Manipulation of Length and Lexicality Localizes the Functional Neuroanatomy of Phonological Processing in Adult Readers

In a previous study of single word reading, regions in the left supramarginal gyrus and left angular gyrus showed positive BOLD activity in children but significantly less activity in adults for high-frequency words [Church, J. A., Coalson, R. S., Lugar, H. M., Petersen, S. E., & Schlaggar, B. L. A developmental fMRI study of reading and repetition reveals changes in phonological and visual mechanisms over age. Cerebral Cortex, 18, 2054–2065, 2008]. This developmental decrease may reflect decreased reliance on phonological processing for familiar stimuli in adults. Therefore, in the present study, variables thought to influence phonological demand (string length and lexicality) were manipulated. Length and lexicality effects in the brain were explored using both ROI and whole-brain approaches. In the ROI analysis, the supramarginal and angular regions from the previous study were applied to this study. The supramarginal region showed a significant positive effect of length, consistent with a role in phonological processing, whereas the angular region showed only negative deflections from baseline with a strong effect of lexicality and other weaker effects. At the whole-brain level, varying effects of length and lexicality and their interactions were observed in 85 regions throughout the brain. The application of hierarchical clustering analysis to the BOLD time course data derived from these regions revealed seven clusters, with potentially revealing anatomical locations. Of note, a left angular gyrus region was the sole constituent of one cluster. Taken together, these findings in adult readers (1) provide support for a widespread set of brain regions affected by lexical variables, (2) corroborate a role for phonological processing in the left supramarginal gyrus, and (3) do not support a strong role for phonological processing in the left angular gyrus.

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

[2]  Jack L. Lancaster,et al.  A modality‐independent approach to spatial normalization of tomographic images of the human brain , 1995 .

[3]  S. Petersen,et al.  Neuroimaging studies of word reading. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Hongtu Zhu,et al.  A developmental fMRI study of self‐regulatory control , 2006, Human brain mapping.

[5]  Guinevere F. Eden,et al.  Neural Systems Affected in Developmental Dyslexia Revealed by Functional Neuroimaging , 1998, Neuron.

[6]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[7]  Michael P Milham,et al.  Reading networks at rest. , 2010, Cerebral cortex.

[8]  Steven E. Petersen,et al.  Automated method for extracting response latencies of subject vocalizations in event-related fMRI experiments☆ , 2003, NeuroImage.

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

[10]  Zhong-Lin Lu,et al.  Sensitivity to orthographic familiarity in the occipito-temporal region , 2008, NeuroImage.

[11]  Karl J. Friston,et al.  Dissociating Reading Processes on the Basis of Neuronal Interactions , 2005, Journal of Cognitive Neuroscience.

[12]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[13]  S. Petersen,et al.  Developmental changes in human cerebral functional organization for word generation. , 2005, Cerebral cortex.

[14]  Bruce D. McCandliss,et al.  Development of neural systems for reading. , 2007, Annual review of neuroscience.

[15]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[16]  S. Dehaene,et al.  The visual word form area: a prelexical representation of visual words in the fusiform gyrus , 2002, Neuroreport.

[17]  M. Raichle The Brain's Dark Energy , 2006, Science.

[18]  Martin Kronbichler,et al.  Taxi vs. Taksi: On Orthographic Word Recognition in the Left Ventral Occipitotemporal Cortex , 2007, Journal of Cognitive Neuroscience.

[19]  D. V. van Essen,et al.  Windows on the brain: the emerging role of atlases and databases in neuroscience , 2002, Current Opinion in Neurobiology.

[20]  Marcus E Raichle,et al.  Neuroscience. The brain's dark energy. , 2006, Science.

[21]  S. Petersen,et al.  A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging , 2003, Neuropsychologia.

[22]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

[23]  Jeffrey R. Binder,et al.  Some neurophysiological constraints on models of word naming , 2005, NeuroImage.

[24]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

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

[27]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[28]  James L. McClelland,et al.  A distributed, developmental model of word recognition and naming. , 1989, Psychological review.

[29]  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 .

[30]  S. Petersen,et al.  The “Task B problem” and other considerations in developmental functional neuroimaging , 2010, Human brain mapping.

[31]  K. Pugh,et al.  Temporal course of word recognition in skilled readers: A magnetoencephalography study , 2009, Behavioural Brain Research.

[32]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[33]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[34]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: I. An account of basic findings. , 1981 .

[35]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[36]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[37]  William W. Graves,et al.  Neural Systems for Reading Aloud: A Multiparametric Approach , 2009, Cerebral cortex.

[38]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[39]  Paul W. B. Atkins,et al.  Models of reading aloud: Dual-route and parallel-distributed-processing approaches. , 1993 .

[40]  D. V. Essen,et al.  Surface-Based and Probabilistic Atlases of Primate Cerebral Cortex , 2007, Neuron.

[41]  G. Box Some Theorems on Quadratic Forms Applied in the Study of Analysis of Variance Problems, I. Effect of Inequality of Variance in the One-Way Classification , 1954 .

[42]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[43]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[44]  Thomas J. Grabowski,et al.  Analysis of speech-related variance in rapid event-related fMRI using a time-aware acquisition system , 2006, NeuroImage.

[45]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

[46]  G. Box Some Theorems on Quadratic Forms Applied in the Study of Analysis of Variance Problems, II. Effects of Inequality of Variance and of Correlation Between Errors in the Two-Way Classification , 1954 .

[47]  A. Mechelli,et al.  Neuroimaging Studies of Word and Pseudoword Reading: Consistencies, Inconsistencies, and Limitations , 2003, Journal of Cognitive Neuroscience.

[48]  C. Price The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

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

[50]  R. Buckner,et al.  Cluster size thresholds for assessment of significant activation in fMRI , 2001, NeuroImage.

[51]  M. Mesulam,et al.  Shifts of Effective Connectivity within a Language Network during Rhyming and Spelling , 2005, The Journal of Neuroscience.

[52]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[53]  Steven E Petersen,et al.  A Comparison of Analysis of Variance and Correlation Methods for Investigating Cognitive Development With Functional Magnetic Resonance Imaging , 2006, Developmental neuropsychology.

[54]  R. Salmelin,et al.  Neural Correlates of Letter-String Length and Lexicality during Reading in a Regular Orthography , 2003, Journal of Cognitive Neuroscience.

[55]  Kristina M. Visscher,et al.  Functional Neuroanatomical Differences Between Adults and School-Age Children in the Processing of Single Words , 2002, Science.

[56]  Stanislas Dehaene,et al.  Specialization within the ventral stream: the case for the visual word form area , 2004, NeuroImage.

[57]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Martin Kronbichler,et al.  On the Functional Neuroanatomy of Visual Word Processing: Effects of Case and Letter Deviance , 2009, Journal of Cognitive Neuroscience.

[59]  Martin Kronbichler,et al.  The visual word form area and the frequency with which words are encountered: evidence from a parametric fMRI study , 2004, NeuroImage.

[60]  James L. McClelland,et al.  Understanding normal and impaired word reading: computational principles in quasi-regular domains. , 1996, Psychological review.

[61]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI I. The Method , 2001, NeuroImage.

[62]  N. Geschwind Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[63]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Jacqueline Cummine,et al.  Understanding white matter integrity stability for bilinguals on language status and reading performance , 2012, Brain Structure and Function.

[65]  R W Cox,et al.  Event‐related fMRI of tasks involving brief motion , 1999, Human brain mapping.

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

[67]  Karl J. Friston,et al.  The Effects of Presentation Rate During Word and Pseudoword Reading: A Comparison of PET and fMRI , 2000, Journal of Cognitive Neuroscience.

[68]  Mark S. Seidenberg,et al.  Phonology, reading acquisition, and dyslexia: insights from connectionist models. , 1999, Psychological review.

[69]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[70]  J. Riddoch,et al.  Reading without the left ventral occipito-temporal cortex , 2012, Neuropsychologia.

[71]  H. Wimmer,et al.  Evidence for a dysfunction of left posterior reading areas in German dyslexic readers , 2006, Neuropsychologia.

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

[73]  Steven E Petersen,et al.  Matching is not naming: A direct comparison of lexical manipulations in explicit and implicit reading tasks , 2013, Human brain mapping.

[74]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[75]  Max Coltheart,et al.  Is there serial processing in the reading system; and are there local representations? , 2006 .

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

[77]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[78]  Timothy T. Brown,et al.  Investigation of the Functional Neuroanatomy of Single Word Reading and Its Development , 2004, The Cognitive Neuroscience of Reading.

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

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

[81]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

[82]  Steven E. Petersen,et al.  The hemodynamic response in children with Simplex Autism , 2012, Developmental Cognitive Neuroscience.

[83]  Rebecca Treiman,et al.  The English Lexicon Project , 2007, Behavior research methods.

[84]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[85]  S. Petersen,et al.  A developmental fMRI study of reading and repetition reveals changes in phonological and visual mechanisms over age. , 2008, Cerebral cortex.

[86]  S. Petersen,et al.  The putative visual word form area is functionally connected to the dorsal attention network. , 2012, Cerebral cortex.

[87]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[88]  Douglas B. Kell,et al.  Computational cluster validation in post-genomic data analysis , 2005, Bioinform..

[89]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[90]  B. Weekes Differential Effects of Number of Letters on Word and Nonword Naming Latency , 1997 .

[91]  M. Coltheart,et al.  Whammies and double whammies: The effect of length on nonword reading , 1998 .

[92]  Dietmar Cordes,et al.  Hierarchical clustering to measure connectivity in fMRI resting-state data. , 2002, Magnetic resonance imaging.

[93]  Thomas A Zeffiro,et al.  Development of neural mechanisms for reading , 2003, Nature Neuroscience.

[94]  H. Wimmer,et al.  Functional abnormalities in the dyslexic brain: A quantitative meta‐analysis of neuroimaging studies , 2009, Human brain mapping.

[95]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[96]  James L. McClelland,et al.  Dissociating stimulus‐driven semantic and phonological effect during reading and naming , 2006, Human brain mapping.

[97]  Daniel Brandeis,et al.  Children with dyslexia lack multiple specializations along the visual word-form (VWF) system , 2009, NeuroImage.

[98]  M. Just,et al.  From the Selectedworks of Marcel Adam Just Neural Basis of Dyslexia: a Comparison between Dyslexic and Non-dyslexic Children Equated for Reading Ability Neural Basis of Dyslexia: a Comparison between Dyslexic and Nondyslexic Children Equated for Reading Ability , 2022 .

[99]  P. Skudlarski,et al.  Disruption of posterior brain systems for reading in children with developmental dyslexia , 2002, Biological Psychiatry.

[100]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.