White matter fascicles and cortical microstructure predict reading-related responses in human ventral temporal cortex

Abstract

HighlightsThe ILF, AF and VOF predict the spatial layout of reading-related responses in VTC Gray matter microstructure improves the prediction of reading-related responses Fascicles and gray matter structure together predict the location of the VWFA Abstract Reading-related responses in the lateral ventral temporal cortex (VTC) show a consistent spatial layout across individuals, which is puzzling, since reading skills are acquired during childhood. Here, we tested the hypothesis that white matter fascicles and gray matter microstructure predict the location of reading-related responses in lateral VTC. We obtained functional (fMRI), diffusion (dMRI), and quantitative (qMRI) magnetic resonance imaging data in 30 adults. fMRI was used to map reading-related responses by contrasting responses in a reading task with those in adding and color tasks; dMRI was used to identify the brain's fascicles and to map their endpoints density in lateral VTC; qMRI was used to measure proton relaxation time (T1), which depends on cortical tissue microstructure. We fit linear models that predict readingrelated responses in lateral VTC from endpoint density and T1 and used leave-one-subject-out cross-validation to assess prediction accuracy. First, by using a subset of our participants (N=10, feature selection set), we find that i) endpoint density of the arcuate fasciculus (AF), inferior longitudinal fasciculus (ILF), and vertical occipital fasciculus (VOF) are significant predictors of reading-related responses, and ii) cortical T1 of lateral VTC further improves the predictions of the fascicle model. Next, in the remaining 20 participants (validation set), we showed that a linear model that includes T1, AF, ILF and VOF significantly predicts i) the map of reading-related responses across lateral VTC and ii) the location of the visual word form area, a region critical for reading. Overall, our data-driven approach reveals that the AF, ILF, VOF and cortical microstructure have a consistent spatial relationship with an individual's reading-related responses in lateral VTC.

General object-based features account for letter perception

“…Constraints imposed by connectivity in the brain may also limit what neural populations language regions can read-out from, making the learning process more difficult. The visual word form area exhibits preferential functional and structural connectivity with language regions of the brain (Stevens et al, 2017; Yeatman et al, 2013), and its location can be predicted based on measurements of structural connectivity (Grotheer et al, 2021; Saygin et al, 2016). These connectivity constraints may prevent the learning of read-out mechanisms operating over the entire population code of inferotemporal cortex, instead requiring read-out from the visual word form area (Hannagan et al, 2015).…”

White matter connections of high-level visual areas predict cytoarchitecture better than category-selectivity in childhood, but not adulthood

“…This process gave us the functionally defined white matter fascicles for each functional ROI. Previous work showed that out of those fascicles classified by AFQ, only 5 fascicles connect to VTC: the inferior longitudinal fasciculus (ILF), inferior frontal occipital fasciculus (IFOF), arcuate fasciculus (AF), posterior arcuate fasciculus (pAF), and vertical occipital fasciculus (VOF) (Ben-Shachar et al 2007;Thomas et al 2009;Wandell and Yeatman 2013;Yeatman et al 2013;Tavor et al 2014;Gomez et al 2015;Song et al 2015;Weiner et al 2016;Kay and Yeatman 2017;Lerma-Usabiaga et al 2018;Broce et al 2019;Grotheer et al 2019;Grotheer, Yeatman, et al 2021). To determine the fascicle connectivity profile, we calculated the distribution of its connections across these five fascicles for each functional ROI in each subject.…”

“…We first examined the fascicle connectivity profiles of VTC face-and wordselective regions in each individual's brain. There are five fascicles that connect to visual regions in VTC (Ben-Shachar et al 2007;Thomas et al 2009;Wandell and Yeatman 2013;Yeatman et al 2013;Tavor et al 2014;Gomez et al 2015;Song et al 2015;Weiner et al 2016;Kay and Yeatman 2017;Lerma-Usabiaga et al 2018;Broce et al 2019;Grotheer et al 2019;Grotheer, Yeatman, et al 2021) (Catani et al 2002), which connects the occipital lobe and frontal lobe, the inferior longitudinal fasciculus (ILF) (Catani et al 2002), which connects the occipital lobe and ventral temporal lobe, the arcuate fasciculus (AF) (Catani et al 2002), which connects the ventral temporal lobe and the frontal lobe, the posterior arcuate fasciculus (pAF) (Weiner, Yeatman, et al 2017), which connects the ventral temporal lobe and the parietal lobe, and the vertical occipital fasciculus (VOF) (Yeatman, Weiner, et al 2014;Takemura et al 2016;Weiner, Yeatman, et al 2017), which connects the ventral and dorsal occipital lobe. Therefore, our fascicle connectivity analysis will focus on these five fascicles.…”

“…Classic theories suggest that function, cytoarchitecture, and connectivity all contribute to cortical organization (Zeki and Shipp 1988;Van Essen et al 1992;Amunts and Zilles 2015). While past work has investigated the relationship between white matter and category-selectivity (Thomas et al 2009;Saygin et al 2011;Gschwind et al 2012;Pyles et al 2013;Yeatman et al 2013;Bouhali et al 2014;Gomez et al 2015;Osher et al 2016;Saygin et al 2016;Grotheer et al 2019;Li et al 2020;Grotheer, Yeatman, et al 2021) cytoarchitecture and category-selectivity , and white matter and cytoarchitecture (Johansen-Berg et al 2004;Klein et al 2007), there has been limited research on the interplay between all three factors, which is the focus of the present study.…”

“…We used a fMRI localizer experiment (Stigliani et al 2015) to define functional ROIs in each individual's brain and dMRI data to generate a whole brain white matter connectome for each individual. We intersected each participant's whole brain connectome with their functional ROIs to identify the functionally defined white matter associated with each functional ROI (Grotheer et al 2019;Finzi et al 2021;Grotheer, Yeatman, et al 2021). We then tested if the functionally defined white matter of face (pFus-and mFus-faces) and word-selective regions (pOTS-and mOTS-words) is linked to category, cytoarchitecture, or both, and if they change from childhood to adulthood.…”