Situating the left-lateralized language network in the broader organization of multiple specialized large-scale distributed networks.

Rodrigo M Braga,Hannah C Becker,Randy L Buckner,Lauren M Dinicola

doi:10.1152/jn.00753.2019

Abstract

Using procedures optimized to explore network organization within the individual, the topography of a candidate language network was characterized and situated within the broader context of adjacent networks. The candidate network was first identified using functional connectivity and replicated across individuals, acquisition tasks, and analytical methods. In addition to classical language regions near the perisylvian cortex and temporal pole, regions were also observed in dorsal posterior cingulate, midcingulate, and anterior superior frontal and inferior temporal cortex. The candidate network was selectively activated when processing meaningful (as contrasted with nonword) sentences, whereas spatially adjacent networks showed minimal or even decreased activity. Results were replicated and triplicated across two prospectively acquired cohorts. Examined in relation to adjacent networks, the topography of the language network was found to parallel the motif of other association networks, including the transmodal association networks linked to theory of mind and episodic remembering (often collectively called the default network). The several networks contained juxtaposed regions in multiple association zones. Outside of these juxtaposed higher-order networks, we further noted a distinct frontotemporal network situated between language regions and a frontal orofacial motor region and a temporal auditory region. A possibility is that these functionally related sensorimotor regions might anchor specialization of neighboring association regions that develop into a language network. What is most striking is that the canonical language network appears to be just one of multiple similarly organized, differentially specialized distributed networks that populate the evolutionarily expanded zones of human association cortex.NEW & NOTEWORTHY This research shows that a language network can be identified within individuals using functional connectivity. Organizational details reveal that the language network shares a common spatial motif with other association networks, including default and frontoparietal control networks. The language network is activated by language task demands, whereas closely juxtaposed networks are not, suggesting that similarly organized but differentially specialized distributed networks populate association cortex.

Highlights

The association cortex comprises a mosaic of distributed networks that each interconnect regions in prefrontal, parietal, temporal, and midline cortices (Goldman-Rakic 1988; see Mesulam 1981; 1990)
Organizational details suggest that the network 1) is distinct but spatially adjacent to the default and frontoparietal control networks throughout the cortex; 2) has a distributed spatial motif that parallels other association networks; 3) involves upwards of nine cortical regions in the left hemisphere alone, some of which extend beyond the classical language zones and have not been previously emphasized; and 4) responds in an anatomically specific manner to language task demands, with adjacent networks showing minimal or no
Motivated by the hypothesis that the location of prominent language network regions may be explained by their proximity to orofacial motor and auditory regions, we initially explored the functional anatomy of these regions in two individuals (Figs. 7 and 8)

Summary

Introduction

The association cortex comprises a mosaic of distributed networks that each interconnect regions in prefrontal, parietal, temporal, and midline cortices (Goldman-Rakic 1988; see Mesulam 1981; 1990). One hypothesis is that the broad organization of higher-order association cortex is established early in development, with subsequent specialization of cortical zones into distinct networks by activity-dependent processes (Buckner and DiNicola 2019). The description of interconnected anterior and posterior language regions inspires much of the contemporary study of human brain networks. The classic perisylvian language system, initially identified through case studies of patients with aphasia, included an extended region encompassing inferior frontal gyrus (IFG) just rostral to motor cortex (i.e., Broca’s area) and the posterior superior temporal cortex (pSTC; i.e., Wernicke’s area; see Geschwind 1970). Classical and contemporary findings on the anatomy of language function support a specialized, left-lateralized network that involves multiple distributed anterior and posterior association regions

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