Reading therapy strengthens top–down connectivity in patients with pure alexia

This study tested the efficacy of audio-visual reading training in nine patients with pure alexia, an acquired reading disorder caused by damage to the left ventral occipitotemporal cortex. As well as testing the therapy’s impact on reading speed, we investigated the functional reorganization underlying therapy-induced behavioural changes using magnetoencephalography. Reading ability was tested twice before training (t1 and t2) and twice after completion of the 6-week training period (t3 and t4). At t3 there was a significant improvement in word reading speed and reduction of the word length effect for trained words only. Magnetoencephalography at t3 demonstrated significant differences in reading network connectivity for trained and untrained words. The training effects were supported by increased bidirectional connectivity between the left occipital and ventral occipitotemporal perilesional cortex, and increased feedback connectivity from the left inferior frontal gyrus. Conversely, connection strengths between right hemisphere regions became weaker after training.

[1]  H. Branch Coslett,et al.  Reading in pure alexiaThe effect of strategy , 1993 .

[2]  A. Leff,et al.  Structural anatomy of pure and hemianopic alexia , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[3]  Walter Schneider,et al.  In vivo quantification of global connectivity in the human corpus callosum , 2012, NeuroImage.

[4]  H B Coslett,et al.  Reading in pure alexia. The effect of strategy. , 1993, Brain : a journal of neurology.

[5]  Stéphane Lehéricy,et al.  The pathophysiology of letter-by-letter reading , 2004, Neuropsychologia.

[6]  M. Behrmann,et al.  Treatment of reading impairment after stroke , 2008, Current opinion in neurology.

[7]  D. Plaut,et al.  A LITERATURE REVIEW AND NEW DATA SUPPORTING AN INTERACTIVE ACCOUNT OF LETTER-BY-LETTER READING. , 1998, Cognitive neuropsychology.

[8]  J. Binder,et al.  The topography of callosal reading pathways. A case-control analysis. , 1992, Brain : a journal of neurology.

[9]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[10]  Karl J. Friston,et al.  Dynamic causal modeling of evoked responses in EEG and MEG , 2006, NeuroImage.

[11]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  F. Gobet,et al.  The Cambridge handbook of expertise and expert performance , 2006 .

[13]  Taraz G. Lee,et al.  The Dynamic Nature of Top-Down Signals Originating from Prefrontal Cortex: A Combined fMRI–TMS Study , 2012, The Journal of Neuroscience.

[14]  M. Laine,et al.  Multiple oral rereading technique in rehabilitation of pure alexia , 1991 .

[15]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[16]  R. Friedman,et al.  Multiple Oral Re-reading treatment for alexia: The parts may be greater than the whole , 2010, Neuropsychological rehabilitation.

[17]  Marlene Behrmann,et al.  Visuoperceptual deficits in letter-by-letter reading? , 2009, Neuropsychologia.

[18]  Laurie S. Glezer,et al.  Overt use of a tactile/kinaesthetic strategy shifts to covert processing in rehabilitation of letter-by-letter reading , 2010, Aphasiology.

[19]  G. Nolte The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. , 2003, Physics in medicine and biology.

[20]  D. Mumford On the computational architecture of the neocortex , 2004, Biological Cybernetics.

[21]  Brian A. Wandell,et al.  Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections , 2013, Brain and Language.

[22]  Karl J. Friston,et al.  Dynamic causal modeling for EEG and MEG , 2009, Human brain mapping.

[23]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses: The role of intrinsic connections , 2007, NeuroImage.

[24]  Joseph T Devlin,et al.  The myth of the visual word form area , 2003, NeuroImage.

[25]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[26]  J. Winn,et al.  Brain , 1878, The Lancet.

[27]  R. Friedman,et al.  Rationale and efficacy of a tactile—kinaesthetic treatment for alexia , 1994 .

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

[29]  Stanislas Dehaene,et al.  Brain activations during letter-by-letter reading: A follow-up study , 2005, Neuropsychologia.

[30]  R. Friedman,et al.  Rapid Word Identification in Pure Alexia Is Lexical but Not Semantic , 2000, Brain and Language.

[31]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[32]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[33]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[34]  M. Bar,et al.  Magnocellular Projections as the Trigger of Top-Down Facilitation in Recognition , 2007, The Journal of Neuroscience.

[35]  K. Seki,et al.  The efficacy of kinesthetic reading treatment for pure alexia , 1995, Neuropsychologia.

[36]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[37]  S. B. Moyer Rehabilitation of Alexia: A Case Study , 1979, Cortex.

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

[39]  A P Leff,et al.  The functional anatomy of single-word reading in patients with hemianopic and pure alexia. , 2001, Brain : a journal of neurology.

[40]  Bruce D. McCandliss,et al.  Fast, visual specialization for reading in English revealed by the topography of the N170 ERP response , 2005, Behavioral and Brain Functions.

[41]  Karl J. Friston,et al.  Dynamic causal modeling for EEG and MEG , 2009, Human brain mapping.

[42]  M. L. Ralph,et al.  Using errorless learning to treat letter-by-letter reading: Contrasting word versus letter-based therapy , 2005, Neuropsychological rehabilitation.

[43]  H. Coslett,et al.  IMPLICIT VS. LETTER-BY-LETTER READING IN PURE ALEXIA: A TALE OF TWO SYSTEMS. , 1998, Cognitive neuropsychology.

[44]  D Mumford,et al.  On the computational architecture of the neocortex. II. The role of cortico-cortical loops. , 1992, Biological cybernetics.

[45]  Michael Wilson MRC Psycholinguistic Database , 2001 .

[46]  Katherine L. Wheat,et al.  During Visual Word Recognition, Phonology Is Accessed within 100 ms and May Be Mediated by a Speech Production Code: Evidence from Magnetoencephalography , 2010, The Journal of Neuroscience.

[47]  Michael S C Thomas,et al.  Multiple Routes from Occipital to Temporal Cortices during Reading , 2011, The Journal of Neuroscience.

[48]  Yehezkel Yeshurun,et al.  Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation , 2006, NeuroImage.

[49]  M. Behrmann,et al.  Rehabilitation for Pure Alexia: Efficacy of Therapy and Implications for Models of Normal Word Recognition , 1995 .

[50]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

[51]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[52]  P. Holcomb,et al.  Cross-modal semantic priming: A time-course analysis using event-related brain potentials , 1993 .

[53]  C. J. Long,et al.  Remediation of alexia without agraphia: a case study. , 1995, Brain injury.

[54]  D. Bub,et al.  Pure Alexia: Attempted Rehabilitation and Its Implications for Interpretation of the Deficit , 1994, Brain and Language.

[55]  W. Penny,et al.  Reading Front to Back: MEG Evidence for Early Feedback Effects During Word Recognition , 2012, Cerebral cortex.

[56]  M. Kringelbach,et al.  Activation of the Left Inferior Frontal Gyrus in the First 200 ms of Reading: Evidence from Magnetoencephalography (MEG) , 2009, PloS one.

[57]  L. G. Gonzalez Rothi,et al.  Rehabilitation of a case of pure alexia: exploiting residual abilities. , 2000, Journal of the International Neuropsychological Society : JINS.

[58]  M. Lee,et al.  Statistical Evidence in Experimental Psychology , 2011, Perspectives on psychological science : a journal of the Association for Psychological Science.

[59]  Alexander P. Leff,et al.  Too Little, Too Late: Reduced Visual Span and Speed Characterize Pure Alexia , 2009, Cerebral cortex.

[60]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[61]  A. Damasio,et al.  The anatomic basis of pure alexia , 1983, Neurology.

[62]  Glyn W. Humphreys,et al.  BORB: Birmingham Object Recognition Battery , 2017 .

[63]  P Berg,et al.  A multiple source approach to the correction of eye artifacts. , 1994, Electroencephalography and clinical neurophysiology.

[64]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

[65]  T Shallice,et al.  Word-form dyslexia. , 1980, Brain : a journal of neurology.

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

[67]  Irene Ablinger,et al.  Improved single-letter identification after whole-word training in pure alexia , 2009, Neuropsychological rehabilitation.

[68]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

[69]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[70]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses in EEG/MEG with lead field parameterization , 2006, NeuroImage.

[71]  Karalyn Patterson,et al.  Selective disorders of reading? , 1999, Current Opinion in Neurobiology.

[72]  Karl J. Friston,et al.  Variational Bayesian inversion of the equivalent current dipole model in EEG/MEG , 2008, NeuroImage.

[73]  M. Sigman,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.7 July 2005 The neural code for written words: a proposal , 2022 .

[74]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..