sagittal slices of the patient's T1-weighted scan. The x coordinates are shown under each slice. (b) Connectivity analysis using predictors derived from P1's activation peaks (in L precentral G (blue asterisk) and LMFG (red asterisk)) for syntactic ambiguity, overlaid on the patient's RH. Activation in L precentral gyrus predicts activation in R angular gyrus (in blue); activation in LMFG predicts activation in R angular gyrus, extending to R supramarginal gyrus, RSTG and RIPL (in red).

Figure 10

Semantic ambiguity effects for patient P1. (a) LH and RH semantic ambiguity activations for patient P1, overlaid on the patient's brain. The x coordinates are shown beneath each sagittal slice. (b) Connectivity analysis using predictors derived from P1's activation peak (see asterisk) for semantic ambiguity, overlaid on the patient's brain. Activation in RIFG, denoted by an asterisk, predicts activation in R anterior STG and L posterior MTG.

Figure 11

Semantic and syntactic connectivity effects for patient P2. (a) T1-weighted MR image for patient P2 (with lesion in L posterior MTG, indicated by a white arrow). (b) Connectivity analysis for semantically ambiguous words using predictors (see asterisk) derived from P2's activation peaks, overlaid on his three-dimensional reconstructed brain. Activity in the LIFG positively predicts activity in anterior regions of the LMTG and RSTG (BA 22, peak at MNI 62, −28, 4). (c) Connectivity analysis for syntactic dominance; activity in the RIFG, marked by an asterisk, positively predicts activity in anterior LMTG/STG and posteriorly in bilateral posterior MTG, and IPL.

Figure 12

Disrupted white matter tracts in patient P2. Directional fractional anisotropy sagittal slices from (a) patient P2 (with L posterior temporal damage, see figure 11) and (b) an age-matched control. The colour maps are based on the principal diffusion directions: green, anterior to posterior; blue, inferior to superior; red, left to right. The arrows indicate a disruption in the LH arcuate fasciculus close to the patient's lesion.