Dyslexic Characteristics of Chinese-Speaking Semantic Variant of Primary Progressive Aphasia
Publication: The Journal of Neuropsychiatry and Clinical Neurosciences
Abstract
Reading disorder is a recognized feature in primary progressive aphasia (PPA). Surface dyslexia, characterized by regularization errors, is typically seen in the English-speaking semantic variant of PPA (svPPA). However, dyslexic characteristics of other languages, particularly logographical languages such as Chinese, remain sparse in the literature. This study aims to characterize and describe the dyslexic pattern in this group of patients by comparing an English-speaking svPPA group with a Chinese-speaking svPPA group. The authors hypothesized that Chinese-speaking individuals with svPPA would likely commit fewer surface dyslexic errors. By accessing the database of Singapore’s National Neuroscience Institute and the National Alzheimer’s Coordinating Center of the United States, the authors identified three Chinese-speaking and 18 English-speaking patients with svPPA, respectively, for comparison. The results suggest that, instead of surface dyslexia, svPPA in Chinese-speaking individuals is characterized by a profound deep dyslexic error. Based on current evidence suggesting the role of the temporal pole as a semantic convergence center, the authors conclude that this region also mediates and converges lexical-semantic significance in logographical languages.
The semantic variant of primary progressive aphasia (svPPA) is a disorder that involves a breakdown in semantic knowledge, typically characterized by impaired single-word comprehension and confrontational naming. Neuroimaging tends to show predominant anterior temporal lobe atrophy or hypometabolism.1 During reading, English-speaking individuals with svPPA typically exhibit surface dyslexia and display regularization error of irregular words, such as “sew” being read as /su/.2 Presence of surface dyslexia is largely due to the dysfunction of the ventral reading pathway and an overreliance on the grapheme-to-phoneme conversion (GPC) or dorsal reading pathway.3
To date, little is known about the dyslexic characteristics in Chinese-speaking patients with svPPA. Chinese is a logographical language that carries distinctive linguistic characteristics when compared with alphabetic languages such as English. Individual characters in the Chinese writing system are formed by basic graphic units. Each character represents the smallest unit of meaning and is monosyllabic.4 Simple characters, made up of various spatial arrangements of strokes, can combine to form logographemes/radicals.5 Approximately 80%−90% of Chinese characters are ideophonetic compounds, formed by phonetic and semantic radicals, providing the pronunciation and the meaning of the character, respectively.4,6 Only a very small portion of simple characters are pictographic in nature. Some authors propose that Chinese characters consist of three levels of regularization with regard to the relationship between shape and pronunciation: regular, semiregular, and irregular. In regular characters, the character is pronounced as a whole in the same manner as its phonetic radical (e.g., “座”/zuo4/, with the phonetic “坐”/zuo4/). In semiregular characters, the phonetic radical provides partial information about pronunciation (e.g., “精”/jing1/ and its phonetic “青”/qing1/). In irregular characters, the pronunciation of the character is different from its phonetic radical (e.g., “埋”/mai2/, with the phonetic “里”/li3/).7–9 As such, the Chinese language is considered an opaque language.4,7,8 However, other researchers have provided evidence that phonological awareness is reported to be comparatively less important in Chinese compared with other opaque languages10–12; instead, reading proficiency is related to other cognitive abilities such as orthographic awareness, visual skills, and morphological awareness.10,11
In view of the absence of phonemes that are associated with letters, some scholars believe that Chinese has no GPC as per alphabetic language.13–16 Studies have attempted to classify children with developmental Chinese dyslexia according to a dual-route model but with inconsistent and controversial results,4,9,17 unlike studies investigating alphabetic languages such as English and French, in which classifications of dyslexia with phonological and surface patterns were consistent.18–23 In order to overcome the dual-route model controversy when classifying Chinese dyslexia, Yin and Weekes used a similar concept called “the triangle model of Chinese reading,” which includes a lexical-semantic pathway that allows phonological output to directly access orthographical representation.24 However, this model still poses limitations with regard to surface-like error finding when reading irregular Chinese words, probably because of the different fundamental linguistic characteristics of phonological processing between Chinese and English. The aforementioned highlights the limitation and controversies of heterogeneity findings of current Chinese reading models.
While previous cases report similar surface dyslexia patterns in Chinese-speaking patients with semantic dementia,25–27 we have also observed a different dyslexia pattern in our patients with svPPA that ranges from failing to recognize characters as a whole (rather than “regularizing” it) to deep dyslexia.28,29 In this study, we aim to further characterize dyslexia patterns in Chinese-speaking patients with svPPA and will compare them with the patterns in English-speaking patients with svPPA. We hypothesize that patients with svPPA will commit less surface dyslexia, due to the lack of a GPC route in the Chinese language.
Methods
Study Participants
We reviewed the dementia database of the National Neuroscience Institute (NNI) Singapore from the year 2014 to the year 2016. Patients who fulfilled Gorno-Tempini et al.’s criteria1 for svPPA, and who had Chinese language as their first language, were identified and included in the study.
We also accessed data from the National Alzheimer’s Coordinating Center (NACC) Uniform Data Set (UDS). The NACC collects data from National Institute on Aging (NIA)-funded Alzheimer’s Disease Centers (ADCs) in the United States. English-speaking patients with a clinical diagnosis of svPPA based on the UDS-Frontotemporal Lobar Degeneration (FTLD) module (Form B9F, item 13, code 1) were included in this study. Information collected during their baseline visits was reviewed, and details were analyzed.
Research using the NACC database was approved by the University of Washington Institutional Review Board, and the data collection process was conducted in accordance with NIA policies. The NACC database includes 34 past and present ADCs. Authors who access the data are required to sign and comply with the data use agreement. Written informed consent was obtained from all participants and informants at the individual ADCs, and NACC data were de-identified.30 The study involving NNI patients was also approved by the SingHealth Centralised Institutional Review Board. Three Chinese-speaking patients with svPPA from the NNI dementia database were identified and included. The final dataset from the NACC database analyzed for the present study used data from 17 ADCs and included 18 patients evaluated at the NIA-funded ADCs from 2005 to December 2016.
Case Summary
Case 1.
A 56-year-old right-handed Chinese Singaporean man presented with difficulty in comprehending sentences for a 1-year duration. He received Chinese-stream education up to secondary school. Neurobehavioral assessments showed fluent spontaneous speech and a Mini-Mental State Examination score of 19/30. An MRI scan of the brain showed left anterior temporal atrophy and a [18]flurodeoxyglucose positron emission tomography scan showed predominant left anterior temporal hypometabolism (Figure 1A).
FIGURE 1. Neuroimaging Examples of Case 1 and Case 2a
a The images show A) Case 1: MRI brain fluid-attenuated inversion recovery (FLAIR) and [18]flurodeoxyglucose positron emission tomography ([18]FDG-PET) showing a predominant left anterior temporal lobe atrophy and hypometabolism; and B) Case 2: MRI brain FLAIR showing a predominant left anterior temporal lobe atrophy.
Case 2.
A 65-year-old right-handed Chinese Singaporean woman presented with gradual worsening of expression over a 2-year period. She received Chinese-stream education up to secondary school. Family members noted that the patient frequently had difficulty in using the correct term and tended to replace it with others. Neurobehavioral examination showed fluent spontaneous speech with on-and-off semantic paraphasia. An MRI brain scan showed left anterior temporal lobe atrophy (Figure 1B).
Case 3.
A 53-year-old right-handed Chinese Singaporean woman who received Chinese-stream education up to secondary school presented with difficulty in comprehending and expressing words over a period between 1 and 2 years. Family members noted that the patient tended to frequently use the wrong names for vegetables and fruits during grocery shopping. Neurobehavioral examination showed fluent spontaneous speech with on-and-off semantic paraphasia. An MRI brain scan showed left anterior temporal lobe atrophy.
Reading and Semantic Tasks
Data collected from the Chinese-speaking patients included a 10-word reading task and a short-passage reading task from the Mandarin version of the Bilingual Aphasic Battery,31 a 10-item semantic picture-matching task derived from the Comprehensive Aphasic Battery (CAT),32 and the 15-item modified Boston Naming Test (BNT). Data collected from the English-speaking patients included in this study were a 30-item word reading test; a 16-item Semantic Associates Test from the FTLD module, Form C1F, items 3 and 6, respectively; and the 30-item BNT from the UDS module, Form C1, item 10.
Exclusion criteria included incomplete or inconsistent data of demographics and reading or semantic data details.
Statistical Analysis
Chinese- and English-speaking groups with svPPA were compared using the Wilcoxon rank sum test with continuity correction for continuous variables, and with chi-square or Fisher’s exact test for categorical variables. p values of less than 0.05 were considered statistically significant. Multivariate analysis was not performed in this study because of the small sample size. All statistical analysis was performed in IBM SPSS, version 23.
Results
Both groups were comparable in terms of basic demographic, except in years of education. Table 1 summarizes the details of the results. Table 2 summarizes the test performances of both language groups. Figure 2 describes the statistical comparison of task performance ratios between the two groups. Results showed comparable task performance of the BNT, word reading task, and semantic picture association task. However, semantic errors during reading tasks, indicating deep dyslexia, were noted to be present only in the Chinese-speaking group (p<0.01). Furthermore, the regularization errors during reading tasks were profoundly biased toward the English-speaking group (p=0.02). Both these findings were statistically significant. Table 3 summarizes the semantic and regularization errors being committed by all 3 patients.
| Characteristic | Chinese-Speaking svPPA (N=3) | English-Speaking svPPA (N=18) | p |
|---|---|---|---|
| Age, mean (SD) | 58.7 (6.6) | 60.6 (12.4) | 0.81 |
| Gender, male, N (%) | 1 (33.3) | 5 (27.8) | 0.84 |
| Education years, mean (SD) | 10.0 (0.0) | 16.9 (2.8) | <0.01 |
| Global CDR, mean (SD) | 0.50 (0.0) | 0.69 (0.42) | 0.45 |
a
Wilcoxon rank sum test with continuity correction for continuous variables and chi-square test for categorical variables. Abbreviations: CDR: Clinical Dementia Rating scale; svPPA: semantic variant of primary progressive aphasia. The p values <0.05 (bold) were considered statistically significant.
| Measure | Chinese-Speaking svPPA (N=3) | English-Speaking svPPA (N=18) |
|---|---|---|
| BNT, mean (SD) | 6.0 (2.6) | 7.0 (6.4) |
| Word reading, mean (SD) | 4.7 (2.9) | 23.2 (3.9) |
| Paragraph reading error, mean (SD) | 3.7 (1.5) | — |
| Total reading error, mean (SD) | 8.3 (1.5) | 6.8 (3.9) |
| Total semantic error, mean (SD) | 5.0 (1.7) | 0.0 (0) |
| Total regularization error, mean (SD) | 1.0 (1.0) | 4.2 (2.5) |
| Semantic Associates Test, mean (SD) | 7.5 (0.7) | 13.8 (1.9) |
a
Abbreviations: BNT: Boston Naming Test; svPPA: semantic variant of primary progressive aphasia.
FIGURE 2. Results Summarizing Performance Ratio of Both Language Groupsa
a Abbreviations: BNT=Boston Naming Test; svPPA=semantic variant primary progressive aphasia. The p values were determined using the Wilcoxon rank sum test, with continuity correction and p values <0.05 considered statistically significant.
| Print Characters | Semantic Error | Regularization Error |
|---|---|---|
| 貓/mao1/cat | 鴨子/ya1zi3/duck, 豬/zhu1/pig | — |
| 狼/lang2/wolf | 熊/xiong2/bear | 良/liang2/good |
| 敲/qiao1/knock | 刮/gua1/scratch | 高/gao1/high |
| 針/zhen1/needle | 夾子/jia2zi3/clip | — |
| 刷/shua1/brush | 掃/sao3/sweep | — |
| 豬/zhu1/pig | 狗/gou3/dog, 鹿/lu4/deer | — |
| 鳥/niao3/bird | 馬/ma3/horse | — |
| 抓/zhua1/catch | 掛/gua4/hook | — |
| 鴿/ge1/pigeon | 雞/ji1/chicken | — |
| 朋友/peng2you3/friend | 兄弟/xiong1di4/brother | — |
Discussion
Consistent with our previous case reports,28,29 the most important and interesting finding of the present study is the significant semantic-related dyslexic error observed only in the Chinese-speaking patients with svPPA. The statistically comparable Clinical Dementia Rating (CDR) and semantic picture task performance rate suggested that the two groups of patients probably shared a similar stage in clinical severity of the disease. Unfortunately, because of the small sample size, multivariate logistic regression models could not be generated; hence, the results were not able to be adjusted for years of education. However, the complete absence of any semantic error in the English-speaking group but relatively high incidence rate in the Chinese-speaking group suggests that the observation is likely valid.
Current literature recognizes a dual-route psycholinguistic model of reading consisting of a lexical route and a sublexical route.33–36 Several functional studies also support the existence of such routes, which include the ventral-lexical sound-to-meaning pathway extending from the occipital-temporal-frontal region and the dorsal-sublexical sound-to-print pathway extending from the occipital-parietal-frontal region. Ventral pathway impairment typically presents as failure to read irregular words, as phonological output of these words is directly imprinted into the orthographical representation in this pathway. Meanwhile, dorsal pathway impairment presents as failure to read morphologically complex words as a result of impairment of the print-to-sound or GPC mechanism.37–42
Lesions in the ventral route result in an overreliance on the dorsal route and produce surface dyslexia, or regularization error. However, patients retain the capability to sound out pseudowords. On the other hand, dorsal route impairment produces phonological dyslexia, characterized by the capability to read concrete words but not pseudowords or words with low semantic value such as function words (e.g., “it,” “the”), signifying an overreliance on the semantic system. A recent behavior-lesion correlation study by Ripamonti and colleagues demonstrated consistent findings that surface dyslexia is predominantly associated with left temporal lesions and phonological dyslexia at left insula and the left inferior frontal gyrus (pars opercularis).43
Semantic-related dyslexic error, or deep dyslexia, which in literature has been mainly described in alphabetic languages such as English, is perhaps the most extensively studied type of central dyslexia.44 The term deep dyslexia was designated by Marshall and Newcombe when they described a patient (G.R.) with a tendency to produce errors that appeared to be semantically related to the target words.34 The failure to produce a phonologically matched but semantically relevant response suggests an impairment of processes mediating the access of stimuli to the visual word form system.45 The current literature mainly describes this phenomenon in alphabetic languages, with deep dyslexia largely being observed in the left hemisphere, especially in relation to large perisylvian lesions extending to the frontal lobe.44 Deep dyslexia is generally seen in patients suffering from nonfluent dysphasia, such as left middle cerebral artery infarction, which, so far, has not been associated with any neurodegenerative language disorder, particularly in alphabetic-language speakers, such as English speakers. The postulation of producing such response has been inconclusive, with no clear consensus among experts. While some experts suggest that residual left hemispheric function is responsible for producing such erroneous responses, Coltheart46 proposed that it could, in fact, be due to underlying right hemispheric regions attributed to reading. Generally, deep dyslexic semantic errors are observed when phonological impairment prevents patients from using the surface route/GPC route and limits them to using a deep, direct route; hence, to be prone for erroneous responses with production of semantic errors.
Literature describing acquired dyslexia in the Chinese language remains sparse to date, which may be due to the different mechanisms underpinning such phenomenology. Current studies of the lesioned brain and physiological functional study models support the notion that Chinese language is processed distinctively when compared with alphabetic languages, such as English.7,28,29,47–50 It is demonstrated that orthography in Chinese is more important in accessing semantics than phonology47,49 and that phonology processing in Chinese is distinctive when compared with alphabetic languages.48 While most studies describing Chinese deep dyslexia used a model with a developmental approach, Shu and colleagues, as well as Yin and Butterworth,7,50 described cases with deep dyslexia that involved either trauma- or vascular-related brain lesions, which were explained well by the triangle model. However, most patients suffered more diffuse and less well localized lesions; thus, determining a more precise brain-behavior correlation was challenging.
Current literature suggests the temporal pole as the convergence region for semantic knowledge. Recent studies have also implicated it in lexical-semantic processing. For instance, Busigny et al.51 suggested a case for lexico-facio-semantics disassociation, secondary to a dysfunction in the left anterior temporal lobe. Abel et al. provided neurophysiological evidence that the left and right anterior temporal lobes showed a robust beta-band during visual naming of famous people and tools.52 In studies investigating the temporal lobe in language processing in PPA, Wilson et al. demonstrated that its role in sentence processing is likely to relate to higher level processes such as combinatorial semantic processing,53 while Migliaccio and colleagues demonstrated its role in the binding of lexical and semantic information in a bidirectional manner.54 As Chinese is a logographical language in which semantic data are tagged to each individual character, we speculate that this region also serves as a center of convergence of lexical semantics of the language, particularly in logographical languages. Taking into account the current existing evidence mentioned earlier, it is possible that this region may mediate the semantic relevance of orthographical representations, in this case, observed via an impaired nonsemantic reading pathway.
Another finding in this study is the presence of surface dyslexia in both groups. However, regularization error, or surface dyslexia, was statistically more significantly observed in the English-speaking group. This is consistent with current literature suggesting a dual-route model in reading for alphabetic languages, in which patients with svPPA exhibit an overreliance on the dorsal GPC route, which produces regularization error. While Chinese is considered an opaque language, with regularization errors described in patients with both developmental and acquired dyslexia,9,27 Weekes and Chen predicted, on the basis of the triangle model, that the presence of surface-like dyslexia is attributable to selective damage to the lexical semantic pathway; this type of error is also described as the legitimate alternative reading of components (LARC),55 which was originally described in Japanese speakers.56 In view of the different linguistic characteristics between English and Chinese, as discussed earlier, it is not surprising to observe a much higher rate of surface dyslexia in the English-speaking group. This is consistent with a neurophysiology study suggesting that the more predominant ventral route functions were used when reading Chinese.57 This is also consistent with our previous observation of Chinese-speaking patients with semantic dementia, in whom regularization error was not the most profound dyslexic finding.28,29
Our findings of predominant deep dyslexia with a milder form of regularization errors appeared consistent with the current disease model of acquired dyslexia in Chinese-speaking patients with lesions, most profoundly at the temporal lobe, which is at the ventral route of the dual-route reading model. These results are probably best explained by the triangle model. The surface-like errors observed in this study could be a result of impairment of semantic knowledge, and more common pronunciations of components would dominate computation of phonology from orthography via the lexical nonsemantic pathway as proposed by Yin and colleagues.16
The strength of this study lies in being the first case series describing such a clinical phenomenon, but the significant limiting factors are due to the small sample size. The complete absence of deep dyslexic errors in the English-speaking group also poses challenges for generating a multivariate regression model. Future studies should look into multicenter collaborations, in view of the relatively rarity of the disease itself, and a more consistent or unified clinical approach for better comparison. Further investigation of the performance of Pinyin, particularly in bilingual cases, should also be considered in the future.
Our present study has a few important conclusions. First, the language-finding function in neurodegenerative disorders is likely dependent on the characteristics of the patient’s dominant language. Second, the left temporal pole could possibly act as a convergence center that mediates lexical semantics in logographical languages.
References
1.
Gorno-Tempini ML, Hillis AE, Weintraub S, et al: Classification of primary progressive aphasia and its variants. Neurology 2011; 76:1006–1014
2.
Brambati SM, Ogar J, Neuhaus J, et al: Reading disorders in primary progressive aphasia: a behavioral and neuroimaging study. Neuropsychologia 2009; 47:1893–1900
3.
Mummery CJ, Patterson K, Wise RJ, et al: Disrupted temporal lobe connections in semantic dementia. Brain 1999; 122:61–73
4.
Ho CSH, Chan DWO, Chung KKH, et al: In search of subtypes of Chinese developmental dyslexia. J Exp Child Psychol 2007; 97:61–83
5.
Law SP, Leung MT: Structural representations of characters in Chinese writing: Evidence from a case of acquired dysgraphia. Psychologia 2000; 43:67–83
6.
Yin B, Rohsenow JS: Modern Chinese Characters. Beijing, Sinolingua, 1994
7.
Shu H, Meng X, Chen X, et al: The subtypes of developmental dyslexia in Chinese: evidence from three cases. Dyslexia 2005; 11:311–329
8.
Ho CSH, Bryant P: Phonological skills are important in learning to read Chinese. Dev Psychol 1997; 33:946–951
9.
Wang LC, Yang HM: Classifying Chinese children with dyslexia by dual-route and triangle models of Chinese reading. Res Dev Disabil 2014; 35:2702–2713
10.
McBride-Chang C, Cho JR, Liu H, et al: Changing models across cultures: associations of phonological awareness and morphological structure awareness with vocabulary and word recognition in second graders from Beijing, Hong Kong, Korea, and the United States. J Exp Child Psychol 2005; 92:140–160
11.
Tong X, McBride-Chang C: Longitudinal predictors of very early Chinese literacy acquisition. J Res Read 2011; 34:315–332
12.
Lau DK, Leung MT, Liang Y, et al: Predicting the naming of regular-, irregular- and non-phonetic compounds in Chinese. Clin Linguist Phon 2015; 29:776–792
13.
Law SP, Or B: A case study of acquired dyslexia and dysgraphia in cantonese: evidence for nonsemantic pathways for reading and writing chinese. Cogn Neuropsychol 2001; 18:729–748
14.
Siok WT, Perfetti CA, Jin Z, et al: Biological abnormality of impaired reading is constrained by culture. Nature 2004; 431:71–76
15.
Weekes BS, Chen MJ, Gang YW: Anomia without dyslexia in Chinese. Neurocase 1997; 3:51–60
16.
Yin W, He S, Weekes BS: Acquired dyslexia and dysgraphia in Chinese. Behav Neurol 2005; 16:159–167
17.
Ho FC, Siegel L: Identification of sub-types of students with learning disabilities in reading and its implications for Chinese word recognition and instructional methods in Hong Kong primary schools. Read Writ 2012; 25:1547–1571
18.
Castles A, Coltheart M: Varieties of developmental dyslexia. Cognition 1993; 47:149–180
19.
Manis FR, Seidenberg MS, Doi LM, et al: On the bases of two subtypes of developmental [corrected] dyslexia. Cognition 1996; 58:157–195
20.
Sprenger-Charolles L, Colé P, Lacert P, et al: On subtypes of developmental dyslexia: evidence from processing time and accuracy scores. Can J Exp Psychol 2000; 54:87–104
21.
Stanovich KE, Siegel LS, Gottardo A: Converging evidence for phonological and surface subtypes of reading disability. J Educ Psychol 1997; 89:114–127
22.
Williams MJ, Stuart GW, Castles A, et al: Contrast sensitivity in subgroups of developmental dyslexia. Vision Res 2003; 43:467–477
23.
Ziegler JC, Castel C, Pech-Georgel C, et al: Developmental dyslexia and the dual route model of reading: simulating individual differences and subtypes. Cognition 2008; 107:151–178
24.
Yin WG, Weekes BS: Dyslexia in Chinese: Clues from cognitive neuropsychology. Ann Dyslexia 2003; 53:255–279
25.
Zhang YM, Huang Y, Sun XJ, et al: Clinical and imaging features of a Chinese-speaking man with semantic dementia. J Neurol 2008; 255:297–298
26.
Luo BY, Zhao XY, Wang YW, et al: Is surface dyslexia in Chinese the same as in alphabetic one? Chin Med J (Engl) 2007; 120:348–349
27.
Wu XQ, Liu XJ, Sun ZC, et al: Characteristics of dyslexia and dysgraphia in a Chinese patient with semantic dementia. Neurocase 2015; 21:279–288
28.
Ting SK, Hameed S: “Lexical alexia” in a Chinese semantic dementia patient. J Neuropsychiatry Clin Neurosci 2013; 25:E37–E38
29.
Ting SK, Chia SP, Hameed S: Deep dyslexia in Chinese primary progressive aphasia of semantic variant. J Neuropsychiatry Clin Neurosci 2016; 28:e25–e26
30.
National Alzheimer’s Coordinating Center: For researchers using NACC data –information and resources. Available at: https://www.alz.washington.edu/WEB/researcher_home.html Accessed Jan. 4, 2016.
31.
Paradis M: Principles underlying the Bilingual Aphasia Test (BAT) and its uses. Clin Linguist Phon 2011; 25:427–443
32.
Swinburn K, Porter G, Howard D: Comprehensive Aphasia Test. East Sussex, Psychology Press, 2004
33.
Marshall J, Newcombe F: Syntactic and semantic errors in paralexia. Neuropsychologia 1966; 4:169–176
34.
Marshall JC, Newcombe F: Patterns of paralexia: a psycholinguistic approach. J Psycholinguist Res 1973; 2:175–199
35.
Morton J, Patterson KE: A new attempt at interpretation, or, an attempt at a new interpretation, in Deep Dyslexia. Edited by Coltheart M, Patterson KE, Marshall JC. London, Routledge and Kegan Paul, 1980, pp 91–118
36.
Coltheart M, Curtis B, Atkins P, et al: Models of reading aloud: Dual-route and parallel-distributed-processing approaches. Psychol Rev 1993; 100:589–608
37.
Borowsky R, Cummine J, Owen WJ, et al: FMRI of ventral and dorsal processing streams in basic reading processes: insular sensitivity to phonology. Brain Topogr 2006; 18:233–239
38.
Friederici AD: Pathways to language: fiber tracts in the human brain. Trends Cogn Sci 2009; 13:175–181
39.
Jobard G, Crivello F, Tzourio-Mazoyer N: Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 2003; 20:693–712
40.
Price CJ: The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 2010; 1191:62–88
41.
Pugh KR, Mencl WE, Jenner AR, et al: Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Ment Retard Dev Disabil Res Rev 2000; 6:207–213
42.
Steinbrink C, Vogt K, Kastrup A, et al: The contribution of white and gray matter differences to developmental dyslexia: insights from DTI and VBM at 3.0 T. Neuropsychologia 2008; 46:3170–3178
43.
Ripamonti E, Aggujaro S, Molteni F, et al: The anatomical foundations of acquired reading disorders: a neuropsychological verification of the dual-route model of reading. Brain Lang 2014; 134:44–67
44.
Coltheart M, Patterson K, Marshall JC (ed): Deep Dyslexia. London, Routledge and Kegan Paul, 1980
45.
Colangelo A, Buchanan L: Localizing damage in the functional architecture: The distinction between implicit and explicit processing in deep dyslexia. J Neurolinguist 2007; 20:111–144
46.
Coltheart M: Deep dyslexia is right-hemisphere reading. Brain Lang 2000; 71:299–309
47.
Kong L, Zhang JX, Ho CS, et al: Phonology and access to Chinese character meaning. Psychol Rep 2010; 107:899–913
48.
Tan LH, Laird AR, Li K, et al: Neuroanatomical correlates of phonological processing of Chinese characters and alphabetic words: a meta-analysis. Hum Brain Mapp 2005; 25:83–91
49.
Zhang Q, Damian MF: Effects of orthography on speech production in Chinese. J Psycholinguist Res 2012; 41:267–283
50.
Yin WG, Butterworth B: Deep and surface dyslexia in Chinese, in Language Processing in Chinese. Edited by Chen HC, Tzeng OJL. Amsterdam, Elsevier Science, 1992, pp 349–366
51.
Busigny T, de Boissezon X, Puel M, et al: Proper name anomia with preserved lexical and semantic knowledge after left anterior temporal lesion: a two-way convergence defect. Cortex 2015; 65:1–18
52.
Abel TJ, Rhone AE, Nourski KV, et al: Beta modulation reflects name retrieval in the human anterior temporal lobe: an intracranial recording study. J Neurophysiol 2016; 115:3052–3061
53.
Wilson SM, DeMarco AT, Henry ML, et al: What role does the anterior temporal lobe play in sentence-level processing? Neural correlates of syntactic processing in semantic variant primary progressive aphasia. J Cogn Neurosci 2014; 26:970–985
54.
Migliaccio R, Boutet C, Valabregue R, et al: The Brain network of naming: a lesson from primary progressive aphasia. PLoS One 2016; 11:e0148707
55.
Weekes B, Chen HQ: Surface dyslexia in Chinese. Neurocase 1999; 5:161–172
56.
Patterson K, Suzuki T, Wydell T, et al: Progressive aphasia and surface Alexia in Japanese. Neurocase 1995; 1:155–165
57.
Sun Y, Yang Y, Desroches AS, et al: The role of the ventral and dorsal pathways in reading Chinese characters and English words. Brain Lang 2011; 119:80–88
Information & Authors
Information
Published In
History
Received: 17 April 2017
Revision received: 25 May 2017
Accepted: 2 August 2017
Published online: 24 October 2017
Published in print: Winter 2018
Keywords
Authors
Competing Interests
The authors report no financial relationships with commercial interests.
Funding Information
National Institute on Aging.10.13039/100000049: U01 AG016976
SingHealth Foundation10.13039/501100004327: NRS 15/001
National Medical Research Council10.13039/501100001349: NMRC/IRG/015
National Neuroscience Institute center grantNCG CS02:
Supported by the Singhealth Foundation (grant NRS 15/001); the National Neuroscience Institute Centre (grant NCG CS02); and the National Medical Research Council, Singapore (grant NMRC/IRG/015). The National Alzheimer’s Coordinating Center (NACC) database is funded by NIA/NIH grant U01 AG016976. NACC data are contributed by the following grants to NIA-funded Alzheimer’s Disease Centers (ADCs): P30 AG019610 (principal investigator [PI]: Eric Reiman, M.D.); P30 AG013846 (PI: Neil Kowall, M.D.); P50 AG008702 (PI: Scott Small, M.D.); P50 AG025688 (PI: Allan Levey, M.D., Ph.D.); P50 AG047266 (PI: Todd Golde, M.D., Ph.D.); P30 AG010133 (PI: Andrew Saykin, Psy.D.); P50 AG005146 (PI: Marilyn Albert, Ph.D.); P50 AG005134 (PI: Bradley Hyman, M.D., Ph.D.); P50 AG016574 (PI: Ronald Petersen, M.D., Ph.D.); P50 AG005138 (PI: Mary Sano, Ph.D.); P30 AG008051 (PI: Steven Ferris, Ph.D.); P30 AG013854 (PI: M. Marsel Mesulam, M.D.); P30 AG008017 (PI: Jeffrey Kaye, M.D.); P30 AG010161 (PI: David Bennett, M.D.); P50 AG047366 (PI: Victor Henderson, M.D., M.S.); P30 AG010129 (PI: Charles DeCarli, M.D.); P50 AG016573 (PI: Frank LaFerla, Ph.D.); P50 AG016570 (PI: Marie-Francoise Chesselet, M.D., Ph.D.); P50 AG005131 (PI: Douglas Galasko, M.D.); P50 AG023501 (PI: Bruce Miller, M.D.); P30 AG035982 (PI: Russell Swerdlow, M.D.); P30 AG028383 (PI: Linda Van Eldik, Ph.D.); P30 AG010124 (PI: John Trojanowski, M.D., Ph.D.); P50 AG005133 (PI: Oscar Lopez, M.D.); P50 AG005142 (PI: Helena Chui, M.D.); P30 AG012300 (PI: Roger Rosenberg, M.D.); P50 AG005136 (PI: Thomas Montine, M.D., Ph.D.); P50 AG033514 (PI: Sanjay Asthana, M.D., F.R.C.P.); P50 AG005681 (PI: John Morris, MD); and P50 AG047270 (PI: Stephen Strittmatter, M.D., Ph.D.).Metrics & Citations
Metrics
Citations
Export Citations
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.
For more information or tips please see 'Downloading to a citation manager' in the Help menu.
View Options
View options
PDF/EPUB
View PDF/EPUBLogin options
Already a subscriber? Access your subscription through your login credentials or your institution for full access to this article.
Personal login Institutional Login Open Athens loginNot a subscriber?
PsychiatryOnline subscription options offer access to the DSM-5-TR® library, books, journals, CME, and patient resources. This all-in-one virtual library provides psychiatrists and mental health professionals with key resources for diagnosis, treatment, research, and professional development.
Need more help? PsychiatryOnline Customer Service may be reached by emailing [email protected] or by calling 800-368-5777 (in the U.S.) or 703-907-7322 (outside the U.S.).