Elsevier

Brain and Language

Volume 125, Issue 2, May 2013, Pages 146-155
Brain and Language

Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections

https://doi.org/10.1016/j.bandl.2012.04.010Get rights and content

Abstract

Circuitry in ventral occipital-temporal cortex is essential for seeing words. We analyze the circuitry within a specific ventral–occipital region, the visual word form area (VWFA). The VWFA is immediately adjacent to the retinotopically organized VO-1 and VO-2 visual field maps and lies medial and inferior to visual field maps within motion selective human cortex. Three distinct white matter fascicles pass within close proximity to the VWFA: (1) the inferior longitudinal fasciculus, (2) the inferior frontal occipital fasciculus, and (3) the vertical occipital fasciculus. The vertical occipital fasciculus terminates in or adjacent to the functionally defined VWFA voxels in every individual. The vertical occipital fasciculus projects dorsally to language and reading related cortex. The combination of functional responses from cortex and anatomical measures in the white matter provides an overview of how the written word is encoded and communicated along the ventral occipital-temporal circuitry for seeing words.

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

References (69)

  • K.M. O’craven et al.

    Voluntary attention modulates fMRI activity in human MT-MST

    Neuron

    (1997)
  • C.J. Price et al.

    The myth of the visual word form area

    Neuroimage

    (2003)
  • C.J. Price et al.

    The interactive account of ventral occipitotemporal contributions to reading

    Trends in Cognitive Sciences

    (2011)
  • A.M. Rauschecker et al.

    Visual feature-tolerance in the reading network

    Neuron

    (2011)
  • D.C. Van Essen et al.

    The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability

    Vision Research

    (1984)
  • B.A. Wandell et al.

    Visual field maps in human cortex

    Neuron

    (2007)
  • K.S. Weiner et al.

    Sparsely-distributed organization of face and limb activations in human ventral temporal cortex

    Neuroimage

    (2010)
  • K. Amano et al.

    Visual field maps, population receptive field sizes, and visual field coverage in the human MT+ complex

    Journal of Neurophysiology

    (2009)
  • T.J. Andrews et al.

    Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract

    Journal of Neuroscience

    (1997)
  • P.J. Basser et al.

    In vivo fiber tractography using DT-MRI data

    Magnetic Resonance in Medicine

    (2000)
  • M.S. Beauchamp et al.

    Graded effects of spatial and featural attention on human area MT and associated motion processing areas

    Journal of Neurophysiology

    (1997)
  • M. Ben-Shachar et al.

    Differential sensitivity to words and shapes in ventral occipito-temporal cortex

    Cerebral Cortex

    (2007)
  • M. Ben-Shachar et al.

    The development of cortical sensitivity to visual word forms

    Journal of Cognitive Neuroscience

    (2011)
  • J.R. Binder et al.

    The topography of callosal reading pathways

    Brain

    (1992)
  • S. Brem et al.

    Brain sensitivity to print emerges when children learn letter-speech sound correspondences

    Proceedings of the National Academy of Sciences of the United States of America

    (2010)
  • A.A. Brewer et al.

    Visual field maps and stimulus selectivity in human ventral occipital cortex

    Nature Neuroscience

    (2005)
  • J.R. Cavanaugh et al.

    Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons

    Journal of Neurophysiology

    (2002)
  • L.C. Chang et al.

    Restore: Robust estimation of tensors by outlier rejection

    Magnetic Resonance in Medicine

    (2005)
  • L. Cohen et al.

    Language-specific tuning of visual cortex? Functional properties of the visual word form area

    Brain

    (2002)
  • L. Cohen et al.

    Visual word recognition in the left and right hemispheres: Anatomical and functional correlates of peripheral alexias

    Cerebral Cortex

    (2003)
  • A.R. Damasio et al.

    The anatomic basis of pure alexia

    Neurology

    (1983)
  • S. Dehaene et al.

    The visual word form area: A prelexical representation of visual words in the fusiform gyrus

    NeuroReport

    (2002)
  • S. Dehaene et al.

    How learning to read changes the cortical networks for vision and language

    Science

    (2011)
  • J.T. Devlin et al.

    The role of the posterior fusiform gyrus in reading

    Journal of Cognitive Neuroscience

    (2006)
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