Anatomical correlates of sentence comprehension and verbal working memory in neurodegenerative disease

Abstract

This study investigates whether sentence comprehension and nonsyntactic verbal working memory (vWM) are sustained by the same or by different neural systems. Scores in a sentence-picture matching task and in digits backward (DB) were correlated with magnetic resonance imaging voxelwise gray matter volumes using voxel-based morphometry in 58 patients with neurodegenerative diseases. Results showed that overall sentence comprehension scores, regardless of grammatical structure, correlated with gray matter volumes in the left temporoparietal region, whereas DB scores correlated with dorsolateral prefrontal and inferior parietal volumes. Comprehension of multiclausal relative sentences (type 3) significantly correlated with voxels in the dorsal portion of the left inferior and middle frontal gyri. When DB and multiclausal relative sentences were directly compared, they showed overlapping neural substrates in the dorsolateral left frontal region, supporting a single source of vWM for syntactic and nonsyntactic tasks. Within this large area of common involvement, a small portion of pars triangularis showed an independent effect of multiclausal sentences, whereas a region in the middle frontal gyrus showed greater correlation with DB. This study reconciles two opposing views, which hold that sentence comprehension and vWM rely on either the same or different anatomical resources.

Figure 1.

a, Main effects of total CYCLE-R accuracy (blue). b, DB (green) scores. c, Type 3 sentences (multiclausal relatives; red). The plots show the relationship between gray matter volumes in arbitrary units (y-axis) and the task scores in the x-axis for each analysis; in particular, the gray matter volumes represent the highest peak of each contrast. Results are superimposed on the three-dimensional rendering of the Montreal Neurological Institute standard brain and displayed at a threshold of p < 0.001, uncorrected.

Figure 2.

a, Conjunction of type 3 sentences and DB (yellow) showing regions that correlate with both variables. b, Independent effect of accuracy for type 3 (red) and DB (green), indicating regions that show correlation with each variable. The design matrix illustrates covariates of interest and confounding variables. Results are superimposed on the three-dimensional rendering of the Montreal Neurological Institute standard brain and displayed at a threshold of p < 0.001, uncorrected.