Language Differences in the Brain Network for Reading in Naturalistic Story Reading and Lexical Decision

Differences in how writing systems represent language raise important questions about whether there could be a universal functional architecture for reading across languages. In order to study potential language differences in the neural networks that support reading skill, we collected fMRI data from readers of alphabetic (English) and morpho-syllabic (Chinese) writing systems during two reading tasks. In one, participants read short stories under conditions that approximate natural reading, and in the other, participants decided whether individual stimuli were real words or not. Prior work comparing these two writing systems has overwhelmingly used meta-linguistic tasks, generally supporting the conclusion that the reading system is organized differently for skilled readers of Chinese and English. We observed that language differences in the reading network were greatly dependent on task. In lexical decision, a pattern consistent with prior research was observed in which the Middle Frontal Gyrus (MFG) and right Fusiform Gyrus (rFFG) were more active for Chinese than for English, whereas the posterior temporal sulcus was more active for English than for Chinese. We found a very different pattern of language effects in a naturalistic reading paradigm, during which significant differences were only observed in visual regions not typically considered specific to the reading network, and the middle temporal gyrus, which is thought to be important for direct mapping of orthography to semantics. Indeed, in areas that are often discussed as supporting distinct cognitive or linguistic functions between the two languages, we observed interaction. Specifically, language differences were most pronounced in MFG and rFFG during the lexical decision task, whereas no language differences were observed in these areas during silent reading of text for comprehension.

[1]  S Lehéricy,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. , 2000, Brain : a journal of neurology.

[2]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

[3]  M Coltheart,et al.  DRC: a dual route cascaded model of visual word recognition and reading aloud. , 2001, Psychological review.

[4]  J. Hsiao,et al.  Position of phonetic components may influence how written words are processed in the brain: Evidence from Chinese phonetic compound pronunciation , 2010, Cognitive, affective & behavioral neuroscience.

[5]  E. Grigorenko,et al.  Phonological awareness predicts activation patterns for print and speech , 2009, Annals of dyslexia.

[6]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

[7]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[8]  T. Rogers,et al.  Anterior temporal cortex and semantic memory: Reconciling findings from neuropsychology and functional imaging , 2006, Cognitive, affective & behavioral neuroscience.

[9]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[10]  J. Zevin,et al.  The impact of task demand on visual word recognition , 2014, Neuroscience.

[11]  Jianfeng Yang,et al.  Orthographic influences on division of labor in learning to read Chinese and English: Insights from computational modeling* , 2012, Bilingualism: Language and Cognition.

[12]  Michael J Cortese,et al.  Visual word recognition of single-syllable words. , 2004, Journal of experimental psychology. General.

[13]  Gary H. Glover,et al.  Reducing interscanner variability of activation in a multicenter fMRI study: Controlling for signal-to-fluctuation-noise-ratio (SFNR) differences , 2006, NeuroImage.

[14]  D. Burman,et al.  Differential prefrontal–temporal neural correlates of semantic processing in children , 2006, Brain and Language.

[15]  Hua Shu,et al.  Simulating Language-specific and Language-general Effects in a Statistical Learning Model of Chinese Reading. , 2009, Journal of memory and language.

[16]  Mark S. Seidenberg,et al.  Reading in different writing systems: One architecture, multiple solutions. , 2011 .

[17]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

[18]  W. Schneider,et al.  Cross‐cultural effect on the brain revisited: Universal structures plus writing system variation , 2005, Human brain mapping.

[19]  Brenna Argall,et al.  SUMA: an interface for surface-based intra- and inter-subject analysis with AFNI , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[20]  P. Fox,et al.  Neuroanatomical correlates of phonological processing of Chinese characters and alphabetic words: A meta‐analysis , 2005, Human brain mapping.

[21]  Jianfeng Yang,et al.  Left fusiform BOLD responses are inversely related to word-likeness in a one-back task , 2011, NeuroImage.

[22]  Hyun Wook Park,et al.  An fMRI study of Chinese character reading and picture naming by native Korean speakers , 2006, Neuroscience Letters.

[23]  L. Tan,et al.  Biological abnormality of impaired reading is constrained by culture , 2004, Nature.

[24]  S E Shaywitz,et al.  Neurobiological studies of reading and reading disability. , 2001, Journal of communication disorders.

[25]  L. Tan,et al.  Distinct brain regions associated with syllable and phoneme , 2003, Human brain mapping.

[26]  James R. Booth,et al.  Specialization of phonological and semantic processing in Chinese word reading , 2006, Brain Research.

[27]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[28]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[29]  R. Rosenfeld Patients , 2012, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[30]  Jun-Young Chung,et al.  Neural mechanisms of Korean word reading: a functional magnetic resonance imaging study , 2005, Neuroscience Letters.

[31]  D. V. von Cramon,et al.  Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[32]  M. Chee,et al.  Overlap and Dissociation of Semantic Processing of Chinese Characters, English Words, and Pictures: Evidence from fMRI , 2000, NeuroImage.

[33]  Shen-Hsing Annabel Chen,et al.  A meta-analysis of fMRI studies on Chinese orthographic, phonological, and semantic processing , 2012, NeuroImage.

[34]  S. Petersen,et al.  The left occipitotemporal cortex does not show preferential activity for words. , 2012, Cerebral cortex.

[35]  G. Humphreys,et al.  Segregating Semantic from Phonological Processes during Reading , 1997, Journal of Cognitive Neuroscience.

[36]  António Sérgio Damásio,et al.  Cortical Midline Structures and Autobiographical-Self Processes: An Activation-Likelihood Estimation Meta-Analysis , 2013, Front. Hum. Neurosci..

[37]  R. Malach,et al.  Syntactic structure building in the anterior temporal lobe during natural story listening , 2012, Brain and Language.

[38]  Michel Paradis,et al.  Visible speech: The diverse oneness of writing systems , 1990 .

[39]  Jianfeng Yang,et al.  Task by stimulus interactions in brain responses during Chinese character processing , 2012, NeuroImage.

[40]  Graham Thurgood,et al.  The Sino-Tibetan Languages , 2016 .

[41]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[42]  Jay G. Rueckl,et al.  A functional magnetic resonance imaging study of the tradeoff between semantics and phonology in reading aloud , 2005, Neuroreport.

[43]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[44]  David A. Balota,et al.  Attentional Control and Flexible Lexical Processing : Explorations of the Magic Moment of Word Recognition , 2007 .

[45]  Phillip J. Holcomb,et al.  Making sense of discourse: An fMRI study of causal inferencing across sentences , 2006, NeuroImage.

[46]  M. Kutas,et al.  Semantic integration in reading: engagement of the right hemisphere during discourse processing. , 1999, Brain : a journal of neurology.

[47]  N. Stanietsky,et al.  The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity , 2009, Proceedings of the National Academy of Sciences.

[48]  B. Argall,et al.  Simplified intersubject averaging on the cortical surface using SUMA , 2006, Human brain mapping.

[49]  Ying Liu,et al.  Evidence for neural accommodation to a writing system following learning , 2007, Human brain mapping.

[50]  James A. Reggia,et al.  Empirically derived probabilities for grapheme-to-phoneme correspondences in english , 1987 .

[51]  U. Hasson,et al.  Speaker–listener neural coupling underlies successful communication , 2010, Proceedings of the National Academy of Sciences.

[52]  Mark S. Seidenberg,et al.  Computing the meanings of words in reading: cooperative division of labor between visual and phonological processes. , 2004, Psychological review.

[53]  L. Katz,et al.  Cerebral organization of component processes in reading. , 1996, Brain : a journal of neurology.

[54]  A. Liberman,et al.  Functional disruption in the organization of the brain for reading in dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J B Poline,et al.  Letter Binding and Invariant Recognition of Masked Words , 2004, Psychological science.

[56]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[57]  J. Xiong,et al.  Neural systems of second language reading are shaped by native language , 2003 .

[58]  Jonas Obleser,et al.  Disentangling syntax and intelligibility in auditory language comprehension , 2009, Human brain mapping.

[59]  Sally Andrews,et al.  From inkmarks to ideas : current issues in lexical processing , 2006 .

[60]  Thomas Crump,et al.  Visible Speech: The Diverse Oneness of Writing Systems. , 1990 .

[61]  Ying Liu,et al.  The lexical constituency model: some implications of research on Chinese for general theories of reading. , 2005, Psychological review.

[62]  D. Balota,et al.  Are lexical decisions a good measure of lexical access? The role of word frequency in the neglected decision stage. , 1984, Journal of experimental psychology. Human perception and performance.

[63]  Stanislas Dehaene,et al.  Universal brain systems for recognizing word shapes and handwriting gestures during reading , 2012, Proceedings of the National Academy of Sciences.

[64]  P. Fox,et al.  The Neural System Underlying Chinese Logograph Reading , 2001, NeuroImage.

[65]  H. Shu,et al.  Brain networks associated with sublexical properties of Chinese characters , 2011, Brain and Language.

[66]  Ram Frost,et al.  Towards a universal model of reading , 2012, Behavioral and Brain Sciences.

[67]  R. Nathan Spreng,et al.  Patterns of Brain Activity Supporting Autobiographical Memory, Prospection, and Theory of Mind, and Their Relationship to the Default Mode Network , 2010, Journal of Cognitive Neuroscience.

[68]  J. Obleser,et al.  Expectancy constraints in degraded speech modulate the language comprehension network. , 2010, Cerebral cortex.