Dynamic spatial organization of the occipito-temporal word form area for second language processing

Neuropsychologia 103 (2017) 20–28

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Dynamic spatial organization of the occipito-temporal word form area for second language processing

MARK

Yue Gaoa, Yafeng Suna,b, Chunming Lua, Guosheng Dinga, Taomei Guoa, Jeffrey G. Malinsc, ⁎ James R. Boothd, Danling Penga, Li Liua, a National Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, People's Republic of China b School of Educational Science, Shanxi University, Taiyuan 030006, People's Republic of China c Haskins Laboratories, New Haven, CT 06511, USA d Department of Psychology and Human Development, Vanderbilt University, Nashville, TN 37203, USA

A R T I C L E I N F O

A B S T R A C T

Keywords: Bilingual Occipito-temporal region Visual word form Proficiency

Despite the left occipito-temporal region having shown consistent activation in visual word form processing across numerous studies in different languages, the mechanisms by which word forms of second languages are processed in this region remain unclear. To examine this more closely, 16 Chinese-English and 14 EnglishChinese late bilinguals were recruited to perform lexical decision tasks to visually presented words in both their native and second languages (L1 and L2) during functional magnetic resonance imaging scanning. Here we demonstrate that visual word form processing for L1 versus L2 engaged different spatial areas of the left occipitotemporal region. Namely, the spatial organization of the visual word form processing in the left occipito-temporal region is more medial and posterior for L2 than L1 processing in Chinese-English bilinguals, whereas activation is more lateral and anterior for L2 in English-Chinese bilinguals. In addition, for Chinese-English bilinguals, more lateral recruitment of the occipito-temporal region was correlated with higher L2 proficiency, suggesting higher L2 proficiency is associated with greater involvement of L1-preferred mechanisms. For English-Chinese bilinguals, higher L2 proficiency was correlated with more lateral and anterior activation of the occipito-temporal region, suggesting higher L2 proficiency is associated with greater involvement of L2-preferred mechanisms. Taken together, our results indicate that L1 and L2 recruit spatially different areas of the occipito-temporal region in visual word processing when the two scripts belong to different writing systems, and that the spatial organization of this region for L2 visual word processing is dynamically modulated by L2 proficiency. Specifically, proficiency in L2 in Chinese-English is associated with assimilation to the native language mechanisms, whereas L2 in English-Chinese is associated with accommodation to second language mechanisms.

1. Introduction The ventral occipito-temporal cortex of the left hemisphere of the brain has been the focus of numerous studies since its identification as a word form selective region (Cohen and Dehaene, 2004; Cohen et al., 2000, 2002b; Dehaene and Cohen, 2011; Dehaene et al., 2002; Mccandliss et al., 2003; Nobre et al., 1994). This region is thought to process orthographic information associated with visual word forms, and its importance in reading has been demonstrated in both alphabetic and non-alphabetic writing systems (Bolger et al., 2005). Despite the finding that visual word form processing engages strikingly consistent localization in the left occipito-temporal cortex of the brain across writing systems (Bolger et al., 2005), reading Chinese (a logographic

⁎

writing system) script has been additionally shown to activate a right homologous region for visual word form processing (Chao et al., 2008; Guo and Burgund, 2010). Compared to its role in native language (L1) reading, the role of the left ventral occipito-temporal word form region in second language (L2) reading has yet to be fully investigated. Baker et al. (2007) found that visual words in Hebrew and English (two scripts utilizing alphabetic writing systems) activated a similar occipito-temporal region in bilingual readers of both languages, with a 79% overlap between voxels. Bai et al. (2011) investigated the spatial characteristics of the left ventral occipito-temporal word form region in L2 reading by testing KoreanChinese proficient early bilinguals. It is worth noting that Korean (L1) is an alphabetic writing system whereas Chinese (L2) is a logographic

Correspondence to: National Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, People's Republic of China. E-mail address: [email protected] (L. Liu).

http://dx.doi.org/10.1016/j.neuropsychologia.2017.06.007 Received 9 January 2017; Received in revised form 8 June 2017; Accepted 9 June 2017 Available online 10 June 2017 0028-3932/ © 2017 Published by Elsevier Ltd.

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experience did not recruit this region. This effect became more pronounced with higher levels of Chinese (L2) proficiency, signifying the modulatory role of L2 proficiency on the right homologous visual word form region. These findings indicate that particular attention should be paid to the modulatory role of L2 proficiency on the brain mechanisms supporting L2 reading. Similar to the asymmetry hypothesis (Cao et al., 2013; Nelson et al., 2009; Perfetti et al., 2007) mentioned above, the modulatory role of L2 proficiency also seems to show an asymmetric pattern: better L2 proficiency in Chinese-English bilinguals is associated with greater involvement of the L1 language network to support English reading acquisition (greater assimilation), whereas better L2 proficiency in English-Chinese bilinguals is associated with greater involvement of the L2 language network to accommodate the demands of Chinese learning (greater accommodation). However, the aforementioned studies on Chinese-English and English-Chinese bilingualism primarily focus on the response intensity of brain activation in different subject groups, and lack detailed spatial information concerning the occipito-temporal word form region. Such spatial information is important, as it is closely related to the characteristics of visual stimuli (Hasson et al., 2002; Vinckier et al., 2007), as well as other factors such as age (Burman et al., 2013; Olulade et al., 2013) and gender (Burman et al., 2013). Previous studies have shown that the complexity of visual stimuli and reading proficiency modulate the spatial organization of the occipito-temporal cortex in a systematic way along the posterior-to-anterior axis. For example, Vinckier et al. (2007) used fMRI to examine neural mechanisms in adult readers who were exposed to increasingly complex stimuli from individual letters to bigrams and morphemes. They found a posterior-to-anterior progression of the peak response coordinates in the left fusiform gyrus as the visual stimuli increased in complexity, implicating a topographical organization of the visual word-form system. Following this work, Olulade et al. (2013) also discovered that activation in the left visual word form system follows a posterior-to-anterior gradient over the course of development. Specifically, adults recruited more anterior subregions than children did, implying that age-related reading skills may be related to the engagement of more anterior regions in the ventral occipito-temporal area during word recognition. Based on the studies mentioned above, we hypothesize that Chinese compared to English visual word recognition should recruit more anterior portions of the occipito-temporal cortex, as Chinese visual word recognition requires mapping from whole morphemes to syllables (Xue et al., 2005). The occipito-temporal cortex has also been reported to show a topographical organization along the lateral-to-medial axis. For example, the lateral portion of this region has been reported to show preference for high-resolution foveal shapes, while the medial portion shows preference for low-resolution peripheral shapes (Hasson et al., 2002). Furthermore, Olulade et al. (2013) observed age-related changes along the lateral-to-medial axis of the visual word form system: namely, adults employed a more lateral portion of the mid-fusiform region, whereas children, as novice readers, recruited more medial areas during implicit word processing tasks. Based on the this evidence, we hypothesize that Chinese compared to English visual word recognition should recruit more lateral portions of the occipito-temporal region, as Chinese characters are visuo-spatially more densely packed than English words. In summary, vital importance should be attached to the spatial characteristics of the occipito-temporal word form area when investigating the precise mechanisms governing how this region supports the recognition of visual words in L2 processing, especially in cases where an individual's L1 and L2 adopt different writing systems. In addition, it is also worthwhile investigating how the location of this region changes spatially during L2 processing as a consequence of increased L2 proficiency. Answering these questions will enable us to better understand the factors governing the organization of the visual word form area in L2. We expect that both the spatial localization of the occipito-temporal region for L2 visual word processing and the

writing system. This study revealed that reading Chinese characters engaged essentially the same region of the occipito-temporal cortex as Korean script, suggesting that different writing systems in bilinguals employ similar neuronal communities to process visual word forms. However, the subjects in this study had acquired both Korean (L1) and Chinese (L2) prior to 5 years of age, technically making them dual native-language speakers. Furthermore, despite Korean characters being constructed from phonetic components, their visual appearance is nevertheless similar to Chinese characters, with both types of characters comprising two-dimensional squares containing various strokes. These visual similarities may be another reason for the similar spatial engagement of the ventral occipito-temporal cortex in processing Chinese and Korean scripts in this study. Chinese-English and English-Chinese bilinguals can provide a systematic perspective to investigate the role of the ventral occipito-temporal cortex in L2 word form processing, especially under the circumstances when L1 and L2 belong to different writing systems. As an alphabetic language, English is strikingly different from Chinese both orthographically and visually. Specifically, the visual form of an English word is set in an established order, with letters arranged from left to right, and words are pronounced following “grapheme-phoneme” conversion. By contrast, each square Chinese character serves as a selfcontained basic logographic unit, and is pronounced following a larger grain-size character-syllable conversion. Testing Chinese-English and English-Chinese bilinguals using lexical decision tasks in both L1 and L2, Sun et al. (2015) showed that both Chinese and English native speakers recruited more brain regions in the Chinese reading network (specifically, the left superior parietal lobule and right occipito-temporal regions) when reading L2 compared to L1. This finding supported the asymmetry hypothesis proposed by Perfetti and colleagues (Cao et al., 2013; Nelson et al., 2009; Perfetti et al., 2007): Chinese native speakers tend to use native language networks to support their English reading acquisition (assimilation), whereas English native speakers tend to develop new neural networks to accommodate the demands of Chinese learning (accommodation). Kim et al. (2015) postulated that when an L2 is more orthographically transparent than an L1, assimilation is expected because the L1 language network should be sufficient to process an orthographically more transparent L2; in contrast, when an L2 is more orthographically opaque than an L1, accommodation is expected because the L1 language network is insufficient and therefore a new language network needs to be developed to meet the requirements of L2 processing which is orthographically more opaque. In this way, the brain mechanisms supporting L2 reading are modulated by the language difference between L1 and L2 in terms of orthographic depth. Besides orthographic depth, the brain mechanisms supporting L2 learning are further modulated by L2 proficiency. As shown by Cao et al. (2013), better L2 proficiency in late Chinese-English bilinguals is associated with greater involvement of the brain regions in the Chinese reading network (specifically, the right precuneus, the left middle frontal gyrus, and the right inferior parietal lobule). These regions have been suggested to be involved in spatial perception and visual-motor integration in Chinese character processing (Andersen and Buneo, 2002; Caspers et al., 2011; Fernandez-Ruiz et al., 2007). Testing late English-Chinese bilinguals, Sun et al. (2015) observed that higher L2 reading proficiency in English native speakers was also correlated with greater recruitment of the brain regions in the Chinese reading network (specifically, the right inferior frontal gyrus and the left inferior parietal lobule). These two regions have been associated with Chinese lexical tone processing and visual-spatial analysis respectively (Sun et al., 2015). Mei et al. (2015) additionally discovered that Chinese learning experiences shaped fusiform laterality in English native speakers. Specifically, English speakers with Chinese learning experience recruited the right posterior fusiform cortex - a region uniquely involved in Chinese character form processing - when processing English words and pseudo-words, whereas individuals with no Chinese learning 21

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tasks is herein abbreviated as CC, and English tasks as CE. Likewise, data from English-Chinese bilinguals are similarly abbreviated as EE and EC. Our study was a re-analysis of Sun et al. (2015) to some extent, as our study drew on some of the data presented in Sun et al.’s study. However, the two studies looked at different aspects of the data. Briefly, Sun et al. (2015) aimed to discern the role of general perceptual features versus fundamental design principles of the orthography in modulating the brain mechanisms for L2 reading by analyzing brain response intensity at the whole brain level. In contrast, the current study focuses on the different spatial organization in the occipitotemporal word form area for L1 versus L2 processing by analyzing peak coordinates at a local brain region level. There were 108 stimuli for the lexical decision tasks in each script; of these, half were real stimuli (Chinese characters or English words), and half were pseudo stimuli (pseudo-characters or pseudo-words). Though lacking pronunciation or meaning, Chinese pseudo-characters were made up of three radicals arranged in a left-middle-right manner, similar to real Chinese characters, whereas English pseudo-words were similarly made by combining three syllables with logical orthography and phonology but lacking meaning. The 108 stimuli in each task were divided into three spacing levels. The first level (normally spaced), comprised visually normal English words or Chinese characters, while in the second and the third levels, stimuli were degraded by inserting 0.75 (4.5 mm) and 1.5 (9 mm) blank spaces between the three radicals in the Chinese characters or the three syllables in the English words. In this paper, we only analyzed data collected from the first level (normally spaced) stimuli, and ignored data collected from stimuli in the other spacing levels. The effects of spacing on second language processing has been discussed in another paper (Sun et al., 2015). Chinese characters were chosen from the Graded Vocabulary for HSK (Hanyu Shuiping Kaoshi), which is a national standardized test used to assess non-native speakers' Chinese proficiency. English words were selected from the English Vocabulary List for College Entrance Examinations (Beijing, 2008). Additionally, two professional language teachers checked the stimuli to ensure that they would be familiar to all participants. We statistically matched the stimuli in terms of familiarity and imageability of the words. Familiarity of the words was obtained by asking participants to rate the extent to which they are familiar with the word. Imageability of the words was obtained by asking participants to rate the ease with which a word rapidly evokes a strong mental image (Bird et al., 2001; Paivio, 1985). Thirty Chinese native speakers were recruited to assess the familiarity and imageability of the Chinese characters. Similarly，30 English native speakers were recruited to assess the familiarity and imageability of the English words. No significant differences were detected between languages in terms of familiarity (t(58) = −1.61, p = 0.113) and imageablity (t(58) = 0.536, p = 0.594).

modulatory role of L2 proficiency on this region will show an asymmetric pattern in Chinese-English and English-Chinese bilinguals. Specifically, the spatial localization of this region for visual word recognition is expected to be more posterior and medial in L2 compared to L1 in Chinese-English bilinguals, whereas English-Chinese bilinguals are expected to show more anterior and lateral in L2 compared to L1. In addition, better L2 proficiency in Chinese-English bilinguals is expected to be associated with greater assimilation to the L1 language network (i.e., a more anterior and lateral occupation of the occipito-temporal region), whereas better L2 proficiency in English-Chinese bilinguals is expected to be associated with greater accommodation to the L2 language network (i.e., also a more anterior and lateral occupation of the occipito-temporal region). 2. Methods 2.1. Participants Two groups of participants from Beijing Normal University were recruited in this study. The first group comprised 16 Chinese-English late bilingual subjects (mean age = 20.18, range: 18–23 years old; 6 males) who had been studying English since approximately 12 years old. The second group comprised 14 late English-Chinese bilinguals (mean age = 21.57, range: 19–25 years old; 11 males) who had begun learning Chinese at age 18 and had continued studying for 1–7 years. Chinese native speakers were marginally younger than English native speakers (t(28) = −2.02, p = 0.053); and the two groups additionally demonstrated a significant difference in terms of gender (Fischer's Exact Test: p = 0.033). Each participant's proficiency in his or her first (L1) and second languages (L2) was assessed using the Language History Questionnaire (Li et al., 2006). In this questionnaire, participants were asked to rate their L1 and L2 language proficiency (speaking, reading, writing and speech comprehension) on a scale from 1 (“illiterate”) to 10 (“fluent”). Based on the self-rating on the questionnaire, Chinese and English native speakers demonstrated significant differences in their judged L1 proficiency (Reading: t(28) = −3.98, p < 0.001; Writing: t(28) = −4.65, p < 0.001; Speaking: t(28) = −3.51, p = 0.002; Comprehension: t(28) = −3.16, p = 0.004). English native speakers rated their L1 proficiency slightly higher in all subtests compared to that of Chinese native speakers (English Mean = 9.7, Chinese Mean = 8.3). However, this is unlikely to reflect true L1 proficiency differences between the two groups as the both Chinese and English participants were all well-educated university students. Instead, this may reflect a culture difference as Chinese people tend to be modest in self-rating (Kim et al., 2010). In terms of L2 proficiency, the two groups of participants showed significant differences in L2 reading (t(28)=3.34, p=0.002) and L2 writing (t(28)=2.80, p = 0.010), but no significant differences were found in terms of L2 speaking (t(28)=0.03, p = 0.98) and L2 speech comprehension (t(28)=0.73, p = 0.47). In general, they were matched in terms of total scores in L2 proficiency (t(28) = −1.76, p = 0.09). Though the two groups were different in age, gender and some aspects of L2 proficiency, we mainly focused on the relative spatial organization of L1 versus L2 in the same group of subjects. The research protocol was approved by the institutional review board (IRB) at Beijing Normal University.

2.3. MRI data acquisition Data acquisition consisted of two runs, one for Chinese tasks, and one for English tasks. The presentation order of the two runs was counterbalanced across participants. Each run consisted of both baseline and lexical trials. Lexical trials consisted of the Chinese (or English) stimuli described above. During baseline trials, participants were asked to passively view a crosshair displayed in the center of the screen for a period varying from 2 s to 12 s. Lexical stimuli and fixations (baseline trials) were presented randomly in an event-related design. The ordering of the stimulus/fixation display was optimized using OptSeq (http://www.surfer.nmr.mgh.harvard.edu/optseq). During experiments, each stimulus image was displayed for 1700 ms, followed by a 300 ms blank interval in each trial. Images were acquired using a 3.0 T Siemens Magnetom Trio Tim magnetic resonance scanner at the Imaging Center for Brain Research of Beijing Normal University. A T2*-weighted gradient-echo echo-plannar imaging (EPI) sequence was used for funtional magnetic resonance

2.2. Task and stimuli Both groups of participants performed lexical decision tasks in their native and second languages. In the Chinese and English lexical decision tasks, participants were requested to judge whether each presented stimulus was a genuine Chinese character or English word, and were required to make decisions as quickly and accurately as possible. Button press responses were performed using the right/left index finger. Data collected from Chinese-English bilinguals performing Chinese lexical 22

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imaging (fMRI) scans, with the following acquisition parameters: TR/ TE/Theta = 2000 ms/30 ms/90°, FOV = 200 * 200 mm, slice thickness = 4 mm, and acquisition matrix = 64 * 64. Thirty-three axial slices were acquired to provide whole brain coverage. Anatomical MRI was acquired using a T1-weighted, three-dimentional, gradient-echo pulsesequence (MPRAGE), with TR/TE/Theta = 2530 ms/ 3.39 ms/ 7°, FOV = 256 * 192 mm, slice thickness = 1.33 mm, and acquisition matrix = 256 * 192. One hundred and twenty-eight coronal slices were acquired to provide a high-resolution structural image of the whole brain.

Table 1 Characteristics of the participants.

2.4. Image analysis Statistical parametric mapping (SPM8 from the Wellcome Department of Cognitive Neurology, London) was employed for preprocessing and statistical analysis. The initial six images were discarded from analysis to eliminate any non-equilibrium effects of magnetization. Funtional images were slice-time corrected to compensate for differences in acquisition time and realigned to the mean image in the scanning session to remove movement artifacts. Preprocessing further included spatial normalization to the EPI template based on the Montreal Neurologic Institute (MNI) stereotactic space (http://www. bic.mni.mcgill.ca). With a resample voxel size of 3 mm * 3 mm * 3 mm, the normalized images were smoothed using a Gaussian Kernel of 5 mm full-width at half maximum (FWHM). General linear model (GLM) analyses were conducted for each voxel at the individual subject level using the following method: three conditions (“real lexical stimuli”, “pseudo lexical stimuli” and “fixation”) were modeled using a canonical hemodynamic response function (HRF) for each task. For each subject, three contrasts of interest were computed separately for Chinese and English tasks: "real lexical stimuli" minus "fixation", “pseudo lexical stimuli” minus “fixation”, “all lexical stimuli” minus “fixation”. Parameter estimates from contrasts in individual subject models were entered into random-effects analysis. Onesample t-tests were used to test whether each comparison was significant in each group and for each task (CC, EE, CE and EC) respectively. We were particularly interested in the brain region involved in visual word form processing. Based on the reported location of the occipito-temporal visual word form region in previous studies (Cohen and Dehaene, 2004; Cohen, Lehericy et al., 2002a; Dehaene and Cohen, 2011) and the bilateral involvement of this region particularly in Chinese word processing (Bolger et al., 2005; Chao et al., 2008), we defined the occipito-temporal visual word form region as the most activated area within a bilateral fusiform gyrus mask. This mask was constructed based on an AAL (Automated Anatomical Labeling) template using a program named ‘REST’ (http://resting-fmri.sourceforge. net). Under a threshold of p < 0.001 uncorrected with a cluster size of at least 15 voxels (Variation of this threshold had no substantive effect on the results), the point with the highest statistical value (t value) in the contrast between lexical stimuli and fixation was defined as the peak response point. The coordinates of peak points for CC, CE, EE, and EC in bilateral fusiform gyri were all extracted for further analyses. We first conducted comparison analyses on the coordinates of the peak points between CC & CE, EE & EC to determine whether there were any differences in the spatial localization of the occipito-temporal visual word form area in native versus second language processing. Subsequently, we conducted comparison analyses on the coordinates of the peak points between CC & EE to determine whether there were any language differences in the spatial localization of the occipito-temporal visual word form area for native speakers. Finally, we conducted brainbehavior correlational analyses to examine how L2 proficiency (reading, writing, speaking) for CE and EC speakers modulates the spatial localization pattern of peak points in the occipito-temporal area during visual word processing. We did not correlate L2 speech comprehension proficiency with the neuroimaging data because we think speech comprehension is rather a complicated high-level language skill

Native Chinese Speakers (N = 16)

Native English Speakers (N = 14)

Age Gender

20.2(1.4) 6 Males

21.6(2.3) 11 Males

L1 Proficiency Reading Writing Speaking Comprehension

8.4(1.0) 7.8(1.2) 8.8(1.1) 8.4(0.9)

9.6(0.6) 9.6(0.8) 9.9(0.4) 9.8(0.4)

L2 Proficiency Reading Writing Speaking Comprehension

6.1(1.0) 5.9(1.6) 5.4(1.5) 5.8(1.5)

4.6(1.6) 4.4(1.5) 5.4(1.9) 5.4(1.9)

than lexical processing skill reflected in the occipito-temporal area. All of the above analyses were performed only on data from real lexical stimuli (Table 1).

3. Results 3.1. Behavioral results Table 2 presents reaction time and accuracy for the lexical decision tasks. We conducted a two-group (native Chinese speakers, native English speakers) by two language order (L1, L2) repeated measures ANOVA with reaction time and accuracy as the dependent variables respectively. An analysis of reaction times only revealed a significant main effect of language order (F (1,13) = 107.098, p < 0.001), yet no main effect of group or group by language order interaction effect. Similarly, an analysis of accuracy only revealed a significant main effect of language order (F(1,13) = 15.889, p = 0.002), without a main effect of group or a group by language order interaction effect. Paired-sample t-tests of the reaction time and accuracy in separate groups of participants revealed that both groups took a statistically significantly longer time to react to second language stimuli compared to those in their native language (Native English speakers: t(13) = 7.070, p < 0.001; Native Chinese speakers: t(15) = 8.009, p < 0.001). An analysis of response accuracy showed that the native English speakers were significantly more accurate at processing their first language than their second language (t(13) = 4.291, p = 0.001) and that native Chinese speakers showed a similar pattern, however the effect was only marginally significant (t(15) = 2.072, p = 0.056).

3.2. Brain results We examined spatial patterns of peak response points in bilateral fusiform gyri for visual word form processing in Chinese-English bilinguals and English-Chinese bilinguals when they performed native and second language lexical decision tasks respectively.

Table 2 Reaction time (RT) and accuracy (ACC) in the Chinese and English lexical decision tasks for native Chinese speakers and native English speakers respectively.

Chinese English

23

Native Chinese speakers

Native English speakers

RT (SD)

ACC (SD)

RT (SD)

ACC (SD)

709 (82) 929 (110)

98.2 (3.4) 91.1 (6.7)

919 (117) 750 (109)

82.4 (14.0) 96.1 (4.9)

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Fig. 1. Comparisons of the X coordinates between CC & CE (A) and EE & EC (B). CC: Chinese native speakers performing Chinese lexical decision tasks; CE: Chinese native speakers performing English lexical decision tasks; EE: English native speakers performing English lexical decision tasks; EC: English native speakers performing Chinese lexical decision tasks. Data points in the brain represent the peak points extracted from bilateral fusiform masks in CC and EE, with red representing CC and the blue representing EE. LH = Left Hemisphere; RH = Right Hemisphere.

3.2.1. Comparisons of the X coordinates of peak points in bilateral fusiform gyri between L1 and L2 processing We compared the X coordinates of peak points extracted from bilateral fusiform masks in L1 versus L2 word form processing. As demonstrated in Fig. 1A, the CC group occupied a more lateral distribution (left fusiform: M = −38.9, SD = 5.4; right fusiform: M = 43.1, SD = 5.7) than the CE group (left fusiform: M = −30.2, SD = 7.5; right fusiform: M = 31.4, SD = 8.7). These differences were significant in both hemispheres (left fusiform: t(15) = −3.02, p = 0.009; right fusiform: t(15) = 4.02, p = 0.001). As can be seen from Fig. 1B, the EC group showed a significantly more lateral distribution than the EE group in the right fusiform (EC: M = 40.7, SD = 8.2; EE: M = 32.1, SD = 9.5; t(13) = −2.65, p = 0.02), but not in the left fusiform (EC: M = −37.2, SD = 5.9; EE: M = −34.2, SD = 7.5; t(13) = 1.37, p = 0.20). To further investigate the effect of language during L1 processing in terms of the localization of the occipito-temporal word form region, we also compared X coordinates of the peak points in bilateral fusiform between the CC and EE groups. The CC group's X coordinates also showed a more lateral pattern (left fusiform: M = −38.9, SD = 5.4; right fusiform: M = 43.1, SD=5.7) than the EE group (left fusiform: M = −34.2, SD = 7.5; right fusiform: M = 32.1, SD = 9.5) - the difference was significant in the right fusiform (F(1, 28) = 12.01, p = 0.002), but only marginally significant in the left fusiform (F(1, 28) = 3.00, p = 0.095), with age and gender controlled. Taken together, visual word form processing for L1 and L2 appear to engage different parts of the occipito-temporal word form region along the lateral-to-medial axis in bilateral fusiform gyri, especially in the right fusiform. In addition, Chinese word form processing, regardless of whether it was processed as an L1 or an L2, demonstrated a more lateral pattern than English word form processing in bilateral fusiform gyri.

Fig. 2. Comparisons of the Y coordinates of peak response points between CC & CE (A), and EE & EC (B) in the right fusiform. No significant results were found for the left fusiform.

we found significant differences in the Y coordinates of peak response points (1) between CC & CE (t(15) = 5.16, p < 0.001), with CE showing a more posterior localization (M = −77.9, SD = 8.5) than CC (M = −62.6, SD = 8.5) (see Fig. 2A), (2) between EE & EC (t(13) = −2.49, p = 0.027), with EC showing a more anterior distribution (M = −61.2, SD = 12.7) than EE (M = −72.4, SD = 11.5) (see Fig. 2B). To further investigate the effect of language during L1 processing, we also compared Y coordinates of the peak points in bilateral fusiform between the CC and EE groups and found that CC showed a more anterior distribution than EE (F(1,28) = 4.89, p = 0.036) only in the right fusiform, with age and gender controlled.

3.2.2. Comparisons of the Y coordinates of peak points in bilateral fusiform gyri between L1 and L2 processing As well as comparing X coordinates, we also compared the Y coordinates of peak points in bilateral fusiform gyri for L1 versus L2 during visual word form processing (see Fig. 2). No significant differences were found in the left fusiform gyrus. In the right fusiform gyrus, 24

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Fig. 3. Brain-behavior analyses demonstrated a significantly negative correlation between L2 proficiency and the X coordinates of peak response points in the CE group in the left fusiform (A), and a positive correlation between L2 proficiency and the X coordinates of peak response points in the EC group in the right fusiform (B). These results (A and B) suggest that a more lateral occupation in bilateral fusiform is related to better L2 proficiency. Brain-behavior analyses also showed a positive correlation between the Y coordinates of peak response points in the EC group and L2 proficiency in the left fusiform (C), suggesting that higher L2 proficiency in English learners of Chinese is correlated with a more anterior occupation of the left fusiform gyrus.

a more anterior peak localization in the occipito-temporal word form region. These above findings, including the spatial organization patterns for L2 visual word processing in bilateral fusiform gyri and the influence of L2 proficiency on these patterns, are summarized in Fig. 4.

These results suggest that visual word form processing for L1 and L2 also engaged different parts of the occipito-temporal word form region along the anterior-to-posterior axis in the right fusiform gyrus. In addition, Chinese word form processing, regardless of whether it was processed as an L1 or an L2, demonstrated a more anterior localization than English word form processing in the right fusiform gyrus.

4. Discussion

3.2.3. Correlations between the X coordinates of bilateral fusiform peak points and L2 proficiency Partial Pearson's correlation analyses were conducted to examine whether the medial or lateral distribution of peak points in bilateral fusiform gyri during L2 word processing was correlated with L2 proficiency separately for CE or EC. Correlations were performed between L2 proficiency and the X coordinates extracted from peak response points in the left and right fusiform gyri in both CE and EC, with the subjects’ age and gender statistically controlled; these partial correlations are presented in Fig. 3. In the left fusiform, the X coordinates of peak response points in CE demonstrated significant negative correlations with L2 proficiency in speaking (Rx-speaking = −0.677, p = 0.008) (Fig. 3A), which suggests that higher L2 proficiency is associated with a more lateral occupation of the left fusiform for visual word processing. In the right fusiform, significantly positive correlations were found between the X coordinates of peak points for EC and L2 proficiency in speaking (Rx-speaking= 0.578, p = 0.049), reading (Rx-reading = 0.593, p = 0.042), and writing (Rx-writing = 0.785, p = 0.002) (Fig. 3B), suggesting higher L2 proficiency is also associated with a more lateral occupation of the right fusiform for visual word processing, a similar pattern as observed for CE in the left fusiform. Taken together, these observations suggest that higher L2 proficiency is associated with a more lateral involvement in the fusiform area for both Chinese-English bilinguals and English-Chinese bilinguals.

Despite the ventral occipito-temporal region showing consistent activation for visual word form processing in different languages across numerous studies (Bai et al., 2011; Baker et al., 2007; Bolger et al., 2005; Chao et al., 2008), the mechanism by which second language word forms are processed in this region is still a subject of significant debate. To examine this issue, we recruited Chinese-English and English-Chinese bilinguals to perform lexical decision tasks in both their first and second languages, thus resulting in four experimental conditions: CC (Chinese native speakers performing Chinese lexical decision tasks), CE (Chinese native speakers performing English lexical decision tasks), EE (English native speakers performing English lexical decision tasks) and EC (English native speakers performing Chinese lexical decision tasks). Using data from these four conditions, we investigated whether the ventral occipito-temporal region was engaged in a spatially consistent way when processing visual words in a subject's L2 versus his or her L1, and whether L2 proficiency modulated spatial localization of the visual word form region in Chinese-English and English-Chinese bilinguals. Our results can be summarized into two main findings. First, visual word form processing for L2 versus L1 engaged different areas of the ventral occipito-temporal cortex along the X (lateral-to-medial) axis. Specifically, the spatial location of this region was more medial for visual word form processing in L2 than L1 in Chinese-English bilinguals, whereas English-Chinese bilinguals demonstrated more lateral activation for visual word form processing in L2 than L1. Additionally, for both groups, a more lateral location of this region in L2 visual word form processing was related to better L2 proficiency. Second, visual word form processing for L2 versus L1 engaged different areas of the ventral occipito-temporal cortex along the Y (anterior-to-posterior) axis. Specifically, the spatial location of this region for visual word form processing in the right fusiform was more posterior for L2 than L1 in

3.2.4. Correlations between the Y coordinates of bilateral fusiform peak points and L2 proficiency We found significant brain-behavior correlations for EC alone. Specifically, L2 (Chinese) reading (Ry-reading = 0.697, p = 0.012) and speaking proficiency (Ry-speaking = 0.594, p = 0.042) were both positively correlated with Y coordinates in the left fusiform gyrus (see Fig. 3C), suggesting that better L2 proficiency for EC is correlated with 25

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Fig. 4. A schematic drawing of the spatial organization patterns for L2 visual word processing in the bilateral fusiform gyri. Dots represent the locations of the averaged X and Y coordinates of peak response points in each experimental condition (CC, CE, EE and EC). The arrows represent the directions of the spatial localization change of the peak points in bilateral fusiform with increased L2 proficiency.

fusiform gyrus has been suggested to be more heavily involved in Chinese word processing (either as L1 or L2) compared to alphabetic languages (Bolger et al., 2005; Chao et al., 2008; Tan et al., 2005; Zhao et al., 2012), due to its importance in visual analysis (Chen et al., 2007; Tan et al., 2001), and its storage of holistic character information (Dien, 2009). Our brain-behavior correlation finding along the posterior-toanterior axis also shows that higher L2 (Chinese) proficiency for English-Chinese bilinguals is associated with more anterior occupation of the left fusiform, The anterior area of the occipito-temporal cortex is theorized to be more involved in whole word recognition whereas the posterior area is theorized to be more involved in letter identification in alphabetic language systems (Tagamets et al., 2000). Many studies report that words are recognized in the fusiform by hierarchically organized system, with increasingly complex and abstract symbol strings being processed more anteriorly (Dehaene et al., 2005; Olulade et al., 2013; Vinckier et al., 2007). Furthermore, a number of studies have suggested the anterior region of the fusiform is an amodal language area, representing abstract word representations and mediating between orthographic, phonological and semantic information (Cohen et al., 2004; Hillis et al., 2005; Jobard et al., 2003, 2007). Consistent with these studies, Purcell et al. (2014) identified an area within the anterior fusiform which they referred to as the Orthography-Semantics Interface Region (OSIR), which specifically supports the mapping of orthographic information onto semantic meaning in reading and spelling. Based on this research, we speculate that the further anterior occupation of the fusiform in Chinese (either as L1 or L2) compared to English word processing in our study could be due to two reasons. First, as Chinese characters are two-dimensional squares constructed from densely packed visual-spatial configurations, Chinese word reading requires more whole word rather than serial processing. Second, Chinese characters are logographic units of semantic meaning at the syllable level; hence, it is possible that Chinese processing utilizes the anterior fusiform to perform orthography-to-semantic mapping. Of note, our finding that L1 and L2 visual word processing engaged different areas of the fusiform gyrus along the medial-to-lateral and posterior-to-anterior axes, is inconsistent with Bai et al. (2011), which found that early proficient Chinese-Korean bilinguals engaged essentially the same visual word form area when processing L1 and L2, which was argued to support the idea that the selectivity of the visual word form area does not depend on language script. The disparity between this study and ours may be mainly due to script differences: Korean script is similar to Chinese in appearance, with both languages adopting a two-dimensional spatial layout, whereas Chinese script is strikingly different from English script with the latter adopting a one-dimensional left to right spatial layout. Another possible cause for this discrepancy

Chinese-English bilinguals, whereas English-Chinese bilinguals demonstrated more anterior activation for visual word form processing in L2 than L1. Additionally, for English-Chinese speakers, a higher L2 proficiency was associated with a more anterior occupation of the left fusiform in L2 visual word processing. The first finding of our study is that Chinese word processing occurred in more lateral regions of bilateral fusiform compared to English word processing, regardless of whether Chinese was processed as an L1 or an L2. This finding is consistent with the functional specialization of the occipito-temporal cortex along the lateral-to-medial axis: the lateral portion of this region has been reported to show a preference for highresolution foveal shapes while the medial portion shows a preference for low-resolution peripheral shapes (Hasson et al., 2002). The more lateral occupation of the bilateral fusiform in Chinese visual word form processing compared to English may be driven by the high demand of fine-grained visual processing due to the logographic nature of Chinese characters (Liu et al., 2012; Shu et al., 2003), with a higher information density higher than that of English letters (Cao et al., 2010; Shu et al., 2003). Our brain-behavior correlation finding between L2 proficiency and the spatial location of the visual word form region along the lateral-tomedial axis is generally consistent with previous studies suggesting that L2 proficiency modulates the brain mechanisms for L2 reading (Cao et al., 2013; Kim et al., 2015; Sun et al., 2015; Zhang et al., 2013). Specifically, we found that for all speakers, better L2 proficiency was correlated with a more lateral occupation of the occipito-temporal word form area. This brain-behavior correlation suggests that higher L2 proficiency in both Chinese-English and English-Chinese bilinguals was associated with greater involvement of Chinese-preferred regions within the bilateral lateral fusiform gyri. Our results are consistent with the findings of Cao et al. (2013) who reported that higher English (L2) proficiency in late Chinese-English bilinguals is associated with greater involvement of the brain regions comprising the Chinese reading network. Our results are also consistent with Sun et al. (2015) who reported that higher Chinese (L2) reading proficiency in late EnglishChinese bilinguals was also correlated with greater recruitment of the brain regions associated with the Chinese reading network. Our study extends these previous findings by showing that L2 proficiency can modulate the fine-grained spatial localization of the occipito-temporal region during visual word processing. Our second finding, that the spatial location of the region for visual word form processing in the right fusiform was more posterior for L2 than L1 in Chinese-English bilinguals, whereas English-Chinese bilinguals demonstrated more anterior activation for L2 than L1, was also in line with the role of the anterior part of the right fusiform. The right

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orthographic transparency of the L1-L2 relationship. Specifically, they theorized that under circumstances where an L2 is more orthographically transparent than an L1, both the L1 and the L2 will share a common native language network as the L1 language network should be sufficient to assimilate the more transparent L2 orthography. In contrast, in situations where an L1 is more orthographically transparent than an L2, a new language network is developed to accommodate the requirements of L2 processing. Our study is the first showing this asymmetric pattern at a finer level of spatial organization in the fusiform area.

may be the bilingual status of the subjects involved: Bai and colleagues studied subjects who had mastered both Chinese and Korean before five years of age, whereas the bilinguals in our study were all late second language learners. The aforementioned similarity in script and orthography between L1 and L2 may also be partly the reason that Baker et al. (2007) found that English and Hebrew visual word processing in bilinguals engaged a similar portion of the occipito-temporal region, as both Hebrew and English belong to alphabetic writing systems. Taken together, similarities and differences in the precise areas of the occipitotemporal cortex engaged by L1 and L2 visual word form processing appear to depend on several factors governing the L1-L2 relationship, including whether they belong to similar or different writing systems and at what age they are acquired. L2 proficiency in the EC group was significantly lower than that in the CE group. Considering cultural differences in the self-rating, the actual L2 proficiency of English speakers is probably even lower compared to that of Chinese speakers. Chinese people tend to be more modest and rate their proficiency lower than it actually is. The L2 proficiency difference between CE and EC, rather than the nature of the L2 language, may cause the L1 versus L2 differential spatial location in each group. However, this is not likely as it could not easily explain the opposite brain-behavioral patterns found in the CE and EC groups. Assuming the nature of L2 language does not play a role in the L1 versus L2 differential results in CE and EC, the two groups should demonstrate similar brain-behavioral correlation patterns between L2 spatial organization and L2 proficiency. However, the CE and EC groups demonstrated opposite patterns: higher L2 proficiency in EC was associated with more distant spatial location for L2 processing from their L1 network, whereas higher L2 proficiency in CE was associated with more similar spatial location for L2 processing to their L1 network. To sum up, proficiency is indeed correlated with the spatial organization of L2 processing, but it may not influence our finding in which the CE and EC groups demonstrated different patterns in L1 versus L2. Objective measures of language proficiency should be used in the future studies. Besides the spatial organization of peak points investigated in the current study, we think that the ventral occipito-temporal region (i.e, the VWFA) may also show plasticity along with L2 learning experience in other aspects, such as location, size and activity. For example, we found some clusters in the left fusiform area extending the typical borders of the VWFA to the Fusiform Face Area (FFA), especially in L2 processing conditions (i.e., CE and EC). This pattern is consistent with the competition for cortical space between the VWFA and the pre-existing neural coding of faces discussed in the literature (Dehaene, 2005; Dehaene and Cohen, 2007; Dehaene, 2010; Plaut and Behrmann, 2011). For example, Dehaene (2010) found that as literacy increases, cortical responses to faces decrease slightly in the left fusiform region, while they increase strongly in the right fusiform area (FFA). This pattern could be explained by neuronal recycling model, in which pre-existing neural systems for vision and language are partially "recycled" for the specific requirement posed by reading (Dehaene, 2005; Dehaene and Cohen, 2007). Therefore, the extended activation into FFA regions observed in CE and EC may indicate that L2 learning may compete with face processing in the fusiform area. Taken together, our results provide evidence of an asymmetric pattern in the spatial organization of the ventral occipito-temporal region during L2 visual word processing. Specifically, English learners of Chinese engaged more L2 preferred regions in the fusiform in L2 processing compared to L1 processing, and activation scaled with increased L2 proficiency. Contrastingly, Chinese learners of English utilized more L1 preferred regions in the fusiform in L2 processing compared to L1 processing, and activation scaled with increased L2 proficiency. This pattern supports the asymmetry hypothesis proposed by (Perfetti et al., 2006), who argued that Chinese-English bilinguals assimilate to regions specific to L1 during L2 processing, whereas English-Chinese bilinguals accommodate to regions specific to L2 during their L2 processing. Kim et al. (2015) explained this asymmetric pattern with reference to the

5. Conclusion Our results show that L1 versus L2 visual word processing recruit spatially different areas of the occipito-temporal cortex when L1 and L2 belong to different writing systems. Specifically, our results suggest that when the orthography of an L1 compared to an L2 requires more wholeword processing and is visually more information intensive as in Chinese, the spatial organization of the occipito-temporal cortex for visual word form processing is more lateral and anterior. In contrast, when the orthography of L1 compared to L2 requires more graphemebased processing and is visually less complex as in English, the spatial organization of the occipito-temporal cortex for visual word form processing is more medial and posterior. In addition, our results show that L2 proficiency modulates this spatial organization. Specifically, when an L1 is orthographically more opaque, better L2 proficiency is associated with accommodation to the L1-preferred localization of the occipito-temporal word form area. In contrast when an L1 is orthographically more transparent than an L2, assimilation to L2-preferred localization of the occipito-temporal word form area is associated with better L2 proficiency. The present study provides important evidence for asymmetric patterns of assimilation and accommodation in the spatial organization of the occipito-temporal cortex in L2 visual word processing. Acknowledgment This research was funded by the Natural Science Foundation of China (31571155), the 973 Program (2013CB837300), the Beijing Higher Education Young Elite Teacher Project (YETP0258), Beijing Municipal Science & Technology Commission (Z151100003915122), and the Fundamental Research Funds for the Central Universities. Special thanks to Mr. Mark Dingwall for his help in grammar correction. References Andersen, R.A., Buneo, C.A., 2002. intentional maps in posterior parietal cortex. Annu. Rev. Neurosci. 25 (1), 189–220. Bai, J., Shi, J., Jiang, Y., He, S., Weng, X., 2011. Chinese and Korean characters engage the same visual word form area in proficient early Chinese-Korean bilinguals. PLoS ONE 6 (7), e22765–e22768. Baker, C.I., Liu, J., Wald, L.L., Kwong, K.K., Benner, T., Kanwisher, N., 2007. Visual word processing and experiential origins of functional selectivity in human extrastriate cortex. Proc. Natl. Acad. Sci., 104(21), pp. 9087–9092. Bird, H., Franklin, S., Howard, D., 2001. Age of acquisition and imageability ratings for a large set of words, including verbs and function words. Behav. Res. Methods, Instrum. Comput. 33 (1), 73–79. Bolger, D.J., Perfetti, C.A., Schneider, W., 2005. Cross-cultural effect on the brain revisited: universal structures plus writing system variation. Human Brain Mapp. 25 (1), 92–104. Burman, D.D., Minas, T., Bolger, D.J., Booth, J.R., 2013. Age, sex, and verbal abilities affect location of linguistic connectivity in ventral visual pathway. Brain Lang. 124 (2), 184–193. Cao, F., Lee, R., Shu, H., Yang, Y., Xu, G., Li, K., Booth, J.R., 2010. Cultural constraints on brain development: evidence from a developmental study of visual word processing in Mandarin Chinese. Cereb. Cortex 20 (5), 1223–1233. Cao, F., Tao, R., Liu, L., Perfetti, C.A., Booth, J.R., 2013. High proficiency in a second language is characterized by greater involvement of the first language network: evidence from Chinese learners of english. J. Cogn. Neurosci. 25 (10), 1649–1663. Caspers, S., Eickhoff, S.B., Rick, T., Kapri, von, A., Kuhlen, T., Huang, R., et al., 2011. Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior

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