Functional organization of the neural language system: dorsal and ventral pathways are critical for syntax

Abstract

The core of human language, which differentiates it from the communicative abilities of other species, is the set of combinatorial operations called syntax. For over a century researchers have attempted to understand how this essential function is organized in the brain. Here, we combine behavioral and neuroimaging methods, with left hemisphere-damaged patients and healthy controls, to identify the pathways connecting the brain regions involved in syntactic processing. In a previous functional magnetic resonance imaging study (Tyler LK, Wright P, Randall B, Marslen-Wilson WD, Stamatakis EA. 2010b. Reorganization of syntactic processing following left-hemisphere brain damage: does right-hemisphere activity preserve function? Brain. 133(11):3396-3408.), we established that regions of left inferior frontal cortex and left posterior middle temporal cortex were activated during syntactic processing. These clusters were used here as seeds for probabilistic tractography analyses in patients and controls, allowing us to delineate, and measure the integrity of, the white matter tracts connecting the frontal and temporal regions active for syntax. We found that structural disconnection in either of 2 fiber bundles--the arcuate fasciculus or the extreme capsule fiber system--was associated with syntactic impairment in patients. The results demonstrate the causal role in syntactic analysis of these 2 major left hemisphere fiber bundles--challenging existing views about their role in language functions and providing a new basis for future research in this key area of human cognition.

Figure 1. Lesion Frequency Map

Axial slices showing extent and variability of lesion location within the patient group, as defined by the automated lesion detection method of Stamatakis & Tyler (2005). Numbers above each slice give its z coordinate in MNI space. Colour bar indicates number of patients whose lesions fell within that region.

Figure 2. Left posterior middle temporal and two left inferior frontal clusters activated in the AP-RWO contrast in the fMRI study

These three regions were used as seeds for tractography. Left: colourmap showing T-score activation values for AP-RWO contrast. Right: Binary masks of the three separated clusters: BA45 (red), BA44 (green), pMTG (yellow).

Figure 3. Control group tracts

Surface renderings of dorsal (AF; light blue) and ventral (EmC; orange) pathways. A) Group average pMTG←→BA44 dorsal and pMTG←→BA45 ventral pathways. B) Renderings of the two dorsal pathways (pMTG←→BA44; A, and pMTG←→BA45) in four example subjects.

Figure 4. Patients’ Tracts

Surface renderings of individual tractography reconstructions in the left hemisphere for each of the 16 patients. Grey regions indicate the outer surface of the lesioned tissue, as defined by the automated lesion detection method of Stamatakis & Tyler (2005).

Figure 5. Tract Template Analyses – controls vs. all patients

Mean FA (A) and MD (B) values weighted by tract probability, extracted from dorsal pMTG←→BA44 (AF) and ventral pMTG←→BA45 (EmC) pathway templates following the method of Hua et al. (2008). Controls show significantly higher FA and lower MD than patients within both the AF and EmC template.

Figure 6. Tract Template Analyses – controls vs. patient groups

Mean FA and MD values weighted by tract probability, extracted from dorsal pMTG←→BA44 (AF) and ventral pMTG←→BA45 (EmC) pathway templates, for the control and each of the four patient groups. As predicted by the individual tractography results, patients with an intact dorsal but no ventral connection showed higher MD in the EmC than the AF, whereas patients with intact ventral but no dorsal connections showed higher MD in the AF than the EmC.

Figure 7. Behavioural Data

Top row: Averaged word position effect (WPE) on normal prose (top left) and anomalous prose (top right) conditions in the word monitoring study, shown for the controls and each of the tract status-based patient groups. Bottom row: Average percent semantic (lexical distracter; bottom left) and syntactic (reverse role; bottom right) errors in the sentence-picture matching task. The controls and patients with both tracts show a large AP WPE in the word monitoring study and make few syntactic errors in the sentence-picture matching task, both indicating good syntactic comprehension. D=dorsal (pMTG←→BA44) tract, V = ventral (pMTG←→BA45) tract.