Neural organization of spoken language revealed by lesion-symptom mapping

Daniel Mirman, Qi Chen, Yongsheng Zhang, Ze Wang, Olufunsho K Faseyitan, H Branch Coslett, Myrna F Schwartz, Daniel Mirman, Qi Chen, Yongsheng Zhang, Ze Wang, Olufunsho K Faseyitan, H Branch Coslett, Myrna F Schwartz

Abstract

Studies of patients with acquired cognitive deficits following brain damage and studies using contemporary neuroimaging techniques form two distinct streams of research on the neural basis of cognition. In this study, we combine high-quality structural neuroimaging analysis techniques and extensive behavioural assessment of patients with persistent acquired language deficits to study the neural basis of language. Our results reveal two major divisions within the language system-meaning versus form and recognition versus production-and their instantiation in the brain. Phonological form deficits are associated with lesions in peri-Sylvian regions, whereas semantic production and recognition deficits are associated with damage to the left anterior temporal lobe and white matter connectivity with frontal cortex, respectively. These findings provide a novel synthesis of traditional and contemporary views of the cognitive and neural architecture of language processing, emphasizing dual routes for speech processing and convergence of white matter tracts for semantic control and/or integration.

Conflict of interest statement

Competing financial interests: All authors declare no competing financial interests.

Figures

Figure 1. Factor analysis results
Figure 1. Factor analysis results
Each panel shows the factor loadings of each test on the named factor. Longer and more saturated bars correspond to stronger loadings with blue indicating positive loading and red indicating negative loading. See Methods for detailed descriptions of the tests and performance measures.
Figure 2. VLSM of Semantic Errors
Figure 2. VLSM of Semantic Errors
VLSM t-map supra-threshold (FDR q = 0.05, t < −2.66) voxels for Semantic Errors factor scores with direct total lesion volume control.
Figure 3. VLSM of Semantic Recognition
Figure 3. VLSM of Semantic Recognition
VLSM of Semantic Recognition factor scores with direct total lesion volume control. Voxels exceeding FDR threshold q = 0.1 are shown in red superimposed on outlines of key white matter tracts: uncinate fasciculus (light blue), inferior fronto-occipital fasciculus (green), and anterior thalamic radiations (blue). Far right panel shows a tractography reconstruction of these tracts and the supra-threshold voxels using the same color scheme. See Methods for details of white matter rendering.
Figure 4. VLSM of Speech Recognition and…
Figure 4. VLSM of Speech Recognition and Production
VLSM t-map showing supra-threshold (FDR q = 0.05) voxels for the Speech Production factor (blue-green) and the Speech Recognition factor (red-yellow) with direct total lesion volume control.

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