Elsevier

NeuroImage

Volume 133, June 2016, Pages 302-312
NeuroImage

Chinese Character and English Word processing in children's ventral occipitotemporal cortex: fMRI evidence for script invariance

https://doi.org/10.1016/j.neuroimage.2016.03.021Get rights and content

Highlights

  • English and Chinese readers activate left OTC while reading their native script.

  • Overlap of activation for English Words and Chinese Characters occurs in left VWFA.

  • Chinese readers show similar activation for characters and objects in left OTC.

  • English readers show less activity to words than objects in left OTC.

Abstract

Learning to read is thought to involve the recruitment of left hemisphere ventral occipitotemporal cortex (OTC) by a process of “neuronal recycling”, whereby object processing mechanisms are co-opted for reading. Under the same theoretical framework, it has been proposed that the visual word form area (VWFA) within OTC processes orthographic stimuli independent of culture and writing systems, suggesting that it is universally involved in written language. However, this “script invariance” has yet to be demonstrated in monolingual readers of two different writing systems studied under the same experimental conditions. Here, using functional magnetic resonance imaging (fMRI), we examined activity in response to English Words and Chinese Characters in 1st graders in the United States and China, respectively. We examined each group separately and found the readers of English as well as the readers of Chinese to activate the left ventral OTC for their respective native writing systems (using both a whole-brain and a bilateral OTC-restricted analysis). Critically, a conjunction analysis of the two groups revealed significant overlap between them for native writing system processing, located in the VWFA and therefore supporting the hypothesis of script invariance. In the second part of the study, we further examined the left OTC region responsive to each group's native writing system and found that it responded equally to Object stimuli (line drawings) in the Chinese-reading children. In English-reading children, the OTC responded much more to Objects than to English Words. Together, these results support the script invariant role of the VWFA and also support the idea that the areas recruited for character or word processing are rooted in object processing mechanisms of the left OTC.

Introduction

Learning to read requires mapping of the written, visual form of a language to its spoken, auditory form. Brain models of reading describe a largely left lateralized network including inferior frontal, temporoparietal, and occipitotemporal cortex (OTC; Dehaene, 2009, Martin et al., 2015, Pugh et al., 2000, Pugh et al., 2001). The contribution of each these regions to the sub-processes of reading has been established, yet the details are continuously being refined. A specific region of left ventral OTC in the mid-fusiform gyrus termed the “visual word form area,” or VWFA (Cohen et al., 2000, Cohen et al., 2002, McCandliss et al., 2003), has been of particular interest because of its role in processing written words. It has been shown that the VWFA responds to words more than to other visual stimuli, such as checkerboards (Cohen et al., 2002), scrambled visual stimuli (Szwed et al., 2011), and line drawings of objects (Baker et al., 2007, Szwed et al., 2011). Also, it responds to written words invariantly in regard to size, position, case, or font (Dehaene et al., 2001, Dehaene et al., 2004). Some investigators also refer to the “visual word form system” (VWFS), recognizing that regions immediately posterior and anterior to the VWFA proper also show some sensitivity to words (Brem et al., 2009, Brem et al., 2010, Olulade et al., 2013a, van der Mark et al., 2009). However, there is an ongoing debate about the characteristics of the VWFA, most notably questioning the specificity of the VWFA to print. Some have argued that this region responds just as much to pictures of objects (Kherif et al., 2011, Mano et al., 2013, Price and Devlin, 2003, Vogel et al., 2012). Independently of this debate on the specificity of the VWFA, it is largely accepted that the VWFA is one of several regions reliably identified during brain imaging studies of reading, in children and adults, as illustrated by a recent meta-analysis (Martin et al., 2015). Interestingly, the posterior portion of the left OTC is engaged more in adults than children (Martin et al., 2015), suggesting an experience/age-dependent increase in the VWFS, consistent with the developmental model of reading advanced by Pugh et al., 2000, Pugh et al., 2001. In adults, training with a novel set of words is associated with increased activity in (Moore et al., 2014) and greater tuning of (Glezer et al., 2015) the VWFA. Further, the left OTC is underactivated in children and adults with the reading disability dyslexia, as demonstrated by several studies and best captured by meta-analyses (Maisog et al., 2008, Richlan et al., 2011).

Of note is that while most studies have been conducted in alphabetic languages, the VWFA is also found to be activated during reading in Chinese, a morphosyllabic (often called “logographic”) writing system. This suggests that despite the difference in visual appearance and in the mapping between written units and language units (mapping principles), the brain utilizes a similar region in the left OTC for reading in Chinese (Nakamura et al., 2012, Perfetti and Tan, 2013). Similar to the work examining the brain bases of alphabetic writing systems described above, real Chinese characters elicit a greater response in the VWFA than do artificial characters (Liu et al., 2008) and scrambled characters (Szwed et al., 2014). Together these findings suggest a consistent and universal role of the VWFA in processing written language.

Dehaene and colleagues explain this consistency across visually dissimilar scripts via the “neuronal recycling hypothesis” (Dehaene and Cohen, 2007, Dehaene et al., 2005). This theory posits that written language, being a recent cultural invention, has not exerted evolutionary pressure on the brain, unlike spoken language, which has had a much longer time to evolve. Accordingly, when learning to read, the brain must recruit regions previously evolved for another purpose. In the case of ventral visual cortex, word reading adopts cortex previously used for processing other categories of visual stimuli such as faces and/or objects (Dehaene and Cohen, 2007, Dehaene et al., 2005). Strong evidence for this hypothesis comes from a study of ex-illiterates (illiterates who learned to read as adults), who showed greater activation to orthographic stimuli in left ventral temporal cortex compared with illiterates. The illiterates, on the other hand, showed greater activation for objects and faces in this region, suggesting that words take precedence over objects once literacy has been acquired (Dehaene et al., 2010).

Consistency of the VWFA across writing systems plays a significant role in the neuronal recycling hypothesis of the VWFA. Evidence for “script invariance” comes from three sources. The first are meta-analyses of adult studies (Bolger et al., 2005, Tan et al., 2005a). For example, Bolger and colleagues drew on publications that independently studied reading in an alphabetic or logographic writing system and grouped these by writing system to generate activation likelihood maps (Bolger et al., 2005). They found that both writing systems activated left OTC (and Chinese also activated right OTC). However, the overlap in the VWFA across both activation likelihood maps was not statistically tested (this is also true for Tan et al. (2005a)).

A second source of evidence comes from studies performed in Chinese L1 speakers who were bilingual in English (Chee et al., 1999, Nelson et al., 2009, Wong et al., 2009). All of these studies showed left OTC activation for English and Chinese. Chee et al. (1999) and Nelson et al. (2009) also showed right hemisphere OTC activation for Chinese characters. Although participants spoke Chinese as their first language, the possibility of bilingual effects on L1 late in life cannot be ruled out. In any case, it is important to have observations of monolingual L1 speakers. In studies designed to assess cross-language bilingual effects, Baker et al. (2007) examined adult English readers with and without experience with written Hebrew. In the group with experience with both scripts, they found greater activation in the VWFA for both Hebrew and English orthographies compared with other visual categories, including Chinese characters (Baker et al., 2007). In the same vein, a study of Japanese Kana, a syllabic system, and Kanji, borrowed from Chinese and thus morphosyllabic, showed overlap in the left VWFA (Nakamura et al., 2005).

The third category of evidence would be studies directly examining native monolingual individuals of logographic and alphabetic writing systems under similar experimental conditions. A recent study (Szwed et al., 2014) of native readers of Chinese and French came close to this, finding that adults demonstrated engagement of the VWFA for both orthographies, despite orthography-specific differences in early visual cortex. However, the Chinese speakers in this study were living in France at the time (for a period of two years or less) and would have been exposed to both spoken and written French, making it more similar to previous studies such as Nelson et al. (2009). Importantly, orthography invariance in VWFA activation has not actually been validated via an empirical study of monolingual beginning readers, which is the ideal situation by which to address this question.

The study of beginning readers affords an opportunity at the early stages of reading acquisition to test for script invariance. Our participants consisted of one group of monolingual (and monoliterate) children in the United States (English readers) and another group of monolingual (and monoliterate) children in China (Chinese readers). Both groups performed the same implicit Single Word Reading task for their native writing system in the scanner (using the same model of scanner in each location) under the same experimental conditions and using the same data acquisition and analysis parameters. Both groups also viewed line drawings of objects as well as words in the other (foreign) writing system. We tested for script invariance by searching for spatial overlap of activity during word or character processing, respectively, among the English and Chinese readers (i.e. their native language), quantified by a conjunction analysis conducted (a) at the level of the whole brain and (b) specifically within the OTC. Based on the work conducted in adults and in keeping with the neuronal recycling hypothesis, we expected to find overlap between the two beginning reading groups' brain activity in OTC, specifically in the VWFA, during the processing of their respective native orthographies.

Next, we characterized each group separately in terms of the functional specialization of the left occipitotemporal pathway for object, word, and character processing. There are reasons to suspect that the invasion or co-opting of object recognition regions in OTC may be especially noticeable in Chinese: There is a greater reliance on orthographic awareness when learning to read Chinese characters (Tan et al., 2005b), and with this one might expect engagement of left OTC in Chinese character processing at the expense of regions subserving object processing. Further, since the response of the VWFA is one that is thought to come about by experience, one would not expect to see VWFA activity during the processing of a writing system with which the participant is not familiar (Baker et al., 2007, Szwed et al., 2011). As such, we examined the activity in response to the other, foreign script (that is, English Words in the Chinese children and vice versa), with the expectation that it will not elicit as much of a response as the native orthography.

The study allowed us to address the following two questions: (1) Is there spatial convergence of the brain regions activated during single word or character processing by English and Chinese readers respectively, and does this convergence fall specifically within the VWFA in support of the neuronal recycling hypothesis? (2) In each group, English and Chinese readers separately, how does signal change in left OTC during word processing in the native writing system compare with signal change during other types of object processing? We expected to find that left OTC regions dedicated to the native writing system would also respond to objects, thus showing signs of object processing cortex being co-opted by print, but to find little response in left OTC to the non-native writing system.

Section snippets

Subjects and behavioral profile

Twenty-six monolingual English readers (mean age 7 years, 3 months) from the greater Washington, D.C., area in the United States and twenty-three Mandarin-speaking, monolingual Chinese readers (mean age 7 years, 1 month) from Beijing, China, completed the behavioral and imaging protocol for this study. After removing subjects for excessive in-scanner motion (see below), seventeen subjects (7 boys, 10 girls) were included in the English-reading group and seventeen subjects (6 boys, 11 girls) were

Behavioral data: in-scanner performance

The task in this study was implicit: Children were not asked to explicitly read the words or characters, or name the objects; rather, they pressed buttons in their left and right hands in response to the relative horizontal position of the stimuli on the screen. As expected based on the nature of the tasks, in-scanner performance accuracy was high for both groups on all stimulus types, all averaging above 93% accuracy. Details for average accuracy (% correct for answered trials) and reaction

Discussion

Left mid-fusiform gyrus has been shown to consistently respond to word reading across cultures, orthographies, and writing systems (Baker et al., 2007, Bolger et al., 2005, Nakamura et al., 2005, Szwed et al., 2014), suggesting a consistent recruitment of ventral visual cortex when learning to read (Dehaene and Cohen, 2007). However, this consistency has yet to be shown within the context of a single study of typically developing, monolingual readers of different writing systems. In this study,

Acknowledgments

This work was supported by the National Institute of Child Health and Human Development (R01HD056107). We thank each of our participants for their time. We are grateful to the staff at the Center for Functional and Molecular Imaging, and the support of the Intellectual and Development Disorders Research Center (IDDRC5P30HD040677). Thanks to Min Xu and Wen Ding for their acquisition of the behavioral and MRI data in Beijing. Thanks to Diana Alkire for editing the manuscript. We are grateful to

References (69)

  • B.D. McCandliss et al.

    The visual word form area: expertise for reading in the fusiform gyrus

    Trends Cogn. Sci.

    (2003)
  • O.A. Olulade et al.

    Developmental differences for word processing in the ventral stream

    Brain Lang.

    (2013)
  • O.A. Olulade et al.

    Dyslexic children lack word selectivity gradients in occipito-temporal and inferior frontal cortex

    NeuroImage Clin.

    (2015)
  • O.A. Olulade et al.

    Abnormal visual motion processing is not a cause of dyslexia

    Neuron

    (2013)
  • C.A. Perfetti et al.

    Write to read: the brain's universal reading and writing network

    Trends Cogn. Sci.

    (2013)
  • C.J. Price et al.

    The myth of the visual word form area

    NeuroImage

    (2003)
  • K.R. Pugh et al.

    Neurobiological studies of reading and reading disability

    J. Commun. Disord.

    (2001)
  • F. Richlan et al.

    Meta-analyzing brain dysfunctions in dyslexic children and adults

    NeuroImage

    (2011)
  • M. Szwed et al.

    Specialization for written words over objects in the visual cortex

    NeuroImage

    (2011)
  • P.E. Turkeltaub et al.

    The neural basis of hyperlexic reading: an fMRI case study

    Neuron

    (2004)
  • S. van der Mark et al.

    Children with dyslexia lack multiple specializations along the visual word-form (VWF) system

    NeuroImage

    (2009)
  • M. Wang et al.

    Chinese–English biliteracy acquisition: cross-language and writing system transfer

    Cognition

    (2005)
  • G. Xue et al.

    Language experience shapes fusiform activation when processing a logographic artificial language: an fMRI training study

    NeuroImage

    (2006)
  • C.I. Baker et al.

    Visual word processing and experiential origins of functional selectivity in human extrastriate cortex

    PNAS

    (2007)
  • D.J. Bolger et al.

    Cross-cultural effect on the brain revisited: universal structures plus writing system variation

    Hum. Brain Mapp.

    (2005)
  • S. Brem et al.

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

    PNAS

    (2010)
  • S. Brem et al.

    Tuning of the visual word processing system: distinct developmental ERP and fMRI effects

    Hum. Brain Mapp.

    (2009)
  • C. Brennan et al.

    Reading acquisition reorganizes the phonological awareness network only in alphabetic writing systems

    Hum. Brain Mapp.

    (2013)
  • M. Brett et al.

    Region of interest analysis using an SPM toolbox

  • M.W. Chee et al.

    Mandarin and English single word processing studied with functional magnetic resonance imaging

    J. Neurosci.

    (1999)
  • L. Cohen et al.

    The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients

    Brain

    (2000)
  • L. Cohen et al.

    Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area

    Brain

    (2002)
  • S. Dehaene

    Reading in the Brain

    (2009)
  • S. Dehaene et al.

    Letter binding and invariant recognition of masked words: behavioral and neuroimaging evidence

    Psychol. Sci.

    (2004)
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