An fMRI study of the differential effects of word presentation rates (reading acceleration) on dyslexic readers' brain activity patterns

Abstract Several lines of evidence have recently provided a clear indication that word reading rate can be considered as an independent variable which influences comprehension as well as accuracy in reading. Thus, not only is fluent reading a critical characteristic of skilled (automatic) reading, it has been shown that faster reading does not necessarily incur a cost in terms of accuracy. Indeed, readers of various levels of reading proficiency, as well as clearly impaired readers (dyslexics), if made to read faster than their normal (routine) reading rate, can increase their decoding accuracy and comprehension. Using block design, blood-(de)oxygenation-level-dependent (BOLD) functional magnetic resonance imaging we studied the differences in brain activation patterns induced by reading and script processing in adult dyslexics and normal reading controls as a function of two word presentation rates. Word presentation rates were set individually for each participant to correspond to his/her routine reading rate (slow) and to a correspondingly faster rate (fast). Three task conditions were tested: sentences (plausibility judgment), single words (concrete/abstract judgment), non-words (homophonic judgment). Comprehension and accuracy in the faster presentation rates were unimpaired in both groups. There were no significant differences between the activation patterns induced in both groups in ‘slow’ reading of sentences and single words, but ‘fast’ reading was related to higher activations in visual areas in the normal readers. However, in the slow non-words condition the dyslexics were characterized by activations in the Lt IFG (Broca's area) and operculum, while the control readers clearly activated visual processing areas (extra-striate cortex). These differences in brain activation patterns were not found in the fast non-words condition. We propose that time-constrained (accelerated) script decoding may prompt the dyslexic brain to process graphemic information in a different manner compared to the one employed in unconstrained (routine) reading, in some conditions in a manner of processing much closer to the one employed by normal reading controls.

[1]  R. Frackowiak,et al.  Demonstrating the implicit processing of visually presented words and pseudowords. , 1996, Cerebral cortex.

[2]  Zvia Breznitz,et al.  Effects of accelerated reading rate on memory for text , 1992 .

[3]  M. Chee,et al.  Relative Language Proficiency Modulates BOLD Signal Change when Bilinguals Perform Semantic Judgments , 2001, NeuroImage.

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

[5]  G. Lyon,et al.  Critical Conceptual and Methodological Considerations in Reading Intervention Research , 1997, Journal of learning disabilities.

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

[7]  J. Petrella,et al.  Cortical localization of reading in normal children , 2001, Neurology.

[8]  M. Snowling,et al.  Dyslexia — integrating theory and practice , 1992 .

[9]  P. Tallal Auditory temporal perception, phonics, and reading disabilities in children , 1980, Brain and Language.

[10]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[11]  U. Frith,et al.  Explicit and implicit processing of words and pseudowords by adult developmental dyslexics: A search for Wernicke's Wortschatz? , 1999, Brain : a journal of neurology.

[12]  U Sabatini,et al.  Supplementary and primary sensory motor area activity in Parkinson's disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. , 1992, Archives of neurology.

[13]  M. Denckla,et al.  Rapid ‘automatized’ naming (R.A.N.): Dyslexia differentiated from other learning disabilities , 1976, Neuropsychologia.

[14]  Maryanne Wolf,et al.  What time may tell: Towards a new conceptualization of developmental dyslexia , 1999 .

[15]  Tamar Flash,et al.  Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Z. Breznitz Asynchrony of visual-orthographic and auditory-phonological word recognition processes: An underlying factor in dyslexia , 2002 .

[17]  N. Goulandris Dyslexia in Different Languages: Cross-Linguistic Comparisons , 2003 .

[18]  M. Lovett Treating the Core Deficits of Developmental Dyslexia: Evidence of Transfer of Learning after Phonologically- and Strategy-Based Reading Training Programs. , 1994 .

[19]  R. Thatcher Developmental neuroimaging : mapping the development of brain and behavior , 1996 .

[20]  A Karni,et al.  Procedural and declarative knowledge of word recognition and letter decoding in reading an artificial script. , 2004, Brain research. Cognitive brain research.

[21]  R. Felton,et al.  Repeated reading to enhance fluency: Old approaches and new directions , 1999 .

[22]  Zvia Breznitz,et al.  Increasing first graders' reading accuracy and comprehension by accelerating their reading rates. , 1987 .

[23]  Anthony D Wagner,et al.  Assembling and encoding word representations: fMRI subsequent memory effects implicate a role for phonological control , 2003, Neuropsychologia.

[24]  A Karni,et al.  Skill learning in mirror reading: how repetition determines acquisition. , 2003, Brain research. Cognitive brain research.

[25]  P. Matthews,et al.  Testing for Dual Brain Processing Routes in Reading: A Direct Contrast of Chinese Character and Pinyin Reading Using fMRI , 2002, Journal of Cognitive Neuroscience.

[26]  Z. Breznitz,et al.  Effects of Accelerated Reading Rate on Processing Words' Syntactic Functions by Normal and Dyslexic Readers: Event Related Potentials Evidence , 2001, The Journal of genetic psychology.

[27]  M. Raichle,et al.  Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. , 1984, Journal of neurophysiology.

[28]  T. Zeffiro,et al.  The neural basis of developmental dyslexia , 2000, Annals of dyslexia.

[29]  Charles Hulme,et al.  Reading and Spelling : Development and Disorders , 1998 .

[30]  J N Giedd,et al.  A magnetic resonance imaging study of planum temporale asymmetry in men with developmental dyslexia. , 1997, Archives of neurology.

[31]  Karl J. Friston,et al.  Regional response differences within the human auditory cortex when listening to words , 1992, Neuroscience Letters.

[32]  Cognitive and Neurobiologic Influences in Reading and in Dyslexia , 1999 .

[33]  M. Wolf,et al.  Naming-Speed Processes and Developmental Reading Disabilities , 2000, Journal of learning disabilities.

[34]  A. Murray Harper,et al.  Regional Cerebral Blood Flow , 1979 .

[35]  A. Baddeley,et al.  Phonological short-term memory and foreign-language vocabulary learning☆ , 1991 .

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

[37]  S E Petersen,et al.  The processing of single words studied with positron emission tomography. , 1993, Annual review of neuroscience.

[38]  C. Leong,et al.  Phonological and morphological processing in adult students with learning/reading disabilities. , 1999, Journal of learning disabilities.

[39]  R S Frackowiak,et al.  A PET study of cognitive strategies in normal subjects during language tasks. Influence of phonetic ambiguity and sequence processing on phoneme monitoring. , 1994, Brain : a journal of neurology.

[40]  Richard S. J. Frackowiak,et al.  Brain activity during reading. The effects of exposure duration and task. , 1994, Brain : a journal of neurology.

[41]  Z. Breznitz Effects of Accelerated Reading Rate on Memory for Text among Dyslexic Readers. , 1997 .

[42]  J. Rumsey,et al.  Failure to activate the left temporoparietal cortex in dyslexia. An oxygen 15 positron emission tomographic study. , 1992, Archives of neurology.

[43]  H. Wimmer,et al.  Poor Reading: A Deficit in Skill-Automatization or a Phonological Deficit? , 1998 .

[44]  Richard S. J. Frackowiak,et al.  Is developmental dyslexia a disconnection syndrome? Evidence from PET scanning. , 1996, Brain : a journal of neurology.

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

[46]  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.

[47]  R Frost,et al.  Prelexical and postlexical strategies in reading: evidence from a deep and a shallow orthography. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

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

[49]  S. Bookheimer,et al.  Regional cerebral blood flow during object naming and word reading , 1995 .

[50]  A Karni,et al.  Alphabetical knowledge from whole words training: effects of explicit instruction and implicit experience on learning script segmentation. , 2003, Brain research. Cognitive brain research.

[51]  J. Millichap,et al.  Brain Activity During Reading , 1995 .

[52]  M. Bruck Outcomes of adults with childhood histories of dyslexia , 1998 .

[53]  Andrea Moro,et al.  Neural Correlates for the Acquisition of Natural Language Syntax , 2002, NeuroImage.

[54]  A. Karni,et al.  Learning perceptual skills: behavioral probes into adult cortical plasticity , 1997, Current Opinion in Neurobiology.

[55]  C. Fiebach,et al.  fMRI Evidence for Dual Routes to the Mental Lexicon in Visual Word Recognition , 2002, Journal of Cognitive Neuroscience.

[56]  John C Gore,et al.  Neural systems for compensation and persistence: young adult outcome of childhood reading disability , 2003, Biological Psychiatry.

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

[58]  Self-Paced Versus Fast-Paced Reading Rates and Their Effect on Comprehension and Event-Related Potentials , 1994 .

[59]  Steven L. Miller,et al.  Temporal Processing Deficits of Language-Learning Impaired Children Ameliorated by Training , 1996, Science.

[60]  Zvia Breznitz,et al.  Topographic measures of cerebral activity during reading of text at fast- and slow-paced rates , 2005, Brain Topography.

[61]  A. Karni The acquisition of perceptual and motor skills: a memory system in the adult human cortex. , 1996, Brain research. Cognitive brain research.

[62]  M. Bruck Word-Recognition Skills of Adults with Childhood Diagnoses of Dyslexia. , 1990 .

[63]  B. Horwitz,et al.  Phonological and orthographic components of word recognition. A PET-rCBF study. , 1997, Brain : a journal of neurology.

[64]  Steven L. Miller,et al.  Language Comprehension in Language-Learning Impaired Children Improved with Acoustically Modified Speech , 1996, Science.

[65]  T. Flash,et al.  When practice leads to co-articulation: the evolution of geometrically defined movement primitives , 2004, Experimental Brain Research.

[66]  J. Desmond,et al.  The neural basis of visual skill learning: an fMRI study of mirror reading. , 1998, Cerebral cortex.

[67]  O. Hikosaka,et al.  Long-term retention of motor skill in macaque monkeys and humans , 2002, Experimental Brain Research.

[68]  R. N. Davis,et al.  Dyslexia-specific brain activation profile becomes normal following successful remedial training , 2002, Neurology.

[69]  Zvia Breznitz,et al.  Enhancing the reading of dyslexic children by reading acceleration and auditory masking , 1997 .

[70]  M. Lezak Newer contributions to the neuropsychological assessment of executive functions , 1993 .

[71]  M. Wolf,et al.  Naming-Speed Processes, Timing, and Reading , 2000, Journal of learning disabilities.