Heteromodal conceptual processing in the angular gyrus

Abstract

Concepts bind together the features commonly associated with objects and events to form networks in long-term semantic memory. These conceptual networks are the basis of human knowledge and underlie perception, imagination, and the ability to communicate about experiences and the contents of the environment. Although it is often assumed that this distributed semantic information is integrated in higher-level heteromodal association cortices, open questions remain about the role and anatomic basis of heteromodal representations in semantic memory. Here we used combined neuroimaging evidence from functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI) to characterize the cortical networks underlying concept representation. Using a lexical decision task, we examined the processing of concepts in four semantic categories that varied on their sensory-motor feature associations (sight, sound, manipulation, and abstract). We found that the angular gyrus was activated across all categories regardless of their modality-specific feature associations, consistent with a heteromodal account for the angular gyrus. Exploratory analyses suggested that categories with weighted sensory-motor features additionally recruited modality-specific association cortices. Furthermore, DTI tractography identified white matter tracts connecting these regions of modality-specific functional activation with the angular gyrus. These findings are consistent with a distributed semantic network that includes a heteromodal, integrative component in the angular gyrus in combination with sensory-motor feature representations in modality-specific association cortices.

Figure 1

Behavioral performance on the lexical decision task. (A) Accuracy was near ceiling for all categories. (B) Reaction times were consistently rapid for all categories. Bars represent means with standard errors.

Figure 2

Region of interest (ROI) analyses for heteromodal regions implicated in semantic memory: the angular gyrus (AG) and the middle temporal pole in the anterior temporal lobe (ATL). Parameter estimates were extracted from both ROIs for the activation of each word category relative to the pseudoword baseline. * = parameter estimates differed significantly from zero.

Figure 3

Heteromodal whole-brain analyses showing greater activity for words compared to pseudowords, as well as overlap of activation across categories (center).

Figure 4

Modality-specific activations in sensory and motor regions. (A) Activations from functional localizers for visual, auditory, and hand-motor cortices. These were combined into a single, sensory-motor mask. (B) Modality-specific activations for Sight (red), Sound (blue), and Manipulation (green) word categories, constrained to the sensory-motor mask (shown in white) in an exploratory analysis (p<0.05 voxelwise uncorrected, cluster peak at p<0.005 uncorrected).

Figure 5

Tractography of angular gyrus and sensory-motor regions. Tracts are shown connecting the angular gyrus activation cluster (tan) with activation clusters in sensory-motor regions for Sight (red; left panel), Sound (blue; middle panel), and Manipulation (green; right panel) words.