The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses

TLDR

Traditional models emphasize the left posterior temporal cortex for language comprehension, but lesion and imaging studies indicate a broader network whose full extent and white matter pathways remain to be characterized. The study investigated the white matter pathways associated with key language‑comprehension regions using diffusion tensor imaging in healthy subjects. Diffusion tensor imaging and resting‑state functional MRI were employed to map structural and functional connectivity of these regions. Fiber tractography and resting‑state fMRI revealed that left MTG, anterior STG/BA22, STS/BA39, and BA47 form a richly interconnected network linked by the inferior occipito‑frontal fasciculus, arcuate fasciculus, middle and inferior longitudinal fasciculi, and tapetum, with the left posterior MTG showing especially extensive connectivity that underlies its central role in language comprehension.

Abstract

While traditional models of language comprehension have focused on the left posterior temporal cortex as the neurological basis for language comprehension, lesion and functional imaging studies indicate the involvement of an extensive network of cortical regions. However, the full extent of this network and the white matter pathways that contribute to it remain to be characterized. In an earlier voxel-based lesion-symptom mapping analysis of data from aphasic patients (Dronkers et al., 2004), several brain regions in the left hemisphere were found to be critical for language comprehension: the left posterior middle temporal gyrus (MTG), the anterior part of Brodmann's area 22 in the superior temporal gyrus (anterior STG/BA22), the posterior superior temporal sulcus (STS) extending into Brodmann's area 39 (STS/BA39), the orbital part of the inferior frontal gyrus (BA47) and the middle frontal gyrus (BA46). Here, we investigated the white matter pathways associated with these regions using diffusion tensor imaging from healthy subjects. We also used resting-state functional magnetic resonance imaging data to assess the functional connectivity profiles of these regions. Fiber tractography and functional connectivity analyses indicated that the left MTG, anterior STG/BA22, STS/BA39 and BA47 are part of a richly interconnected network that extends to additional frontal, parietal and temporal regions in the two hemispheres. The inferior occipito-frontal fasciculus, the arcuate fasciculus and the middle and inferior longitudinal fasciculi, as well as transcallosal projections via the tapetum were found to be the most prominent white matter pathways bridging the regions important for language comprehension. The left posterior MTG showed a particularly extensive structural and functional connectivity pattern which is consistent with the severity of the impairments associated with MTG lesions and which suggests a central role for this region in language comprehension.