Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections
Graphical abstract
Highlights
► We describe the cortical architecture and white matter tracts of the visual word form area (VWFA). ► The VWFA is adjacent to visual field maps VO-1 and VO-2 and close to the motion selective cortex (hMT). ► The vertical occipital fasciculus connects the VWFA to the angular gyrus and lateral occipital lobe.
Introduction
In their studies of reading disorders in neurological patients, Warrington and colleagues found support for the existence of a visual word-form system “which parses (multiply and in parallel) letter strings into ordered familiar units and categorizes these units visually (p. 110)”. The methods of neurology available to Warrington and colleagues yielded inconsistent evidence about the location of this system. They speculated that the anatomical locus of acquired dyslexia might be in ventral occipital temporal cortex (Kinsbourne & Warrington, 1963) or in temporal parietal cortex (Warrington & Shallice, 1980).
During the following decades, advances in neuroimaging measurements provided compelling evidence that regions within ventral occipital-temporal (VOT) cortex are part of the network for skilled reading (Dehaene et al., 2002, Nobre et al., 1994, Petersen et al., 1990, Price et al., 1994, Salmelin et al., 2000, Salmelin et al., 1996, Wandell, 2011, Wandell et al., 2012). Damage in this region or nearby white matter can result in selective reading deficits (Cohen et al., 2003, Damasio and Damasio, 1983, Epelbaum et al., 2008, Gaillard et al., 2006, Greenblatt, 1973); VOT responses are relatively weak in poor readers (Maisog, Einbinder, Flowers, Turkeltaub, & Eden, 2008); in healthy skilled readers, VOT circuitry is highly responsive to visual word forms (Ben-Shachar et al., 2007b, Dehaene et al., 2002, Dehaene et al., 2011, Mccandliss et al., 2003); during development, improvements in reading performance are correlated with increases in VOT responses to written words (Ben-Shachar et al., 2011, Brem et al., 2010, Maurer et al., 2005). Cohen and colleagues proposed that within the extensive cortical region of VOT there is a specific location – the visual word form area (VWFA) – that is the key neuronal circuitry that learns to recognize word forms (Cohen et al., 2002). The specific functional role of the VWFA within the word-form system is debated (Dehaene and Cohen, 2011, Price and Devlin, 2003, Price and Devlin, 2011, Vogel et al., 2011).
Skilled reading must involve multiple brain regions. Thus, Warrington’s observations that damage in either VOT or temporal parietal cortex may impair reading are still relevant. For example, Greenblatt (1973) reported that damage to the vertical occipital fasciculus, a fiber tract that connects ventral occipital with dorsal–lateral occipital regions, results in pure alexia, also called alexia without agraphia or word blindness. Thus damage affecting either cortical region, or the circuitry carrying signals between them, may result in letter-by-letter reading.
There is no definitive demonstration of a cortical circuit that performs a single cognitive function. It is particularly unlikely that a region dedicated uniquely to reading exists; after all, reading has only become important to society over the last few hundred years. To understand the VWFA function, and how this might contribute to reading, we can rely on two general cortical principles. First, cortical circuits with similar functions are often clustered together (Brewer et al., 2005, Wandell et al., 2007); such clustered regions are typically connected by the U-fibers system within the white matter. To understand the VWFA’s role in reading we should consider the properties of adjacent cortical circuitry. Second, cortical circuits communicate with specific and targeted distant cortical regions via long-range axon bundles. To further understand the role of the VWFA’s role in reading, it will be helpful to delineate its long-range connections.
Improvements in the resolution and signal quality of functional and structural magnetic resonance imaging (MRI) have made it possible to map reliably the VWFA and nearby cortical circuitry in single subjects using functional MRI (fMRI), and to estimate long-range inputs and outputs using diffusion weighted imaging (DWI). The fMRI measurements situate the VOT circuitry involved in seeing words with respect to other important cortical regions; the diffusion measurements provide insight into the long-range connections between VOT and other cortical regions. Recent reviews have emphasized the importance of a circuit diagram for reading, and specifying the inputs and outputs of the VWFA (Price and Devlin, 2011, Wandell et al., 2012). Here, we describe new measurements of these properties in the brains of individual subjects.
Section snippets
Methods and materials
The subjects and data used in this study have been described in previous reports from our group (Ben-Shachar et al., 2007a, Rauschecker et al., 2011, Yeatman et al., 2011).
Visual field maps and the VWFA
Responses in V1 and nearby cortical regions (V2, V3, hV4, VO-1, VO-2) are organized into retinotopic maps (Wandell and Winawer, 2010, Wandell et al., 2007). Viewing a single word evokes a series of responses in several of these maps (Fig. 1). A word evokes a response in primary visual cortex (V1) at a position that corresponds to the word’s visual field position; for example, a word positioned on the horizontal meridian, just to the right of fixation, elicits a response in the depth of
Discussion
The VWFA is located near ventral visual field maps and probably receives direct input from these maps (Fig. 1). The VWFA is adjacent and lateral to visual field maps VO-1 and VO-2 in all subjects. Between subjects, the VWFA position varies significantly with respect to sulcal and gyral landmarks and less with respect to the visual field maps. Within subjects the responses that define the VWFA position are relatively stable across time (Fig. 2).
The ILF and IFOF pass within close proximity of the
Acknowledgments
This work was supported by NIH Grants EY015000 and EY03164 to Brian A. Wandell; an NSF Graduate Research Fellowship to Jason D. Yeatman; the Medical Scientist Training Program and a Bio-X Graduate Student Fellowship to Andreas Rauschecker. We thank Jonathan Winawer for help collecting retinotopy data and with definition of retinotopic maps. We thank Michal Ben-Shachar and Robert F. Dougherty for assistance with VWFA localizer data and diffusion weighted imaging data. We thank Lee M. Perry for
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2021, NeuroImageCitation Excerpt :The present study also extends these previous results and reveals novel information about the structural white matter connectometry anomalies underlying dyslexia. The results suggest that dyslexia is underpinned by structural dysconnectivity in a left-lateralized network interconnecting frontotemporal (uncinate fasciculus, superior longitudinal fasciculus), frontoparietal (superior longitudinal fasciculus), temporoparietal (superior longitudinal fasciculus, parietal aslant tract/posterior segment of the arcuate fasciculus) and occipitotemporal (vertical occipital fasciculus) regions (Catani et al., 2003, 2002; Catani and Thiebaut de Schotten, 2008; Panesar et al., 2019; Yeatman et al., 2013). Our results can be viewed as evidence that supports both the dual route model of reading (Jobard et al., 2003) and the direct and the indirect routes as means for word access: i) Vertical occipital fasciculus forms the core of the visual word forming area circuitry that projects dorsally to language and reading related cortical areas and facilitates encoding of written words (Yeatman et al., 2013), ii) the dorsal stream (i.e., arcuate fasciculus, superior longitudinal fasciculus) is important for phonological awareness, an essential skill in reading development (Vandermosten et al., 2012a; Yeatman et al., 2011), and iii) the uncinate fasciculus, part of the ventral stream, subserves semantic processing (Han et al., 2013) and its greater FA values have been shown to correlate with better semantic performance in healthy adults (De Zubicaray et al., 2011).
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These authors contributed equally to this work.