Converging evidence for functional and structural segregation within the left ventral occipitotemporal cortex in reading

Abstract

The ventral occipitotemporal cortex (vOTC) is crucial for recognizing visual patterns, and previous evidence suggests that there may be different subregions within the vOTC involved in the rapid identification of word forms. Here, we characterize vOTC reading circuitry using a multimodal approach combining functional, structural, and quantitative MRI and behavioral data. Two main word-responsive vOTC areas emerged: a posterior area involved in visual feature extraction, structurally connected to the intraparietal sulcus via the vertical occipital fasciculus; and an anterior area involved in integrating information with other regions of the language network, structurally connected to the angular gyrus via the posterior arcuate fasciculus. Furthermore, functional activation in these vOTC regions predicted reading behavior outside of the scanner. Differences in the microarchitectonic properties of gray-matter cells in these segregated areas were also observed, in line with earlier cytoarchitectonic evidence. These findings advance our understanding of the vOTC circuitry by linking functional responses to anatomical structure, revealing the pathways of distinct reading-related processes.

Keywords: functional and structural MRI; quantitative MRI; reading; visual word form area; visual word recognition.

Fig. 1.

Functional MRI contrasts. (A) OTS in Freesurfer’s fsaverage left hemisphere inflated surface showing the averaged GMax for the LEX (RWvsCS/PW/FF) and PER (RWvsPS/CB/SD) contrasts. The red hexagon corresponds to the clustered LEX contrasts (mOTS), and the blue hexagon corresponds to the clustered PER contrasts (pOTS). The black hexagons correspond to VWFAs identified in previous research as aVWFA, cVWFA, and pVWFA and are drawn just for comparison purposes (4). (B) Functional activation results plotted in MNI152 y and x coordinates. The size of the inner black circle indicates the average T value, and the size of the colored outer circle is scaled to the standard deviation of the coordinate positions. Red outer circles are used for LEX contrasts, and blue outer circles are utilized for PER contrasts. (C) Analogous plot to B with clustered averaged values and standard deviations. The centers of the clusters define mOTS and pOTS. ant. occ. sulcus, anterior occipital sulcus; coord., coordinate; inf. occ. sulcus, inferior occipital sulcus; inf. temp. sulcus, inferior temporal sulcus; val., value.

Fig. 2.

Probabilistic maps for the aggregated LEX and PER contrasts in the OTS and parameter estimates (percentage signal change) analyses for the mOTS and pOTS. (A) The PER contrasts showed two activation clusters in the probabilistic maps which overlapped with the described mOTS and pOTS. LEX contrasts only showed anterior activated clusters in OTS. (B) PER contrasts revealed similar percentage signal change across both the mOTS and pOTS. For LEX contrasts, the mOTS was more strongly engaged than the pOTS. Error bars represent one SEM. n.s., not significant.

Fig. 3.

Associations between functional activation and reading latencies. The green outlines show areas where significant associations between fMRI activation and reading behavior RTs (z scores) were found, vertex- and cluster-wise corrected for multiple comparisons (P = 0.05). (A) Associations between the aggregated LEX contrast fMRI activation with CS (A1) and RW (A2) RTs (z scores). (B) Cortical associations between aggregated PER contrasts fMRI activation with CS (B1) and RW (B2) RTs (z scores). The scatterplots show the averaged functional t values inside the green outlined regions (horizontal axis) against the behavioral indices RT z scores (vertical axis). The mOTS (red hexagon) and pOTS (blue hexagon) are rendered as references.

Fig. 4.

Associations between functional activations and the cortical endings of the tracts of interest. (A) A 3D representation of the pAF and vOF tracts for the left hemisphere of a representative subject, in standard axial, sagittal, and coronal views. (B) Average inflated surface rendering probabilistic maps (thresholded at 20%) of the pAF (B1) and vOF (B2) tract cortical endings in the vOTC cortex. In the probabilistic map, red indicates that a high percentage of subjects showed a correspondence between the tract and that vertex, green indicates medium correspondence, and blue indicates low correspondence. Note the outlines of the mOTS (red) and pOTS (blue) superimposed: The mOTS corresponds to the pAF cortical endings and the intersection of the cortical endings of both tracts, and the pOTS overlaps with the cortical endings of the vOF. (C) The same white-matter cortical endings from B, but projected into MNI x and y axes, with pAF in yellow and vOF in blue. Both graphs in C show the same projections, but they overlay specific (C1) and clustered (C2) contrasts (the LEX cluster defines the mOTS and the PER cluster the pOTS). The size of the inner black circle indicates the average t value, and the size of the outer circle is scaled to the standard deviation of the coordinate positions.

Fig. 5.

White-matter cortical endings and T1 relaxation time results on the left OTS. (A) pAF, vOF, and the intersection of the cortical ending probabilistic maps on the left hemisphere. The red hexagon corresponds to mOTS, and the blue hexagon corresponds to pOTS. The orange outline corresponds to the cytoarchitectonic area FG4, and the light blue outline to cytoarchitectonic area FG2 (13). The intersection of the pAF and vOF cortical tract endings roughly coincides with the separation between FG2 and FG4 cytoarchitectonic areas. B1 shows the same mOTS, pOTS, FG2, and FG4 area outlines, with an additional green outline corresponding to the cluster of significant association between the averaged PER contrasts fMRI T values, and the reading behavior index (CS detection RTs in the lexical decision task). The heatmap corresponds to the T1 relaxation values, which can be seen enlarged in B2. (B3) Comparison of T1 relaxation times in mOTS and pOTS: Left shows violin plots representing the different T1 relaxation values in each ROI, and the significance and effect size of a simple t test between these values; Right shows a scatterplot with the individual subject values in pOTS plotted against the equivalent mOTS values. Almost all values systematically lie below the identity line, and the T1 relaxation values of the mOTS and pOTS show a highly predictable relation.

Fig. 6.

Averaged T values in each vertex plotted along the y axis for averaged PER (red) and LEX (cyan) functional contrasts across subjects and x–z locations. The red box represents the location of the mOTS and the blue box the location of the pOTS. The horizontal parallel black lines indicate the maxima inside the pOTS and mOTS for the PER and LEX averaged functional contrasts. Thus, the gray two-headed arrows indicate the difference of response in the pOTS and mOTS due to visual word form signal.

Fig. 7.

Examples of stimuli for the seven experimental conditions and the task included in the functional localizers. (i) RW. (ii) PW. (iii) CS. (iv) PS. (v) SD. (vi) CB. (vii) FF. (t1) Example of task stimuli.

Fig. 8.

Left vOTC area of interest (in red) used as a mask in the fMRI analysis and regional subdivisions within the vOTC. (A) Left hemisphere pial surface renderings in lateral (A1), ventral (A2), and posterior (A3) perspectives. (B) Left vOTC on an inflated Freesurfer fsaverage brain, with dark areas indicating sulci and light areas indicating gyri. (C) Regional subdivisions within the left vOTC area of interest. The litVWFA comprises three regions described in the literature: aVWFA, cVWFA, and pVWFA. The other four regions in aa-ca-cp-pp were manually designed to cover the litVWFA region and the OTS without overlaps or empty spaces between them. They were organized along an anterior–posterior gradient.