Common and distinct neural substrates of sentence production and comprehension

Abstract

Functional neuroimaging and lesion-symptom mapping investigations implicate a left frontal-temporal-parietal network for sentence processing. The majority of studies have focused on sentence comprehension, with fewer in the domain of sentence production, which have not fully elucidated overlapping and/or unique brain structures associated with the two domains, particularly for sentences with noncanonical word order. Using voxel-based lesion symptom mapping (VLSM) we examined the relationship between lesions within the left hemisphere language network and both sentence comprehension and production of simple and complex syntactic structures in 76 participants with chronic stroke-induced aphasia. Results revealed shared regions across domains in the anterior and posterior superior temporal gyri (aSTG, pSTG), and the temporal pole (adjusted for verb production/comprehension). Additionally, comprehension was associated with lesions in the anterior and posterior middle temporal gyri (aMTG, pMTG), the MTG temporooccipital regions, SMG/AG, central and parietal operculum, and the insula. Subsequent VLSM analyses (production versus comprehension) revealed critical regions associated with each domain: anterior temporal lesions were associated with production; posterior temporo-parietal lesions were associated with comprehension, implicating important roles for regions within the ventral and dorsal stream processing routes, respectively. Processing of syntactically complex, noncanonical (adjusted for canonical), sentences was associated with damage to the pSTG across domains, with additional damage to the pMTG and IPL associated with impaired sentence comprehension, suggesting that the pSTG is crucial for computing noncanonical sentences across domains and that the pMTG, and IPL are necessary for re-analysis of thematic roles as required for resolution of long-distance dependencies. These findings converge with previous studies and extend our knowledge of the neural mechanisms of sentence comprehension to production, highlighting critical regions associated with both domains, and further address the mechanism engaged for syntactic computation, controlled for the contribution of verb processing.

Keywords: Aphasia; Sentence processing; Syntax; Voxel-based lesion-symptom mapping.

Fig. 1.

A lesion overlap map of 76 participants with aphasia. The map shows regions with no overlap (blue) to maximum overlap (red; N = 58 participants).

Fig. 2.

VLSM maps showing left hemisphere regions significantly associated with sentence performance. Panels A-B: lesions correlated with sentence production (red) and comprehension (blue) measures, after covarying areas associated with spoken verb production and comprehension, respectively, and overlap (purple) between the two maps. Panels C-D: lesions correlated with each domain over- and-above the other domain. All voxels shown in color survived a threshold of p<.001 voxel-level, based on cluster size and permutation method correction (brighter color bars indicate greater t-values).

Fig. 3.

VLSM maps showing left-hemisphere regions that were significantly associated with syntactically complex, noncanonical, sentence performance. Panels A-B: lesions correlated with production (red; p<.001, uncorrected), and comprehension (blue; p<.001, corrected) of noncanonical sentences, after covarying areas associated with canonical sentence production and comprehension, respectively, and overlap (purple) between the two maps (brighter color bars indicate greater t-values).