Not All Reading Disabilities Are Dyslexia: Distinct Neurobiology of Specific Comprehension Deficits

Although an extensive literature exists on the neurobiological correlates of dyslexia (DYS), to date, no studies have examined the neurobiological profile of those who exhibit poor reading comprehension despite intact word-level abilities (specific reading comprehension deficits [S-RCD]). Here we investigated the word-level abilities of S-RCD as compared to typically developing readers (TD) and those with DYS by examining the blood oxygenation-level dependent response to words varying on frequency. Understanding whether S-RCD process words in the same manner as TD, or show alternate pathways to achieve normal word-reading abilities, may provide insights into the origin of this disorder. Results showed that as compared to TD, DYS showed abnormal covariance during word processing with right-hemisphere homologs of the left-hemisphere reading network in conjunction with left occipitotemporal underactivation. In contrast, S-RCD showed an intact neurobiological response to word stimuli in occipitotemporal regions (associated with fast and efficient word processing); however, inferior frontal gyrus (IFG) abnormalities were observed. Specifically, TD showed a higher-percent signal change within right IFG for low-versus-high frequency words as compared to both S-RCD and DYS. Using psychophysiological interaction analyses, a coupling-by-reading group interaction was found in right IFG for DYS, as indicated by a widespread greater covariance between right IFG and right occipitotemporal cortex/visual word-form areas, as well as bilateral medial frontal gyrus, as compared to TD. For S-RCD, the context-dependent functional interaction anomaly was most prominently seen in left IFG, which covaried to a greater extent with hippocampal, parahippocampal, and prefrontal areas than for TD for low- as compared to high-frequency words. Given the greater lexical access demands of low frequency as compared to high-frequency words, these results may suggest specific weaknesses in accessing lexical-semantic representations during word recognition. These novel findings provide foundational insights into the nature of S-RCD, and set the stage for future investigations of this common, but understudied, reading disorder.

[1]  K. Nation Reading and language in children: Exposing hidden deficits , 2001 .

[2]  L. Katz,et al.  Functional neuroimaging studies of reading and reading disability (developmental dyslexia). , 2000, Mental retardation and developmental disabilities research reviews.

[3]  M. Seghier,et al.  Functional Subdivisions in the Left Angular Gyrus Where the Semantic System Meets and Diverges from the Default Network , 2010, The Journal of Neuroscience.

[4]  K. Nation,et al.  Developmental differences in sensitivity to semantic relations among good and poor comprehenders: evidence from semantic priming , 1999, Cognition.

[5]  K. Cain,et al.  To get hold of the wrong end of the stick: reasons for poor idiom understanding in children with reading comprehension difficulties. , 2008, Journal of speech, language, and hearing research : JSLHR.

[6]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[7]  J. Fletcher,et al.  Cerebral mechanisms involved in word reading in dyslexic children: a magnetic source imaging approach. , 2000, Cerebral cortex.

[8]  C. A. Rashotte,et al.  Test of Word Reading Efficiency , 1999 .

[9]  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.

[10]  Rutvik H. Desai,et al.  The neurobiology of semantic memory , 2011, Trends in Cognitive Sciences.

[11]  S. Bradley-Johnson,et al.  Test of Language Development‐Primary: Third edition , 1998 .

[12]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[13]  John O. Willis,et al.  Peabody Picture Vocabulary Test–Third Edition , 2008 .

[14]  Anthony Randal McIntosh,et al.  A common functional brain network for autobiographical, episodic, and semantic memory retrieval , 2010, NeuroImage.

[15]  Suiping Wang,et al.  The role of left inferior frontal gyrus in explicit and implicit semantic processing , 2012, Brain Research.

[16]  Martin Kronbichler,et al.  Meta-analyzing brain dysfunctions in dyslexic children and adults , 2011, NeuroImage.

[17]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

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

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

[20]  Dorothy V M Bishop,et al.  A longitudinal investigation of early reading and language skills in children with poor reading comprehension. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[21]  John O. Willis,et al.  Test of Language Development—Primary, Fourth Edition , 2008 .

[22]  D. Wechsler Wechsler Intelligence Scale for Children , 2020, Definitions.

[23]  K. Stanovich TOWARD AN INTERACTIVE-COMPENSATORY MODEL OF INDIVIDUAL DIFFERENCES IN THE DEVELOPMENT OF READING FLUENCY , 1980 .

[24]  Kate Nation,et al.  Suppressing Irrelevant Information from Working Memory: Evidence for Domain-Specific Deficits in Poor Comprehenders. , 2010 .

[25]  K. A. Williams,et al.  Not All Reading Disabilities Are Alike , 1999, Journal of learning disabilities.

[26]  E. Mahone,et al.  Executive Dysfunction Among Children With Reading Comprehension Deficits , 2010, Journal of learning disabilities.

[27]  Bruce D. McCandliss,et al.  Neural systems predicting long-term outcome in dyslexia , 2010, Proceedings of the National Academy of Sciences.

[28]  Joseph K. Torgesen,et al.  Individual Differences in Response to Early Interventions in Reading: The Lingering Problem of Treatment Resisters , 2000 .

[29]  F. Richlan Developmental dyslexia: dysfunction of a left hemisphere reading network , 2012, Front. Hum. Neurosci..

[30]  K. Amunts,et al.  Left cytoarchitectonic area 44 supports selection in the mental lexicon during language production , 2009, Brain Structure and Function.

[31]  D. Francis,et al.  Intelligent testing and the discrepancy model for children with learning disabilities. , 1998 .

[32]  M. Coltheart,et al.  Serial and strategic effects in reading aloud , 1999 .

[33]  E. Kaplan,et al.  Delis-Kaplan Executive Function System , 2012 .

[34]  Daniel Brandeis,et al.  Evidence for developmental changes in the visual word processing network beyond adolescence , 2006, NeuroImage.

[35]  D. Fulker,et al.  Specific Deficits in Component Reading and Language Skills , 1989, Journal of learning disabilities.

[36]  H. Scarborough,et al.  Late-emerging reading disabilities. , 2003 .

[37]  David Badre,et al.  Semantic retrieval, mnemonic control, and prefrontal cortex. , 2002, Behavioral and cognitive neuroscience reviews.

[38]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[39]  Laurie E. Cutting,et al.  Prediction of Reading Comprehension: Relative Contributions of Word Recognition, Language Proficiency, and Other Cognitive Skills Can Depend on How Comprehension Is Measured , 2006 .

[40]  G. Lyon,et al.  Toward a definition of dyslexia , 1995, Annals of dyslexia.

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

[42]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

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

[44]  Jane Oakhill,et al.  Matthew Effects in Young Readers , 2011, Journal of learning disabilities.

[45]  Jane Oakhill,et al.  Profiles of children with specific reading comprehension difficulties. , 2006, The British journal of educational psychology.

[46]  E. Mahone,et al.  Effects of fluency, oral language, and executive function on reading comprehension performance , 2009, Annals of dyslexia.

[47]  Marilyn Jager Adams,et al.  Beginning To Read: Thinking and Learning about Print. , 1991 .

[48]  Gian Luca Romani,et al.  Low- and high-frequency evoked responses following pattern reversal stimuli: A MEG study supported by fMRI constraint , 2007, NeuroImage.

[49]  Kate Cain,et al.  Individual differences in children's memory and reading comprehension: An investigation of semantic and inhibitory deficits , 2006, Memory.

[50]  J. Maisog,et al.  A positron emission tomographic study of impaired word recognition and phonological processing in dyslexic men. , 1997, Archives of neurology.

[51]  Jonathan L Preston,et al.  Early and late talkers: school-age language, literacy and neurolinguistic differences. , 2010, Brain : a journal of neurology.

[52]  Joe P. Sutton,et al.  Woodcock Reading Mastery Tests Revised/Normative Update (WRMT-R/NU) , 1999 .

[53]  A. Liberman,et al.  The Angular Gyrus in Developmental Dyslexia: Task-Specific Differences in Functional Connectivity Within Posterior Cortex , 2000, Psychological science.

[54]  Margaret J. Snowling,et al.  Semantic processing and the development of word-recognition skills: Evidence from children with reading comprehension difficulties. , 1998 .

[55]  F. Fazio,et al.  Dyslexia: Cultural Diversity and Biological Unity , 2001, Science.

[56]  D. Cordes,et al.  Low-frequency signal changes reflect differences in functional connectivity between good readers and dyslexics during continuous phoneme mapping. , 2006, Magnetic resonance imaging.

[57]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[58]  Donald Shankweiler,et al.  Words to Meanings , 1999 .

[59]  R D Abbott,et al.  Dyslexic children have abnormal brain lactate response to reading-related language tasks. , 1999, AJNR. American journal of neuroradiology.

[60]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.