Multiple dimensions underlying the functional organization of the language network

Abstract

Understanding the different neural networks that support human language is an ongoing challenge for cognitive neuroscience. Which divisions are capable of distinguishing the functional significance of regions across the language network? A key separation between semantic cognition and phonological processing was highlighted in early meta-analyses, yet these seminal works did not formally test this proposition. Moreover, organization by domain is not the only possibility. Regions may be organized by the type of process performed, as in the separation between representation and control processes proposed within the Controlled Semantic Cognition framework. The importance of these factors was assessed in a series of activation likelihood estimation meta-analyses that investigated which regions of the language network are consistently recruited for semantic and phonological domains, and for representation and control processes. Whilst semantic and phonological processing consistently recruit many overlapping regions, they can be dissociated (by differential involvement of bilateral anterior temporal lobes, precentral gyrus and superior temporal gyri) only when using both formal analysis methods and sufficient data. Both semantic and phonological regions are further dissociable into control and representation regions, highlighting this as an additional, distinct dimension on which the language network is functionally organized. Furthermore, some of these control regions overlap with multiple-demand network regions critical for control beyond the language domain, suggesting the relative level of domain-specificity is also informative. Multiple, distinct dimensions are critical to understand the role of language regions. Here we present a proposal as to the core principles underpinning the functional organization of the language network.

Keywords: Control; Language; Meta-analysis; Multiple Demand Network; Phonology; Semantics.

Graphical abstract

Fig. 1

Results for the phonology and semantics domains are shown in blue (left column) and red (right column) respectively. Top row: original results by Vigneau et al., 2006, Vigneau et al., 2011; figures are reproduced with permission from Vigneau et al. (2011). Middle row: formal ALE meta-analysis of the recreated Vigneau et al., 2006, Vigneau et al., 2011 datasets, with 615 foci from 44 experiments for phonology, and 788 foci from 70 experiments for semantics. Bottom row: meta-analysis of full datasets, with 1176 foci from 82 experiments for phonology, and 2819 foci from 209 experiments for semantics.

Fig. 2

Top row: a comparison of the formal ALE analyses conducted for Vigneau et al.’s semantics (red) and phonology (blue) datasets. Bottom row: a comparison of the formal ALE analyses conducted on the full datasets. Left column: the semantic and phonological activation maps are shown overlaid. Overlap may be seen in violet. Right column: formal ALE contrasts (phonology > semantics in blue, semantics > phonology in red).

Fig. 3

Top row: activation map for semantics domain (red) overlaid with semantic control (green, overlap in yellow). Bottom row: activation map for full phonological domain (blue) overlaid with phonological control, represented by hard > easy phonology formal ALE contrast (green, overlap in cyan).

Fig. 4

Top row: activation map of semantic control (red). Second row: map of phonological control regions (blue), represented by hard > easy phonology contrast. Third row: activation map for the n-back working memory domain. Bottom row: map of the multiple demand network from Fedorenko et al. (2013).

Fig. 5

Schematic diagrams of the core organizational principles of the language network, based on the meta-analytic results. Top left: regions implicated in the semantic (red) and phonological (blue) subdomains with overlap shown in purple. Top right: regions implicated for semantic/phonological representation (purple) and control (green). Bottom left: domain-specificity of regions implicated in semantic and phonological control. Domain-general regions are shown in green and subdomain-specific regions in yellow (all of which reflect semantic control regions). Language-general regions would be displayed in light blue, yet no regions were found to be shared between semantics and phonology without a more domain-general role. Bottom right: a proposed multidimensional organization of the language network. The angular gyrus is shaded as its role in semantic representation is highly debated (Humphreys et al., 2015, Cabeza et al., 2012, Seghier, 2013); see Discussion for more detail.