Privileged Functional Connectivity between the Visual Word Form Area and the Language System

Abstract

The visual word form area (VWFA) is a region in the left occipitotemporal sulcus of literate individuals that is purportedly specialized for visual word recognition. However, there is considerable controversy about its functional specificity and connectivity, with some arguing that it serves as a domain-general, rather than word-specific, visual processor. The VWFA is a critical region for testing hypotheses about the nature of cortical organization, because it is known to develop only through experience (i.e., reading acquisition), and widespread literacy is too recent to have influenced genetic determinants of brain organization. Using a combination of advanced fMRI analysis techniques, including individual functional localization, multivoxel pattern analysis, and high-resolution resting-state functional connectivity (RSFC) analyses, with data from 33 healthy adult human participants, we demonstrate that (1) the VWFA can discriminate words from nonword letter strings (pseudowords); (2) the VWFA has preferential RSFC with Wernicke's area and other core regions of the language system; and (3) the strength of the RSFC between the VWFA and Wernicke's area predicts performance on a semantic classification task with words but not other categories of visual stimuli. Our results are consistent with the hypothesis that the VWFA is specialized for lexical processing of real words because of its functional connectivity with Wernicke's area.SIGNIFICANCE STATEMENT The visual word form area (VWFA) is critical for determining the nature of category-related organization of the ventral visual system. However, its functional specificity and connectivity are fiercely debated. Recent work concluded that the VWFA is a domain-general, rather than word-specific, visual processor with no preferential functional connectivity with the language system. Using more advanced techniques, our results stand in stark contrast to these earlier findings. We demonstrate that the VWFA is highly specialized for lexical processing of real words, and that a fundamental factor driving this specialization is its preferential intrinsic functional connectivity with core regions of the language system. Our results support the hypothesis that intrinsic functional connectivity contributes to category-related specialization within the human ventral visual system.

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: VWFA; fMRI; functional connectivity; language; multivoxel pattern analysis; resting-state.

Copyright © 2017 the authors 0270-6474/17/375288-10$15.00/0.

Figures

Figure 1.

Functional localizer. An independent functional localizer was used to identify language regions: VWFA, Wernicke's area (Wern), Broca's area (Broc), and PCG. Activations are t-statistic maps for the contrast words > nameable entities, displayed at node-wise (surface)/voxelwise (volume) threshold p < 0.001; whole-brain threshold p < 0.01, false discovery rate corrected; minimum cluster size of 25 nodes/voxels. a, Group-level analysis (n = 33) identified all left-lateralized core language regions, and very little right-lateralized activation, displayed on the left (L) and right (R) lateral cortical surfaces (top) and on coronal (cor) and axial (ax) volume slices (bottom), in standardized anatomical space (AFNI/SUMA TT_N27). b, Localizer results for an example single participant, displayed as in a in participant's native anatomical space. c, Location of the planum temporale, as defined by FreeSurfer cortical parcellation, displayed on the left lateral cortical surface of a single participant in native anatomical space.

Figure 2.

MVPA. a, b, Representational similarity analysis was used to quantify the ability of the VWFA to discriminate words versus pseudowords (a) and between picture categories (b), relative to the g-VWFA, left i-FFA (L i-FFA), and right i-FFA (R i-FFA) in 26 participants. There were significant crossover interactions for comparisons of the i-VWFA to the L i-FFA and R i-FFA for word/pseudoword versus picture-category discrimination. The i-VWFA was better at discriminating words from pseudowords than all control ROIs (a), and worse at discriminating picture categories than both the L i-FFA and R i-FFA (b). ***p < 0.001; **p < 0.01; *p < 0.05.

Figure 3.

RSFC of the VWFA. a, Whole-brain voxelwise RSFC of the i-VWFA for an example single participant showed strong RSFC (r > 0.5) with Wernicke's area (Wern), Broca's area (Broc), and PCG, displayed on the left lateral cortical surface in native anatomical space. b, VOTC seeds used for the ROI-based RSFC analysis: individually localized left i-FFA (L i-FFA) and i-VWFA for an example single participant in native anatomical space, and the g-VWFA in standardized space, displayed on axial volume slices. c, RSFC of the i-VWFA (n = 33) with core language regions overall was stronger than that of the g-VWFA and L i-FFA (F(2,64) = 5.933, p < 0.01), including Wernicke's area (g-VWFA: t(32) = 2.073, p < 0.05; L i-FFA: t(32) = 2.762, p < 0.01), Broca's area (L i-FFA: t(32) = 2.375, p < 0.05), and PCG (g-VWFA: t(32) = 3.860, p < 0.001; L i-FFA: t(32) = 2.162, p = 0.05). ***p < 0.001; **p < 0.01; *p < 0.05.

Figure 4.

Brain–behavior correlations. a–f, Strength of RSFC of the i-VWFA (n = 33) with Wernicke's area (a) was significantly correlated with accuracy on the semantic classification task for words only (b), marginally for pseudowords (c), but not for all nameable pictures (d), or any of the individual nameable picture categories—e.g., animals (e) and scenes (f). Wern, Wernicke's area; n.s., not significant.